<title>Biological Monitoring: Signals from the Environment</title>
Hermann Ellenberg et al.
A Publication of the Deutsches Zentrum für Entwicklungstechnologien - GATE , a Division of the Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH - 1991
<section>Acknowledgements</section>
Deutsches Zentrum für Entwicklungstechnologien - GATE
Deutsches Zentrum für Entwicklungstechnologien - GATE - stands for German Appropriate Technology Exchange. It was founded in 1978 as a special division of the Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH. GATE is a centre for the dissemination and promotion of appropriate technologies for developing countries. GATE defines "Appropriate technologies" as those which are suitable and acceptable in the light of economic, social and cultural criteria. They should contribute to socio-economic development whilst ensuring optimal utilization of resources and minimal detriment to the environment. Depending on the case at hand a traditional, intermediate or highly-developed can he the "appropriate" one. GATE focusses its work on three key areas:
- Dissemination of Appropriate Technologies. Collecting, processing and disseminating information on technologies appropriate to the needs of the developing countries; ascertaining the technological requirements of Third World countries; support in the form of personnel, material and equipment to promote the development and adaptation of technologies for developing countries.
- Research and Development: Conducting and/or promoting research and development work in appropriate technologies.
- Environmental Protection. The growing importance of ecology and environmental protection require better coordination and harmonization of projects. In order to tackle these tasks more effectively, a coordination center was set up within GATE in 19X5.
GATE has entered into cooperation agreements with a number of technology centres in Third World countries.
GATE offers a free information service on appropriate technologies for all public and private development institutions in developing countries. dealing with the development, adaptation. introduction and application of technologies.
Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH
The government-owned GTZ operates in the field of Technical Cooperation. 2 200 German experts are working together with partners from about 100 countries of Africa, Asia and Latin America in projects covering practically every sector of agriculture' forestry, economic development, social services and institutional and material infrastructure. The GTZ is commissioned to do this work both by the Government of the Federal Republic of Germany and by other government or semi-government authorities.
The GTZ activities encompass:
- appraisal technical planning, control and supervision of technical cooperation projects commissioned by the Government of the Federal Republic or by other authorities providing an advisory service to other agencies also working on development projects
- the recruitment, selection, briefing, assignment, administration of expert personnel and their welfare and technical backstopping during their period of assignment
- provision of materials and equipment for projects, planning work' selection, purchasing and shipment to the developing countries
management of all financial obligations to the partner-country.
Deutsches Zentrum fur Entwicklungstechnologien GATE
in: Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ) GmbH
P. O. Box 5180
D-6236 Eschborn
Federal Republic of Germany
Telephon: (06196) 79-0
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Fax: (06196) 794820
A Publication of Deutsches Zentrum fur Entwicklungstechnologien - GATE
A division of the Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ) GmbH
The authors
Prof. Dr. Uwe Arndt, University of Hohenheim, Institute of Plant Ecology. Ecotoxicologist, working on plant ecology, ecophysiology, ecotoxicology, ecology of emmisions.
Dr. Rainer Bretthauer, University of Constance, Faculty of Biology. Biologist, working on physio-chemical and biological analysis of running and standing waters, bioindication, biomonitoring, restoration of water bodies.
Dr. rer. net. Hermann Ellenberg (born 1944). Biologist, having worked extensively on population ecology of wild ungulates (roe deer), raptors (gosshawks) and passerine birds (magpies).
Prof. Dr. Barbara Ruthsatz, University of Trier, Institute of Geobotany. Botanist, having conducted studies in biology, ecology and plant science.
Prof. Dr. Lore Steubing, Justus-Liebig-University of Gielßen, Institute of Plant Ecology. Plant ecologist, having worked on various fields of environmental pollution.
Translated from the German by Gregory Woods-Schank
Cover: Dorsi Germann
Die Deutsche Bibliothek - CIP-Einheitsaufnahme
Biological monitoring: signals from the environment; a publication of Deutsches Zentrum fur Entwicklungstechnologien - GATE, a division of the Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH / Hermann Ellenberg et al. - Braunschweig: Vieweg 1991
ISBN 3-528-02302-3
NE: Ellenberg, Hermann; Deutsches Zentrum für
Entwicklungstechnologien <Eschborn>
The author's opinion does not necessarily represent the view of the publisher.
All rights reserved.
(c) Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH, Eschborn 1991.
Published by Friedr. Vieweg & Sohn Verlagsgesellschaft mbH, Braunschweig Vieweg is a subsidiary company of the Bertelsmann Publishing Group International.
Printed in the Federal Republic of Germany by Lengericher Handelsdruckerei, Lengerich
ISBN 3-528-02302-3
<section>Foreword</section>
You have acquired a publication dealing with bioindicators. It provides an overview as to the data on the environment which they can supply, and how to interpret those data. With a complex, technical-sounding topic such as this, one might well ask: What use are bioindicators in development cooperation? And the question would appear legitimate.
For several years, environmental impact assessments (EIAs) have been conducted in a growing number of countries. This instrument provides information on the anticipated effects of a project on the environment. What is particularly important in this context is to establish whether and to what extent the natural environment in which the project is to be launched can withstand those impacts.
Unfortunately, the rich body of scientific knowledge already on hand is far from reaching the point where all the effects of all substances and all interventions on all living organisms (plant, animal, man) have been established. It will be many decades before that point is reached - and even then the knowledge we have will be incomplete.
One way of observing the effects of substances is through bioindicators. This publication is designed to give the reader an overview of the type of information which bioindicators can provide, what inferences can be made on the basis of that information, and how those inferences can be put to good use.
In producing the work a deliberate attempt has been made to avoid language which is too "scientific", in order to make the book more readily accessible to readers not yet familiar with the field. Sit back and enjoy the rich diversity of nature and the signals which she sends out to us. Discover too that in your immediate sphere, in your field of activity the appropriate instruments to monitor the environment have still to be found. Perhaps doing so will spur you on to study in greater depth the complex topic of bioindicators, and to put some of the latest findings into practice.
You will find more than enough references to specialized literature in the reference sections. And should you have any further questions, then please feel free to contact the authors or the staff of GATE at GTZ.
Finally, a word of gratitude to the authors of the various contributions which make up this work. Without their commitment and patience the book could not have been produced.
Brigitte Baumer
Project advisor at the Environmental Unit of GTZ
<section>Introduction</section>
With the growing environmental problems in both the industrialized and the developing countries, suitable methods are needed for monitoring of the environment and pollution levels. In view of the inherent limitations on what can be learned from discrete physicochemical measurements, and because of the practical difficulties which these must overcome in developing countries, it is important to investigate whether "bioindicators" could be used alternatively and/or as a complementary approach for environmental monitoring in tropical and subtropical ecosystems. The aim of this volume is, accordingly, to search for possibilities and to point out approaches which could be used in future to identify and give greater consideration to ecological restraints that must be obeyed by development projects. In this context, toxin related problems are not the only aspect deserving of attention.
By necessity, each of the following articles represents nothing more nor less than an expression of the well-founded opinions of an individual who has been concerned with the topic at hand for a lengthy period of time. It would go beyond the scope of this book to include either a comprehensive discussion of individual aspects with consideration of all of the relevant publications, or a synthesis of all five papers. We have endeavored, above all, to point out possibilities. They are intended to give the reader inspiration and ideas, if he or she is involved in dealing with the consequences which human activities have for the environment and environmental monitoring.
Nearly all of the experts contacted have made generally acknowledged contributions to the use of bioindicators for specific applications. However, most of these men and women have expressed basic skepticism and disapproval towards attempts to indiscriminately generalize biological monitoring techniques that have proven their worth under specific environmental conditions. In particular, they have reservations towards the attitude that biological monitoring is primarily a relatively inexpensive method of monitoring temporal and spatial trends in environmental change. This attitude may be justifiable up to a certain point, provided that precisely defined field and laboratory methods are available. However, this is normally the case only after lengthy and staff-intensive research work, often involving intensive use of expensive equipment, has already been performed. Knowledge derived from such efforts exists in only a small number of countries. There is an even greater lack of
essential prerequisites in many developing countries compared to some industrialized nations, especially as concerns knowledge of species and their natural history.
The most urgent task thus appears to be the establishment of and continuous support for research teams whose members possess knowledge of regional sociological, economic and ecological factors, as well as an extensive theoretical background. Even in Central Europe, few such research groups exist. They have already been publishing their results for many years, pointing out the irreversible ecological changes which could be brought about within the space of just a few human generations. Yet it was not until fairly recently that their warnings began to be taken seriously, and for this to happen political movements at the so-called grassroots level have had to force our so-called leaders to increasingly take them into account in their well-meant planning and forecasts.
Politics, industry, legislation and the classical natural sciences are all dominated by the belief that it is fundamentally possible to demonstrate clearcut relationships between causes and effects. The sad truth is, however, that monofactorial causal relationships are rare in ecosystems. As a consequence of this, ecologists usually look upon scientific results differently than the above-mentioned groups. From their experience with complex, highly intricate ecological structures, ecologists tend to take a cautious, perspicacious and reserved approach to things. Only in exceptional cases can the immediate effects, and much less the long-term impact, of direct and indirect intervention in ecosystems be predicted or demonstrated with the certainty and clarity demanded by politics, industry and legislation.
In societies that are characterized by competition, vacuums - even those of an argumentative nature - are quickly occupied by groups of individuals whose actions are governed first and foremost by what is likely to further their own personal advantage. This is no different in nature; no unoccupied ecological niches are left vacant for idealistic reasons there either. Instead, if at all possible they are filled and exploited. The yardstick for measuring the success of such "action" in nature is whether the organisms in question manage to produce young that are in turn capable of reproduction. At the limits of the capacity of a biotope to support a given species, this aim is striven for by the parent generation with enormous expense of energy, and is accompanied by losses in the next generation that are difficult to accurately predict in any specific instance. Even the most highly specialized "C strategist" ) maximizes the number of its offspring as far as possible under the
given circumstances.
It can thus be seen that a number of practical problems are urgently in need of solution in order to permit a consensus to be reached by all concemed on the results of ecological research. Optimization of the future limits to be placed on utilization of natural resources is something only human beings can strive for, and then only if understanding of ecological relationships goes hand in hand with the achievement of compatible behavior at the sociological, economic and political levels. If the individual is to preserve the high status which has hitherto been awarded to him in human society, then this cooperation must be put into practice much more effectively than has been the case in the past. In nature, by contrast, need and misery are everyday events.
The author would like to thank Dr. PLUSCHKE and with him GATE and the Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH, who organized this project, for giving him the opportunity to present his points of view here. He also had occasion to personally visit and/or hold lengthy telephone conversations with a large number of experts in these and related fields. In addition to all of the authors of this volume, I owe special thanks to the following persons:
Prof. Dr. H. BICK, Bonn; Dr. R. BRANDL, Bayreuth; Prof. Dr. E.F. BRUNIG, Hamburg; Prof. Dr. Heinz ELLENBERG, Gottingen; Dr. Lutz FAHSER, Hamburg; Dr. habil. E.J. FITTKAU, Munich; Dr. H. JUNGIUS, IUCN/WWF, Gland, Switzerland; Dr. JUNK, Plon/Manaus; Prof. Dr. G. KAULE, Stuttgart; Prof. Dr. H. KLINGE, Plon/Manaus; Prof. Dr. R. LEWIS, Saarbrucken; Dr. C. MARTIN, WWF Switzerland, Zurich; Prof. Dr. H.-J. v. MAYDELL, Hamburg; Dr. U. NAGEL, WWF Switzerland, Zurich; Dr. H. PAPKE, Julich; Dr. Joseph REICHHOLF, Munich; Prof. Dr. K.-F. SCHREIBER, Munster; Prof. Dr. H. SCHWOERBEL, Constance; Dr. W. STOEPPLER, Julich; Prof. Dr. H. ZWOLFER, Bayreuth.
These contacts, study of current literature, and travel for the purpose of this project took place for the most part during the fall and winter of 1984/85. This is also true for the majority of the coauthors. Only Dr. Bretthauer, the limnologist, was later invited to present a contribution on his field of specialization. The authors' papers were discussed at two workshops, in 1985 and early 1988, organized by the GTZ. Appropriate coverage of the literature up to about 1984 has been achieved in the majority of the contributions. Updating was possible only in some cases. Nevertheless, the main lines of thinking and of practical work developed and diversified particularly rapidly during the late seventies and early eighties, most of which are referred to by the authors. Therefore we think that a publication today is worthwhile in that it may encourage readers the world over to focus their interest on the dwindling natural resources of life. It is hoped that it will stimulate
them to ask questions as to how to become aware of and monitor change and the impacts of pollution in ecosystems, and how to help nature persist and recover in spite of growing human populations and so-called developments in technology and agriculture which all too often burden our ecological environment, the environment which at the same time is the basis of our lives.
<section>Bioindicators and Biological Monitoring</section>
by Hermann Ellenberg
<section>1. Abstract</section>
"A bioindicator is a related group or community of organisms whose occurrence or an easily detectable trait of which can be so closely correlated with certain environmental conditions that it can be utilized as a pointer or quantitative test." - In this article, the attempt is made to present the interrelationships between the environment and indicators within the context of ecosystems in an easily understandable manner. In doing so, examples are provided, concentrating on the biological monitoring "levels" of the ecosystem and the biocenosis, and on the "levels" of populations and individuals. Higher and lower reference levels - e.g. those of landscapes and biomes, organs, cells, biochemistry and genetics - are dealt with here only peripherally, without ignoring the fact that ecosystemic relationships and thus also biological monitoring by no means exist only within isolated levels, instead running across all of the defined reference levels, and secondly keeping in mind
that the other authors of this volume (ARNDT, BRETTHAUER, RUTHSATZ and STEUBING) concentrate on other aspects not treated here.
As far as possible, examples are presented to thoroughly illustrate the use of changes which pollutants released into the environment cause in vegetation and vascular plants, these representing the basis for other life forms, and of phenological mapping for agricultural land-use planning. Shifts in the competitive relationships among individuals and populations provoked by anthropogenically induced modifications in environmental conditions are recognized as being essential factors. If correctly interpreted, they can reveal organisms suitable for use as bioindicators. A lengthy section is devoted to the use of birds as biomonitors of environmental pollution. Here, the attempt is made to demonstrate that, with appropriate standardization, well-defined "environmental specimens" are suited for monitoring of patterns and trends of impact or pollution, integrating by their way of life entire spans of time and geographical areas. These living organisms may be particularly
well-suited for interpolation between high-input physicochemical measurement stations (which nevertheless are necessary for "calibration" of bioindicators). The future risks of continued pesticide application in agriculture and to combat disease vectors are also dealt with; here, development of resistant strains, undesirable side effects at all ecosystem levels, and the availability of soil, water and air for sustained use are the crucial parameters.
The general theses advanced in this article can be roughly paraphrased as follows:
- Certain bioindicators can be absolutely quantified by calibrating them with physicochemical measurements. However, it is vital not to allow biological monitoring techniques to remain restricted to physicochemical residue analysis. This would rob them of their unique nature and of the possibilities which they offer for providing much-needed and frequently called-for independent evaluations.
- Bioindications - i.e. that which is indicated by organisms used for biological monitoring - can only be correctly interpreted and predicted on the basis of thorough understanding of ecosystems.
- Understanding of ecosystems must be derived from knowledge of species, and from local measurements and experiences.
- Working groups with an extensive theoretical background must be established to compile and process local and/or regional ecological data, and long-term support must be given to them. This is not primarily a research task; above all, it is important in connection with development cooperation in the developing countries (and, to a large extent, in the industrialized countries themselves).
- For the good of all, greater environmental awareness must be achieved in the face of powerful egotistical national end group interests. In view of the urgent necessity to cease squandering and destroying the world's natural resources, isolated and time consuming pilot projects are not enough.
- With each year that passes without taking action, the organizational effort required to establish such a "fire brigade" grows. Yet, we have at our disposal here a unique opportunity to link idealism and economic interests in the pursuit of similar goals for the good of the greater whole.
- Human intervention in and utilization of ecosystems are not only causing the balance to shift in their intricate structure of assimilation, predation, parasitism and dissimilation, but are also and above all endangering the continued survival of those organisms that are relatively long-lived and large in size and which reproduce at a slow rate among animals, the risk is greatest to those that roam over large areas. Biological monitoring with and of such organisms is therefore of overriding priority, especially since human beings - although themselves relatively long-lived and large in size - are only available to a limited extent for experiments and specimen collection of all kinds.
<section>2. The situation</section>
LIFE IN ECOSYSTEMS IS NOT
"NECESSARY" BUT "POSSIBLE" ....
..... IF AND/OR WHERE FUNDAMENTAL
REGULATORY PROCESSES ARE IN OPERATION
Basically, life need not necessarily exist if and/or where certain fundamental regulatory processes are in operation, but these are nonetheless prerequisites for it, without which life would be impossible. Within an ecosystem, energy, matter and information carriers interact in an intricate web of processes (see Figure 1). Changes in one compartment necessarily induce reactions, i.e. changes, in others. From an economic point of view, this can entail changes which are positively assessed, but it can also detract from or even endanger the usefulness of ecosystems, populations or individuals. Not infrequently, it is quite difficult to detect spatial and/or temporal trends in the network of interacting ecological factors amidst the regular, episodic or catastrophic oscillation of individual factors. The rate at which changes take place in ecosystems is also modified by adaptation and selection processes at the levels of individual and population. Our understanding of the
processes involved is, at best, only partial, and the search for keys to the workings of ecosystems tends to focus on those few aspects that are known, although in many cases their discovery has been accidental. The difficulties are compounded by the fact that one and the same problem can appear in a different light depending on the point of view and perspective (Figure 2). Consequently, any contribution towards solving a specific problem, including scientific endeavors such as ours, is inevitably one-sided. A synthesis must be sought at the sociopolitical level, as I have already stressed above in the introduction.
<section>3. The problem</section>
Biological monitoring can be described as any method that makes use of the reactions of life at any level - from the subcellular dimension to entire biocenoses - for identifying and/or characterizing substances and energy cycles in its environment. In this sense, biological monitoring is nothing more than a new word for more or less well known practices (STOCKER 1981). For this reason, STOCKER would like to restrict the concept of "bioindication" to the measurable reactions of biota to anthropogenically induced changes in environmental conditions. I believe that this narrowing of the concept goes too far. For certain applications it may be a feasible definition (e.g. studies of environmental pollution), but it excludes monitoring of ecosystems in their natural state.
This can be illustrated by the following example: the phenology of plants, i.e. the science of the interrelations of climate and periodic biological phenomena such as budding, flowering, etc. of fruit trees can be applied to characterizing the growing conditions in greatly varying landscapes. According to STOCKER's definition, however, only those fruit trees can truly be used for biological monitoring that grow inside of a human settlement, in front of a house wall on which the sun shines, or in a cold air mass which has accumulated alongside a road or an elevated railway line, and consequently blossom earlier or later relative to the "unmodified" microclimate in the same area.
As a rule, destruction of forests goes hand in hand with the disappearance of rare forest animals. The opposite occurs only in exceptional cases: namely those in which the disappearance of rare animals dependent on certain forest structures causes the demise of these same structures.
Here is an example from Central Europe: in order to find large, old oaks, it is not usual to begin by searching for the rare middle-spotted woodpecker (Dendrocopos medius); however, when middle-spotted woodpeckers - which in Central Europe are strongly dependent on old oaks with their thick, furrowed bark - are demons/ratably absent, in spite of the fact that such trees occur over a large area, investigation of the causes of their absence can sometimes lead to an improved understanding of ecological interreactions.
From a practical point of view, bioindicators or indicator species are sought which permit conclusions to be drawn on the situation or changes in ecosystems, providing information that would be difficult to obtain and quantify in any other way, or at least not as easily, as quickly, or as cheaply.
<section>4. Definitions</section>
At a meeting of experts held by the German Research Society (Deutsche Forschungsgemeinschaft) in May 1975, the following definition, proposed by ELLENBERG sen., was discussed and agreed upon:
"A bioindicator is a related group or community of organisms whose occurrence or an easily observed behavioral trait of which can be so closely correlated with certain environmental conditions that it can be utilized as a pointer or quantitative test."
This definition is likely to satisfy both practitioners and discerning observers. Nonetheless, it calls for observable facts to be corroborated by measurements or experiments.
REMMERT (1978) introduces two additional demands to the discussion when he writes (p. 232):
"The basic biochemical processes are the same in [many] organisms, and as a result it seems reasonable to utilize organisms as bioindicators that react faster than human beings to environmental toxins, and which therefore can be used to detect changes in the environment induced by human activities which could become dangerous to the human beings themselves."
Providing that the term "environmental toxins" is not understood too narrowly, this definition appears to me to be usable, especially with regard to the topic of this article (see introduction). However, REMMERT's definition lacks a number of important aspects which are covered by the first definition.
As already mentioned above, STOCKER, a highly reputed East German theoretician and expert on nature conservation, defines "bioindication" in a particularly narrow manner: "a time-dependent, sufficiently sensitive indication of anthropogenic or anthropogenically modified environmental influences with the aid of changed parameters (measurable attributes) of biological objects and systems in relation to defined reference conditions." Accordingly, he defines bioindicators as "biological objects, compartments and ecosystems that provide bioindications." I have already expressed my views on these definitions in the previous chapter.
A concise and easily grasped definition was attempted by Paul MULLER in 1980. According to his interpretation, biological monitoring (bioindication) involves "the decoding of the information content of biosystems for the purpose of evaluating a given space or domain." Apart from its failure to mention monitoring through time or possibilities of utilizing test organisms, this definition would appear to be broad and apt. Nevertheless, it has the drawback of lacking the practical dimension which is clearly expressed in the definition accepted by the German Research Society, although this very lack could be positively interpreted by some researchers: an understanding of the interactions and structures of ecosystems must be the basis for the practical use of bioindicators and biological monitoring. This aspect is also incorporated into the definition of the German Research Society. We therefore give preference to it.
<section>4.1 Relationship between the "environment" and "indicators"</section>
An essential component of any attempt to define bioindications or biological monitoring is that it must stress a clear correlation between the environmental attribute under study and the reaction of the studied organism on the one hand, and that the organism and/or the changes which it undergoes must be relatively simple to detect. An important prerequisite for the success of biological monitoring itself is that the specific working goal in each case be clearly and precisely formulated. "Environmental quality" for example, a concept which represents the sum total of a large number of isolated assessments, is a much too diffuse objective for scientifically practiced biological monitoring. The many subjective evaluations which this objective calls for must be derived from the political domain, including the politics of individuals or the researchers themselves.
If, however, biological monitoring is only possible on the basis of painstaking and expensive studies, then there is little demand for it. Besides being very time-consuming and requiring a great deal of patience, such studies must rely on a high degree of commitment and substantial financial support as well. Many researchers have often managed this all by themselves - this has occurred much more often in Central Europe, Scandinavia, Great Britain, Japan, Canada and the United States than in most of the developing countries of the dry and moist tropics, in which up to very recently only a relatively small number of research teams - predominantly from the first-mentioned countries have conducted relevant studies. Yet, much too little use seems to have been made even of their results and experience.
We are convinced that many of the goals of environmental assessment and monitoring could be achieved more efficiently than by elaborate research programs with expensive test equipment' namely by following these two steps:
1. Arranging of meetings between experts with the aim of elaborating clearly defined approaches.
2. Consulting and employment of individuals with relevant expertise and experience. These are often able to recognize and demonstrate connections, causes and effects on a broader basis - in the geographical sense as well - than could ever be achieved by technologically oriented programs. A small number of measurements performed at critical points can then be enough to confirm the statements made by such experts or to tie them into an absolute frame of reference.
We are aware of the particularly great difficulties confronting many developing countries in the search for persons with such thorough knowledge of species and biocenoses. The only possible answer is to train more such persons, to /et them gain experience, and to grant them continuous support.
The economic exploitation of areas and entire regions by human beings is normally governed by the seeming objectivity of economic or political "givers" and "compulsions". Until quite recently, for all practical purposes only a few "callers in the dark" were engaged in calling attention to ecological considerations and interconnections. The land-use and settlement policies practiced by Brazil in the Amazon basin, for example, or Indonesia's resettlement program in Borneo (transmigrasi) are creating more problems than they solve in both the long and the short term, because fundamental facts about the general nutrient poverty of the soils and their extremely low capacity for capturing and holding introduced nutrients have been given too little consideration by the government agencies responsible for planning and promotion of such programs (ENGELHARDT and FITTKAU 1984; BRUNIG, KLINGE, v. MAYDELL: personal communications). The fact that the incredible species diversity found in
tropical rain forests is in actuality a direct result of this very lack of nutrients under otherwise optimum conditions as regards temperature, light and water availability was not realized until relatively recently (FITTKAU 1984). Even in Central Europe, the vast majority of plant species are only able to compete under low-nutrient conditions (ELLENBERG jun. 1983): within the limits imposed by the other ecological factors, they are "just able" to tolerate the lack of nutrients, but have difficulty in shouldering aside their competitors because - and this holds for all plant species concurrently present on such sites - the chemical prerequisites are lacking.
<section>4.2 Qualitative and quantitative biological monitoring</section>
Qualitative and quantitative bioindicators can be distinguished. At least the qualitative ones have long been used for some applications. These approaches involve simple "yes/no decisions" based on the presence or absence of certain species or combinations of species, or on attributes that prominently change in reaction to certain environmental influences, e.g. many lichen species in response to air pollution. This category also includes the "indicator values of plants" defined by Heinz ELLENBERG (1950-1983). Different plant species are useful as indicators of light intensity, temperature, continentality of the climate, soil moisture and soil pH level, nitrogen availability, soil salinity and/or heavy metal concentrations, etc. It is advisable not to make use of merely one of these indicator species, since the occurrence or absence of all of them is governed by more than one environmental factor, and in addition several species that react in a similar way can serve to round
out and differentiate the picture.
This brings us to quantitative bioindicators. Quantitative biological monitoring always requires considerably greater labor inputs than qualitative monitoring - independent of the research effort which must be devoted beforehand to interpreting the situation. In the above example, at least the occurring plants must all be identified at a given site in order to determine which combination of indicator values applies. For qualitative monitoring, it would have been sufficient to know about a few characteristic plant species. Quantitative biological monitoring always involves measurements of some kind. This requires a certain amount of organizational effort. In order to ensure comparability of the collected data, the same attributes must be observed in individuals of the same species in the same general physiological condition at the same time, but at different places. Quantitative biological monitoring therefore calls for the existence of a particularly well-defined set of
procedures, or else the importance of the problem to be solved must justify the greater expense and labor. Biological monitoring must always be relatively simple, even elegant, since there will otherwise be little demand for it in our technologically oriented society.
In order to utilize the advantages of biological monitoring, namely sensitivity, differentiability, descriptiveness, ecological relevance and, above all, the possibility of identifying and detecting changes in environmental factors more quickly and more cheaply than is feasible by chemical or physical analysis alone, in my opinion two aspects are particularly important:
1. As already mentioned, there must be a clear and scientifically proven correlation between that which is to be indicated on the one hand and the indicator or its reaction on the other hand.
2. Discerning experts on the species and/or biocenosis involved, possibly including physiologists or analytical chemists, must be available who are able to determine and assess the presence or absence of organisms and their reactions - if necessary with the aid of technical apparatus and/or chemical or physiological methods. In my opinion, the knowledge and experience of such experts are neither utilized nor supported to the extent which they deserve in our technologically oriented society.
<section>4.3 Bioindicator types</section>
Bioindicators in the broad sense of the word can be usefully subdivided into three groups: indicators or pointer species in the narrow sense, so-called "biomonitors", and test organisms (e.g. BICK 1982). Provided that their ecology is sufficiently well understood, conclusions can be drawn from the decline or increase of indicator species in an ecosystem on the effects of biotope changes, climatic changes, and in some cases of pollution as well. Biomonitors are organisms that assimilate certain toxins in the environment over a period of time (plants) or also in different places (mobile animals), possibly accumulating them in their tissues. They can then yield information on the geographical pattern and temporal trend of concentrations of these toxins in the environment. Such biomonitors can be "passively" utilized by observing their natural occurrence. The alternative is to "actively" expose individuals or populations of them to the pollutants under study and to monitor their
reactions. Either "sensitive" or "cumulative" indicators can be used for both approaches. In the case of "sensitive" indicators, for trivial reasons the sensitivity of the reaction - in addition to its specificity - is of enormous importance for their practical application. Cumulative indicators assimilate toxins in their tissues not just over the course of time (such as plants and sessile animal species), but also over significant spatial ranges, such as animal species whose individuals roam over large areas, migrate, or defend large territories. In practice, when using cumulative indicators to obtain a description of temporal or spatial trends in the effects of pollution, an extremely great variability of pollutant concentrations is typically encountered in individuals of the same species in the same study area. Not infrequently, the measured levels can range over two to three orders of magnitude, even among individuals taken from a single square kilometer of land (e.g.
MAY and ELLENBERG 1985).
Analysts who think in terms of physics and chemistry, as well as many specialists occupied with analysis of environmental toxins in the tissue of plants and animals destined for human consumption, attempt to escape from this dilemma by taking into consideration as large a number of specimens as possible, with the aid of which mean values for concentrations can be "confirmed" by applying statistical criteria. So far, too little study has been devoted to the causes of such variability. My coauthors and I have prepared examples of this which are reported on further below.
For many pollutants, analytical techniques are available today which are capable of detecting concentrations as small as a few parts per billion (ppb). Even at such low concentrations, reproducibility of the analysis results within 10% or 15% at the most is aimed for (STOEPPLER, personal communication). In view of the potential sources of error in connection with specimen collection in the field under ecosystem conditions, such precision is far greater than what can presently be achieved by practical environmental monitoring, the success of which - in the final analysis - must be measured by observing living organisms. It is therefore urgently necessary to devote considerably more attention than has hitherto been the case to standardizing specimen-collection procedures within the scope of biological rnonitoring of pollution levels. and to give more consideration to ecosystemic interrelationships. This fact is now also receiving increasing recognition in the Federal Republic
of Germany in connection with the establishment of an "environmental specimen bank" (LEWIS et al. 1983; LEWIS 1984).
Various investigators have sought a way out of this dilemma for years, resulting in - above all in the field of active monitoring - successful standardization efforts worthy of recognition, e.g. for exposure of transplanted lichens (Hypogymnia physodes) and standardized grass culture methods (Lolium multiflorum). In other articles contained in this volume, ARNDT and STEUBING report in greater detail on these and other procedures. Such standardized exposure methods for active monitoring appear to be suitable for bridging the gap between readily reproducible laboratory measurements and the intricate structure of ecosystems. The latter is difficult to apprehend, but an understanding of it is nevertheless of paramount importance for assessing the impact of adverse environmental influences.
Thus, the third category of biological indicators, namely test organisms - used in experimental studies on the environmental compatibility of certain substances, which have subsequently been developed into standardized test procedures - are likewise of only limited usefulness from an ecosystemic point of view. As one moves from indicator organisms through the various categories of biomonitors and on to the test organisms, the precision of the information provided generally increases, while at the same time its ecological relevance normally diminishes.
In view of the progressive chemical contamination of our environment (RAT VON SACHVERSTANDIGEN FUR UMWELTFRAGEN 1978; BALK and KOEMAN 1984; BIEDERMANN et al. 1984), the entire range of biological monitoring approaches, from test organisms all the way to indicator organisms, should be applied by several regionally specialized working groups. Of importance for mutual understanding among the individual researchers, who, for methodological reasons, are of necessity highly specialized, is that the various different approaches be coordinated within the framework of a single organization, the leadership of which should remain constant, at least in the medium term. Endeavors of this kind are now being considered in the Federal Republic of Germany in connection with the national "environmental specimen bank" established in 1985. The activities of this bank are systematically directed - consistent with the ecosystem research and biological monitoring approaches discussed above -
towards the collection of biological specimens in so-called "main research areas", in which multifaceted monitoring, observation and research programs are devoted to obtaining the necessary background information for the interpretation of changes in ecosystem processes and, as far as possible, making this data available to others.
For the utilization of the results of such environmental monitoring in the political realm, it will be indispensable to place the burden of proof on potential polluters: only in rare cases is it possible to demonstrate causal ecological relationships beyond a shadow of a doubt in the sense of the classical natural sciences. Even if there are merely plausible reasons to suspect that the environment is being permanently harmed by pollutant emissions or seriously altered in other ways, great attention must be focused on the matter. In cases of doubt, those responsible for the discharge of pollutants into the environment or those who employ new methods for exploitation of the environment would have to be responsible for proving that their activities are not causing any permanent harm to the affected local ecosystems and the relevant larger-scale or global natural transport systems (water, air, organisms).
In this connection, it is also necessary to call for testing of imported biocides in developing countries, at least in various different ecologically distinct regions on locally relevant biota under locally typical ecological conditions. In 1981 only 24 countries had a strict approval and control system for the use of pesticides, backed by legislation, among them the Federal Republic of Germany. In 81 countries there were no known restrictions of any kind. An additional 6 countries were in the process of introducing such a system, and 26 governments failed to enforce existing regulations (BATES 1981). It would appear that this situation has not substantially improved since then.
<section>4.4 "Levels" of biological monitoring</section>
Bioindications, i.e. the reactions of life to their environment and/or changes in it, can be hierarchically ordered using the following scheme, borrowing from SCHUBERT 1979 and the symposium on biological monitoring organized by him in Halle in 1979 (SCHUBERT and SCHUH 1980) and from the organizational principles used in ecological science:
Landscape
Water bodies
Ecosystem
Soils
Biocenosis
Species
Population
Social groups
Individual
Organ
Cell
Biochemistry
Genetics
This list represents only one of many possible organizational approaches. Within such a hierarchical system, inductive and deductive research efforts are mutually dependent upon one another. The articles in this volume have been tentatively arranged in an order corresponding to the above list. Based on an understanding of higher levels, "bioindications" at one or more of the lower levels can often be predicted and scientifically examined.
Example: the introduction of nutrients to ecosystems leads to changes in the ways in which the populations of different species within a biocenosis compete with one another. Provided that the ecological requirements and tolerances of the individual species are known, changes in the species distribution can, to a certain extent, be predicted in the form of reactions to the increased nutrient availability. The prerequisite for this is that the requirements and tolerances of the individual species first be studied at many levels from population down to biochemistry and genetics (cf. section 5.2.1).
Such varied information, either on utilized species or species that are not directly utilized, is rare in the developing countries however.
Even in those parts of Central, Northwestern and Northern Europe that have been thoroughly studied for decades using a diversity of different approaches, such syntheses are the exception rather than the rule. A study of the invertebrate fauna of a relatively clean mountain stream up to 2 m wide conducted by the researchers of the Limnological Station in Schlitz, Hesse, has still not been completed after more than three decades of continuous work (FITTKAU, personal communication). The situation is similar on the island of Barro Colorado in a lake created by the Panama Canal, although it spans only a few square kilometers, where systematic biological, biocenotic and ecological research studies have been under way for longer than anywhere else in the tropics.
As can be seen, biological monitoring must always concentrate on practicable, often relatively narrow sections within the mentioned hierarchical system.
By the same token, it is impossible to stress too emphatically that the results of biological monitoring studies can only be reproduced within certain predefined limits. Such limits can be sought, for example for planning or rural development purposes, in the form of a geographically defined "organizational scheme of natural zones" like that developed by MEYNEN and SCHMITHUSEN for the Federal Republic of Germany in the years up to 1962, and like those which have been drawn up since then and developed further for many other countries.
As a rule, a number of possible causes can be found for bioindications at relatively low hierarchical levels. The conclusions drawn from such a bioindication must therefore be repeatedly checked at other levels. This applies at the biochemical level, as well as at those of ecosystems and landscapes. This is illustrated by two examples:
The diminished phosphatase activity caused by exposure to SO[2] in lichens within the scope of active monitoring would appear to be suitable for early detection of SO[2]-induced injury (SCHMID and KREEB 1975). However, this phenomenon is a relatively nonspecific reaction that can also be caused by other stress factors. Consequently, this reaction is only suitable for interpolation within gradients, the quality of which is already known from independent studies.
As a second example, I would like to briefly mention the forest decline being caused by air pollution in Central Europe, which has been the subject of intensive discussion during the last few years. The most important symptoms, namely discoloration or necrosis of needles or leaves, defoliation, reduced net primary production, etc., can be regarded as a syndrome in which an important role is played by a worsening of the supply of water to the assimilation organs. A number of possible causes for this are being discussed today. So far, there is only widespread agreement that the observed damage cannot be explained without air pollution. There are divergent opinions on chiefly which specific atmospheric contaminants are contributing to this situation, and on specifically how damage takes place. In view of the diversity of conditions in the affected landscapes and ecosystems, a uniform reaction can hardly be expected, even if the pollution levels are comparable. Studies that go
beyond specific aspects for which cause and effect can be closely correlated are still few and far between. Far too few ecosystem studies are also included in bibliographies. For example, SCHRADER et al. 1984 list nearly 800 titles but fail to mention the original publications by the mycorrhizal specialist F.H. MEYER, although he also published in journals widely read by foresters. MEYER recognized that the introduction of additional nitrogen to ecosystems - one of the factors involved in acid pollution (e.g. by "acid rain") causes a shift in the competitive equilibrium between mycorrhizae and forest trees, at least on acidic and hitherto relatively nutrientpoor sites. Consequently, the water stress syndrome mentioned above also becomes understandable in the light of other relationships, e.g. eutrophication (cf. ASMAN et al. 1987). Which of these aspects plays the greater role in causing the observed symptoms under the ecological conditions at a given site can only be
determined by analysis in each individual case.
<section>5. Examples</section>
<section>5.1 The landscape and biome levels</section>
Traditionally, living organisms and biocenoses are utilized to characterize and classify landscapes and natural zones. Designations such as rain forest, savanna, desert, macchia, broad-leaved forest, taiga and tundra - to mention only a few examples - are associated not only with pictures of the structure and dynamics of the vegetation, but also with a variety of other information on climate, geology, geomorphology, soils, water, fauna and the role played by human beings within this system as well as the possibilities for utilization of such landscapes. There is no need to define these aspects more precisely. It is nevertheless important to point out here that fundamental misunderstandings can arise if what is known about a familiar biome is transferred uncritically to another, such has often been done during the last centuries and decades by European colonists and their descendants, e.g. regarding the agricultural use of soils on which tropical rain forests are able to
thrive (WEISCHET 1980; IUCN 1983; ENGELHARDT and FITTKAU 1984).
<section>5.2 The ecosystem and biocenosis levels</section>
5.2.1 Changes in the spectrum of vascular plant species under the influence of fertilization and nutrient input by immission in Central Europe, and their impact on climatic parameters and fauna
5.2.2 Phenological mapping as the basis for planning of agricultural land use
The "occurrence or easily detectable behavior" of certain organisms can be easily interpreted by an expert as providing an indication on the occurrence or behavior of other species that are difficult to observe. This statement can also be applied to potential agricultural or other uses. The following two examples illustrate this.
5.2.1 Changes in the spectrum of vascular plant species under the influence of fertilization and nutrient input by immission in Central Europe, and their impact on climatic parameters and fauna
Plants represent the nutritional basis of and provide the biotope structure for animal life, including human beings. Usable written documents listing the species occurring in different landscapes and dating back further than about 1800 are rare, and only a limited number exist from the 19th century. In many developing countries, efforts to complete such lists of species did not begin until very recently. There, more in-depth studies on the possibilities for use and ecology of the listed species are today still the exception. One of them is that by v. MAYDELL (1983) on the trees and shrubs of the Sahel.
Decades of preliminary studies and the experiences of a large number of researchers provided the basis for two different, completely independent quantitative surveys of the vascular plants of Central Europe: the works by SUKOPP et al. (1978) and ELLENBERG sent (1979). In the developing countries, within the foreseeable future it will be possible to attain such thorough knowledge on only a small number of selected areas, although even this would be an important achievement. SUKOPP and his coworkers classified the vascular plant species in their study area according to the extent to which they are endangered. They distinguished among unendangered species, endangered species, highly endangered species, species threatened by extinction. and extinct species; an additional category is that of the potentially endangered species, which I did not consider in my own evaluation (see below).
Except for species that are restricted for natural reasons to just a l`ew sites, these levels of endangerment document a trend over the course of time. If ecological factors enter into consideration as the causes of this trend, then they must have had a greater impact on the endangered species than on the others. It therefore appeared meaningful to compare the ecological behavior of the unendangered species with that of the endangered species. For the purposes of this comparison, the indicator value ranges, ) of species with similar sociological behavior (ELLENBERG sent 1979) were chosen as being suitable. The aim of this comparison was to identify current or potential ecological bottlenecks that could endanger species. The results clearly revealed implications for endangered animal species, for other plant groups, for the understanding of important aspects of the forest decline mentioned above, and for human beings themselves (ELLENBERG jun. 1983, 1985, 1986 a, b, 1987;
KAULE and ELLENBERG 1985).
The results can only be roughly sketched here. If all of the species are considered, without distinguishing between endangered and unendangered species, then in absolute terms by far most of the species can be found on sites that are poor or very poor in nitrogen. It is only on such poor sites that they appear to be capable of competing, although they usually - e.g. when individual plants are raised in nurseries - grow better in soil high in nitrogen then on those sites where they naturally occur as a result of interspecies competition. Under natural conditions on sites in Central Europe with a better supply of nitrogen, in nearly all cases broad leaved forest species prevail, thus depriving the frequently small "hunger artists" of light. In the past, under the influence of human activities forests were encroached upon and many tree species actively displaced, while others were favored. At the same time, overgrazing and primitive farming methods depleted most sites of
important nutrients. In the long run, therefore, up until around 100 years ago the "hunger artists" among the plants were at a distinct advantage in Central Europe. This situation has changed drastically; active fertilization practices, as well as an influx of nutrients from the air - which in recent years has contributed between a tenth and a third as much nitrogen as full-scale agricultural fertilization (200 kg of N per year per hectare) - have caused, above all since the end of the Second World War, eutrophication of virtually all sites in Central Europe (MOHR 1986; ELLENBERG jun. 1987, as well as earlier publications by the same author). Plant species with higher nitrogen requirements that previously had only limited possibilities and/or survived only at isolated locations are now able to grow quickly and densely to considerable heights in many areas, thus cutting off the supply of sunlight - the source of energy for all green plants - to the many species that tolerate
low nutrient availability but are, for this very reason, light-demanders.
In agriculture, this trend has been actively promoted by fertilization and other practices aimed at increasing the yields of crop plants. In areas that are not directly fertilized, particularly the forests, moorlands and semi-dry heathlands, over a lengthy period of time contamination from the air- the primary sources of which are combustion of fossil fuels and ammonia emissions from intensive livestock keeping and treatment of fields with slurried animal excrement - has resulted in a similar situation: the tree growth increments measured in the 1960s and early 1970s, for example, exceeded all of the standard values which had been recorded in yield tables during the 1920s and 1930s (SEIBT 1981; SCHNEIDER and LORENZ 1986). As a consequence of this, on nearly all Central European sites the highly light demanding species have no longer been able to compete. This fact is expressed quite clearly in the so-called "red data lists" (BLAB et al. 1983).
Taken as a whole, the class of "red data list species" among the plants, i.e. those that are more or less greatly endangered in the sense defined by SUKOPP et al. (1978), is much more prevalent on sites poor in nitrogen than the class of species not considered to be endangered. At the same time, most of the endangered species require significantly more light than the corresponding unendangered species with similar social behavior.
Beneath a closed canopy of leaves, regardless of whether it is formed by arctic cushion plants, e.g. Loiseleuria procumbens (CERNUSCA 1977), by a well-fertilized dense wheat field, or by a closed forest stand, at least during the daylight hours there is a somewhat moister and significantly cooler microclimate than outside of such stands or above ground which is not as densely covered by plants. Sites with a dense plant cover are heated to a lesser extent by energy-rich sunlight falling upon them than sparsely covered or open sites. Moreover, dissipation of energy, especially at night or during the winter, is greater from open sites than from sites with a plant cover. For this reason, endangered plant species as a whole can also be expected to respond differently to temperature, moisture and climatic continentality than the unendangered species, as well as to the already discussed ecological factors, namely nitrogen and light.
An analysis of the distribution of endangered and unendangered species over the corresponding indicator value gradients from cold to warm, oceanic to continental, and from dry to wet, confirms the expectations: in all investigable major ecosystems, whether forested or not, the endangered species turn out to have much greater warmth requirements, to be more strongly adapted to a continental climate, and to exhibit far greater tolerance of drought than the unendangered plant species. Since these distributions are basically the same in fertilized ecosystems and in those that are not directly fertilized, one is forced to the conclusion that, at least in Central Europe, over the years an influx of nutrient-rich contaminants into the environment mainly as immission and deposition via the air has made a major contribution to this general eutrophication tendency.
a)
"?" not known; "x" indifferent
"1" most pronounced nitrogen deficiency
"3" poor in nitrogen
"5" just sufficient in nitrogen
"7'' more often found at places rich in N
"8" nitrogen indicator
"9" surplus nitrogen to polluted with N
"2'', "4", "6" intermediate
b) Most of the threatened species can only compete on nitrogen - deficient stands (57 "potentially threatened" species not considered)
c) The fraction of threatened species within the total of species in a given class of nitrogen indicator value diminishes with better nitrogen supply. It remains constant from value "5" upwards (see above).
These trends have been demonstrated not only for the Federal Republic of Germany, but also for the Netherlands, Switzerland, the former German Democratic Republic and other countries as well.
Very few of the wildlife species that have vanished from the Federal Republic of Germany have become extinct, since they survive elsewhere; nevertheless. as a result of farming activities in the past and up until roughly the middle of the 20th century they had earned the status of Idigenous plants and animals. A large number of the currently endangered species are hunger artists that receive their chance to receive light on sites that are artificially kept open. On such sites, insolation raises the temperature near the ground. At least near the surface, this can also result in a drying out of the soil. Increased dissipation at night and during the winter further enhances the continental nature of these sites.
Modern farming practices and pollution have created forest-like microclimates characterized by very little light reaching the undergrowth, moderate temperatures marked by low fluctuations, moderate to high moisture levels, and a permanently abundant supply of nutrients. These occur nearly everywhere in the Federal Republic of Germany, both along bodies of water in open country and in the forest. Plant species unable to tolerate this, as well as animal species that are dependent on certain landscape structures that have vanished along with the plant species that characterized them, will continue to be threatened in Germany as long as the described influences have a large-scale impact and as long as no effort is made to actively counteract them.
The principal threat to ecosystems in the Federal Republic of Germany is thus an over supply of nutrients, as well as of acids and other pollutants. This also has directly relevant consequences for human beings, e.g. contamination of drinking water and accumulation of toxins down through food chains, aspects which I choose not to go into in greater depth at this point. Nevertheless, a few other facts should be mentioned that round out the picture just sketched.
Among the vertebrates of Central Europe, those species are particularly endangered that require dry, warm habitats on sites with short grass and patchy ground cover. This applies equally to mammals, birds, reptiles and amphibians. Those amphibians that are more strongly restricted to moist or forest biotopes are less endangered than those that inhabit open sites even outside of the spawning season, e.g. yellow- and fire-bellied toads (Bombina spp.), the common spadefoot (Pelobutes fuscus), the natterjack (Bufo calamita) and the green toad (Bufo viridis). The situation is similar with the lizards: the forest or moor lizard (Lacerta vivipara) is still quite common, while the sand lizard (Lacerta agilis) is becoming rare everywhere, and the wall lizard (Podarcis muralis) has survived only on the very warmest Central European sites (cf. FELDMANN 1981). Where endangered bird species are concerned, it is conspicuous that they include many denizens of open, permanently green
heathland with a short grass cover. Many even have names that reflect the structure of the sites they inhabit, like the extinct rock sparrow and the rock thrush, as well as the wheatear (German: Steinschmatzer) and the little owlet (German: Steinkauz), both of which are on the decline everywhere. Among the endangered mammals, the white toothed shrews are a prominent example. The dying out of certain larger animals has had other causes (ELLENBERG 1980). Many of the animal species listed above prefer relatively large insect species as a source of nourishment, with "large" meaning, in this case, having an overall length of more than approximately 5 to 8 mm. Since they are less susceptible to desiccation, such large insects are at an advantage over smaller arthropods under Central European conditions on sites with a patchy ground cover and significant fluctuations in temperature and moisture. In western Gambia, the distribution of bird species that feed on small insects was
significant during the dry season of 1985. Their occurrence was restricted almost exclusively to the mangrove belt, since sufficiently high atmospheric humidity could only be found there (ELLENBERG 1987). Small-bodied arthropods can only multiply fast enough to build up a significant biomass if there is considerable moisture in the air. When such conditions are given, however, they appear to operate more effectively within the food web than large insects, which are consequently supplanted. REMMERT (1978) found that the size distribution of insects as a function of relative humidity is typical of a wide range of different ecosystem types. Whether it is also true for tropical "moist" forests is a question for further investigation. It is possible that low digestibility of plant materials favors larger-bodied insects - thus contributing to the discussed discrepancy in body size. These insectivores relying on large-bodied insects, which also include the shrikes (Laniidae, four
species occuring in Central Europe, plenty more related species in the tropics), the hoopoe (Upupa epops) and a great many other species, are largely on the decline in Central Europe. As regards mammals, those bat species deserve mention which do not usually hunt over water. These include the horseshoe bats (Rhinolophus spp.), which have become virtually extinct in Northwestern and Central Europe and whose food and foraging behavior was not analyzed under field conditions using modern methods until quite recently (STREBBINGS et al. 1984), and the mouse-eared bat (Myotis myotis), which also regularly obtains food from the ground surface.
The decline of the cited animal and plant species has long been known to zoologists, botanists and observers interested in nature conservation in Central Europe. As a rule, however, the causes are sought after within "limited contexts". Only rarely has it occurred to anyone to draw an explicit connection between the decline of a specific species and the generally increased nutrient availability in Central European ecosystems. Equally little thought is devoted to the fact that increased utilization of fossil fuels has made the many draft animals superfluous that used to graze on large areas, thus keeping the ground vegetation cropped short and preventing nutrient build-up. If the changes which entire biocenoses have experienced are examined, however, the connections among these factors are impossible to overlook. On the other hand, the reduction of the grazing pressure of livestock on many tropical ecosystems certainly would be an advantage for the recovery of the ground
vegetation and regeneration of forests.
Besides containing a biocenosis, every ecosystem is also associated with abiotic factors. We have already discussed the implications of changes in heat dissipation, temperature, moisture and light. These are all climatic factors. On a small scale, changes in them can be measured and documented (cf. ELLENBERG sent 1982). But since the described elevated influx of nutrients is affecting nearly all parts of Central Europe, detectable changes in large-scale climatic factors are to be expected. At a conference on climate held in November 1983 in Bad Soden-Allendorf by the German Federal Ministry of Research and Technology, the nestor of German climatological science, Prof. FLOHN, reported on observed trends towards a warmer climate on our planet that are presumably related to the proven increase in carbon dioxide levels in the atmosphere. This increase in temperatures seems to apply globally, as the worldwide discussion of the topic makes clear. Central Europe represents an
exception to the extent that in recent years the winters have been milder, in keeping with the general tendency, while the summers have been cooler than in the past. This is well known and is referred to as a tendency towards a more atlantic climate, although this does nothing to clarify its causes. It is conceivable that the global trend towards warmer temperatures is being overcompensated during the growing season by the increasingly luxuriant plant cover on ever-greater areas, with its changed heat retention, dissipation and evapotranspiration attributes as compared to sites with sparse vegetation.
At this point we have come full circle. In one of the introductory chapters, I attempted to explain that three major components interact and mutually influence one another in all ecosystems: energy, matter and information carriers, all of which can take a variety of different forms. It was my intention to sketch an example of these interactions and also to provide concrete examples of how modifications of the individual parameters can affect the system as a whole. An understanding of these interconnections permits one to deduce a great deal from the structure of a plant cover - sporadic, patchy, closed, etc. - such as competition among various plant species, microclimatic conditions, and trophic relationships both between plants and animals and among the fauna.
The nutrient situation is not always the determining factor. As one moves along the gradient from rain forest to desert, the crucial aspect is obviously water availability, although the cation content of the soil also plays a role. Moving along the gradient from lowlands to mountain sites, or from the temperate latitudes towards the poles, the temperature factor is apparently dominant.
I would like to stress once again that our Central European ecosystems are being depleted of their species diversity because of a general trend towards eutrophication and hypertrophication. The supplementary nitrogen input is resulting from the burning of fossil fuels, from the production and use of artificial fertilizers, and from the use of imported feed, leading to an oversupply of livestock and thus also of animal excrement, which is used in slurry form to fertilize fields. The feed itself comes in part from the excess agricultural production of North America, in part from painstakingly nurtured so-called cash crops grown in developing countries, and in part in the form of fish meal made from fish caught off their coasts. For areas in which the soils are naturally poor in nutrients (WEISCHET 1980; FITTKAU 1984), this cannot be a positive development. The same statement holds in reverse for the countries at the receiving end. The rapid population growth in the countries
of the Third World is further aggravating the described discrepancy.
Only relatively few tropical sites, for the most part with young, often volcanic soils, are suitable, for pedological and climatic reasons, for sustained fertilized farming practices. On the other hand, the forests, especially the rain forests, are highly adapted to maximizing capture of nutrients from the air. If fossil fuels and wood from forests continue to be burned at an increasing rate, therefore, it can be expected that the remaining forests will ultimately react to the continuous influx of nutrients, which are introduced in sufficiently finely dispersed quantities for them to be utilized by existing ecosystems, in a way similar to that described above for the vegetation of Central Europe. On the whole, the distribution of numbers of species in the lowland rain forest of the Amazon basin along the nutrient gradients is similar to that in Central Europe: by far the greatest numbers of plant species per unit area can be found on poor to very poor sites. The number of
species is significantly lower on sites with a better supply of nutrients, and the few sites with an adequate supply are relatively poor in species - and are, incidentally, for the most part already being exploited by human beings. On the other end of the scale, however, the number of plant species per unit area declines again on the very poorest sites (FITTKAU). These observations apply similarly to forests in Southern Asia, for example in Borneo (BRUNIG).
It can be expected that finely dosed introduction of nutrients from the air over a long period of time will alter the competitive situation in existing ecosystems at the levels of the plants, the animals, and the decomposers as well. The usability of soils with a poor nutrient reserve is not likely to improve as a result of this. Climatic changes caused by other phenomena could possibly even be offset in this way.
I would like to round off this section by discussing the impact of eutrophication on organisms involved in the decomposition process. As far as I know, "red data lists" documenting the degree to which individual species are endangered in delimited reference areas exist only for species belonging to the ecological compartments of the producers (green plants), and the consumers (animals that eat living organic matter), provided that a few groups of invertebrate fauna are left out of account that help to break up litter and organic debris. WINTERHOFF and KRIEGLSTEINER (1984) prepared a "red data list" for larger fungi, the first of its kind on a group of saprophytes in a Land of the Federal Republic of Germany. Many of the surveyed fungi are not only saprophytic, i.e. able to live on dead plant or animal remains, but also - as mycorrhizal fungi - enter into important symbioses with many green plants, in particular many forest trees, the recent threat to which (forest decline)
has already been discussed. In this "red data list", a large number of observations have been compiled that strongly point to pollution, i.e. to surplus nitrogen input to ecosystems by immission, as causing the decline of the surveyed species. This applies particularly to mycorrhizal fungi, which play a vital role for the plant species with which they coexist in acid and nutrient-poor soils (MEYER 1984). In addition to the use of fertilizers on farmland and the washing-out of these nutrients into other zones, transport through the air is thus also increasing in importance. Mycorrhizal fungi also play a vital role in the nutrient cycle of tropical rain forests, with their acidic substrates that are low in bases. In spite of this, not a single study is known to the author or any of the experts interviewed by him on the reactions of these tropical mycorrhizae to inputs of allochthonous nutrients.
5.2.2 Phenological mapping as the basis for planning of agricultural land use
The occurrence or certain easily detectable behavior of organisms permits conclusions to be drawn on the living conditions, either positive or negative, of other organisms. In the majority of cases, because of their habits plants are easier to locate and to observe than animals, and should therefore be given preference for detailed mapping of entire areas.
One goal which is relevant to farming practices, even those of the Federal Republic of Germany, would be to carry out highly differentiated mapping of microclimatic factors for supraregional, regional and local planning of agricultural land use. Climatological measuring stations are usually far apart, and often separated by very large distances. In spite of what is known about the effect on climate of the morphology of the terrain and other factors, as a rule they are so far apart that interpolation between these measurement points becomes too coarse for high resolution differentiation on the scale of a few hundred meters or less. Yet, denser networks of measurement stations are usually disproportionately expensive. On the other hand, detailed maps of areas that are significantly smaller than the surveyed region, e.g. a town with its surrounding country, are a prerequisite for elaboration of concrete proposals.
In this situation, one solution is to prepare "maps of the climate for growth". This mapping approach takes advantage of the phenology of a large number of easily identified, widespread plant species with a high frequency of occcurrence. The growth/climate mapping technique was developed in the early 1950s in southwestern Germany by ELLENBERG sen., and since then has been successfully applied to large areas in the Federal Republic of Germany, as well as by K.F. SCHREIBER and his coworkers to all of Switzerland on a scale of 1: 200,000. A similar mapping project for the state of North-Rhine/Westphalia by SCHREIBER is due to be completed soon. This method is based on the distinguishable so-called phenological states of flowers and leaves - i.e. of budding, flowering, fading of flowers, and development of new leaves. In each mapping area, 20 or more different plant species are evaluated that typically develop at different rates during the course of the spring. The phenological
states of the different plants are observed in the field - as a rule from a slowly traveling automobile and entered in a rough map in the form of "heat levels". The phenological states are designated using a scale of ten, with I = still completely bare and 10 = flowers have faded completely or, with respect to the leaves, 10 = completely developed. Emergence of flowers or leaves = 5, leaves 75 % developed or flowers mature = 8. The various different plant species at a given site exhibit, because of their different ecological requirements, as a rule different phenological states at a given point in time. In order to permit assignment of these different levels of development to uniform "heat levels", a so-called calibration line must be drawn and surveyed, along which as many as possible of the typical zones of the studied area should occur, from the warmest to the coldest sites, and with the aid of which the heat levels can be defined. During the course of the season, such
calibration lines can be used to identify the typical phenological states of the different test plant species for a wide range of heat levels. A phenological spectrum at a given point in time remains valid for 1-3 days, depending on weather conditions. In this way, during the course of just a few weeks in the spring - if the area is sufficiently accessible by road, from an automobile - an area spanning many thousands of square kilometers can be surveyed with great topographical accuracy by two experienced persons (one driver and observer, one recorder and mapper). In addition to mapping the general distribution of heat levels, such a procedure also permits fine local heat gradients to be distinguished. The possibility of using aerial photographs of appropriate scale instead of driving automobiles has to be tested.
Phenological mapping of heat levels is consistent in a typical way with the definition of a bioindicator, which it is worthwhile to repeat here: "A bioindicator is a related group or community of organisms whose occurrence or an easily observed behavioral trait of which can be so closely correlated with certain environmental conditions that it can be utilized as a pointer or quantitative test." Such a heat level classification or ecological map of climate for growth or growth/climate classification scheme - whatever one chooses to call it - can, with the aid of just a few climatological measuring stations, be calibrated to absolute reference values, e.g. to mean temperatures, heat sums or similar measured parameters. In this way, bioindicators and measurement technology complement one another ideally. It would be worthwhile to examine whether a phenological mapping approach could also be applied to other climatological or even geographical gradients. It would appear quite
apt for mountainous regions with differences in altitude (warmth) and slope (radiation).
<section>5.3 The levels of populations and individuals</section>
5.3.1 Preliminary remarks
5.3.2 Future risks of continued pesticide use
5.3.3 Use of birds as "biomonitors" of pollutant burdens in landscapes - a survey
5.3.3.1 A field experiment on the ecology of the contamination of birds with pollutants
5.3.3.2 How to identify suitable species for biomonitoring
5.3.3.3 A routine example of detection of spatial variations in pollution levels
5.3.3.4 Quantitative biomonitoring of heavy metal pollution with the aid of bird feathers
5.3.1 Preliminary remarks
Genetically speaking, species exist in and are constituted by populations; these are the actual reproductive units that permit the long-term survival of a uniquely composed pool of genetic material (MAYR 1967). There is a lower limit to how small such a population can become. According to what little is now known, the minimum population size so that a species of vertebrate animal can be expected with relative certainty to survive and, possibly, grow in number again, is between 100 and 500 individuals that are capable of reproducing. Smaller populations than this are highly endangered, and often die out for obscure reasons. If it is wished to prevent their extinction, therefore, they must receive special protection and care. This is virtually impossible in the case of rain forest species, for example. The only viable solution here is to set aside a minimum area of land that will ensure survival of a sufficiently large population. These so called minimum areas are thought to
be at least equivalent to the sum of the areas required by the above-mentioned 100 to 500 individuals. The determination of such minimum areas represents one of the greatest challenges of our time for international wildlife protection efforts and ecology. The WWF is currently engaged in promoting such "minimum-size projects", one of which is being conducted in Amazonia in cooperation with the IUCN. Within the scope of the so-called Soil Protection Project of the German Federal Ministry of Research and Technology, we are presently working on the topic "minimum areas for animal populations from the point of view of nature conservation" for Central Europe.
Because of the extreme nutrient poverty of many ecosystems in the moist tropics, a large number of different species occur per unit area; however, the vast majority of these have only a very small population density. That means that the required minimum areas for maintenance of populations of certain species must be relatively large under such conditions. Species which, for natural reasons, require a large area within which each individual can roam, e.g. certain large vertebrates, especially predators, or whose individuals defend extensive territories, are hardest-hit by a fragmentation or reduction of their habitats. The just-mentioned animal groups have already largely disappeared from Central Europe, some of them centuries ago (ELLENBERG jun. 1980). These facts can be expected to have equal validity in the developing countries. Here are two examples to illustrate this:
Predatory birds offer a range of species of manageable size to which the above-mentioned criteria apply. Many birds of prey are conspicuous and easily recognized by those familiar with them. For this reason, REICHHOLF (1974) made use of the diversity of predatory birds for the purpose of characterizing the degree to which certain South American landscapes are still intact. His approach was also adopted by BRANDL et al. (1984) and applied to areas in Botswana, Zimbabwe and northeastern South Africa. Both studies arrived at the same conclusion. The influence of human economic activities on the utilized landscapes serves to reduce the diversity of predatory bird communities occurring in them. It favors certain species, while creating difficulties for other species that can range in severity all the way to the point of causing their extinction. Regions that are relatively thinly populated by human beings and are characterized by relatively extensive land use exhibit a larger
number of predatory bird species than intensively utilized landscapes. In this context, pesticide related problems play only a subordinate role. Similar observations can also be made in Central Europe; for example, the particularly sparsely populated parts of Lorraine south of Saarbrucken and of the young moraine landscape of Mecklenburg still continue to harbor intact populations of some predatory bird species which have become exceedingly rare in the rest of Europe (e.g. Montagu's harrier in the first case, and the sea eagle and osprey in the second).
The studies which are currently being conducted for the purpose of identifying the most important biological refuges in the earth's tropical rain forests are caught up in an almost hopeless race against time. It is precisely in those regions which have the character of refuges that the forests are being destroyed at a particularly fast rate. Such areas are found, for instance, in the peripheral zones of Amazonia and not in the economically less interesting central part of the tropical rain forest (REICHHOLF 1984). Zoogeographers have provided an important insight: protective measures should concentrate on the pleistocene forest refuges, since these are largely identical with the zones having the highest number of species per unit area. The secondary contact zones between the habitats of regional fauna also deserve attention when selecting those zones particularly deserving of protection (HAFFER 1983).
Another problem which weighs as heavily as the race against time is how to efficiently survey and monitor species. This aspect has already been touched upon above. To a certain extent, this difficulty also applies to vertebrates, although birds and, perhaps, amphibians as well appear to be relatively wellsuited for such survey programs, among other reasons because they can be detected by acoustic means in difficult terrain. This aspect also holds true for some insects, e.g. grasshoppers and locusts. However, we still know far too little even about them in order to conduct a reasonably reliable survey of the range of species actually present at a given site within a short time. For decades, there has been an acute lack of research funding for "mere inventories". The supposed "low priority" of faunistic and even floristic surveys has presented a major obstacle to studies of the animal life of tropical regions. The real reason is that few spectacular results can be expected
when selected groups of species are thoroughly researched, while such studies mean years of hardships in the field for the participating biologists. Even organizations devoted to supporting scientific research, being primarily guided by practical considerations, rarely provide backing for such projects. It should therefore come as no surprise that in many developing countries the inventory phase has barely even begun, in spite of the fact that work is now being done on a broad front and within the scope of international cooperation - although the Federal Republic of Germany has so far remained virtually uninvolved - to survey and classify the flora and fauna of the tropical rain forests (REICHHOLF 1984). The ecosystems of tropical rain forests, with their vigorous plant growth and large biomass, are "as vulnerable to outside intervention as a hemophiliac" (WEISCHET 1984). Logging and conversion of forest for agricultural use inevitably lead to the displacement and, in many
cases, the extinction of thousands of animal and plant species (cf. TEMPLE 1978). In those parts of the coastal mountain range of Southeastern Brazil and the Eastern Cordillera of Colombia that have been largely logged over during the course of the last few decades - previously harboring an extraordinary diversity of bird species with numerous endemic varieties - this decline in species has been particularly prominent and relatively well documented (KING 1978). In the Brazilian state of Sao Paulo, for example, the large parrots have ceased to breed due to the lack of suitable forests (FITTKAU, REICHHOLF). It can be safely assumed that similar statements hold for other animal groups and plants that are not as well known.
Based on the amount of food available for each individual within a population per unit of time and land area, i.e. the carrying capacity of the biotope and the energy and nutrient content of the available food, the characteristic parameters which govern population dynamics fluctuate: namely population growth rates, mortality, immigration and emigration (in each case per unit of time and land area). This phenomenon was investigated in the case of the roe deer (Capreolus capreolus) by ELLENBERG jun. (1974, 1978, 1979, 1984) in a comprehensive field experiment spanning a period of several years. If a population is subjected to particularly severe environmental stress, e.g. by being hunted, by harsh winters, by episodic environmental catastrophes of other kinds, or by acute or chronic poisoning such as can occur in connection with the use of pesticides and introduction of heavy metals into the environment, within certain limits population growth can be stimulated, the survival
rate of the young animals raised, immigration boosted and the number of emigrating individuals reduced. In other words, populations subjected to such environmental stress tend to exhaust the carrying capacity of a given biotope by maintaining a fair/y constant population size, and in the case of' temporary setbacks to quickly reattain this level. Unless the dynamics of such populations are studied in greater detail, at first glance they appear to fluctuate about a steady-state size. This is achieved by means of the diverse mechanisms involved in intraspecies competition. It is therefore all the more surprising when a population "crashes", dropping to a low level because its natural regulatory mechanisms have no longer been able to cope. This phenomenon has been the object of much study in connection with the pesticide problem and its impact on predatory birds (NEWTON 1979; ELLENBERG jun. 1981). Nevertheless, these and similar aspects continue to receive too little attention
for assessment of ecotoxicological problems related to the use of pesticides. Moreover, only in a very limited number of cases are the maximum tolerable concentrations of toxins known for species and/or populations.
On the other hand, under the influence of chronic stress populations of a wide range of different species are able to adapt to these new selection pressures. Both statements also apply to human beings. Species with shorter generation times, however, are at an advantage under such conditions. The ability of bacteria and insects to develop resistance when antibiotics or biocides are used widely and/or over long periods of time has been demonstrated many times (IUCN-UNEP-WWF 1980). Attempts are made to compensate for this by employing increasingly large biocide doses. But the increased amounts used then have an ever-greater impact on other types of organisms within the same ecosystem, and the self-regulatory mechanisms of the ecosystem based on competition, predator-prey and host-parasite relationships, etc. are weakened more and more. A runaway control loop with positive feedback!
In this context, it is necessary to point out the fundamental difference between the ethics of human populations and those of animal and plant populations living in the wild. In the case of human beings themselves, and to a more limited extent where domestic animals and crop plants are concerned as well, every single individual counts. The death or lack of the ability or opportunity to reproduce of individuals in such populations is generally considered to be a loss. Any other way of dealing with this phenomenon would constitute a serious affront to our most basic ethical and moral principles. In wild populations, by contrast, such"losses" are looked upon as being necessary to maintain the system as a whole. Without them, natural selection processes that permit adaptation to changing conditions would no longer work. This also applies to gradients which are influenced, either directly or indirectly, by human beings.
Differentiated diagnoses of the causes of death of single individuals of free-living populations are only possible under special conditions. A certain amount of background information is therefore required if changes in population dynamics or population densities are to be understood. By the same token, it has taken the decimation of the wild populations of animal species sensitive to specific factors - e.g. the peregrine falcon, the sparrow hawk, the osprey and the brown pelican - to call our attention to previously unknown noxious factors in the environment and make us initiate investigations of their causes. In some cases, e.g. the causal relationship between reduced thickness of the eggshells and contamination of the food of these birds with DDT, it has taken the work of many researchers and laboratories more than 10 years to get to the bottom of the problem (RATCLIFFE 1970). Continuous monitoring and study - at both the regional and supraregional levels - of animal
groups which are already known to be sensitive to the effects of contaminants, especially of such species whose individuals are dispersed over large areas, is therefore already being practiced by several environmental monitoring programs, for instance in Sweden (SNV 1980) and Canada (ELLIOT 1984). Many primarily laboratory-oriented physiologists and ecologists are still reluctant to consistently apply such approaches, however. One reason given for this is that collection of specimens, e.g. for an environmental specimen bank (LEWIS et al. 1984)is regarded as posing extremely difficult problems in the case of warm-blooded vertebrates, as compared to other types of organisms. Moreover, it would seem that the number of specimens which it is possible to collect per unit of time and land area is not quite sufficient to meet the requirements which have been formulated to date. LEWIS (1984) has already taken a more highly differentiated stand on this matter, however. Apparently,
publications by the author of the present article have contributed to this reassessment. For this reason, in section 5.3.3 below I have attempted to present a survey of the possibilities for using birds as biomonitors of environmental pollution, although other animal groups would of course also be suitable for this purpose. First, however, it is necessary to discuss a few general aspects.
5.3.2 Future risks of continued pesticide use
In view of the apparently unstoppable population explosion which is looming on the horizon, especially in the countries of the Third World, and in view of the limited possibilities for extending the land area suitable for agricultural use, the food problem can only be solved by achieving higher yields per unit area of land. Inevitably, irrigation and fertilization will be used to attain this goal. Both of these measures also have an effect on the anatomy of the plants growing under the correspondingly changed conditions. The plant tissues become more "hygrophilous", i.e. the walls of the cells remain thinner and exhibit less lignification, the epidermal cells are cutinized less, etc. Such fertilized plants with a good supply of water become more attractive to herbivorous insects, and at the same time the competitors of the crop plants are also promoted, namely the so-called weeds. Anywhere that labor-intensive control measures or ecologically sounder farming methods cannot
be used or are decided against for other reasons, the use of pesticides offers itself as a solution to the problem: herbicides to combat the weeds, insecticides to kill off the insects, and a variety of different poisons to keep away snails, seed-eating birds and other bothersome organisms. Effective pesticides are efficient in reducing the population densities of the organisms against which they are used, but they are rarely successful in completely eliminating them. Moreover, an inadvertent side effect is that other organisms which live off the pests lose, suddenly and unexpectedly, their source of nourishment, and the structure of their habitat is destroyed. Only a few of these predators (organisms that feed on other organisms in the broadest sense of the term, thus including herbivores) are able to temporarily survive this loss by emigrating, switching to other food sources, or going into a dormant state. Most of them can be expected to die out. Since food organisms - at
least outside of forests - are generally characterized by shorter generation times and population cycles or regeneration times in affected individuals, than the predators which feed on them, in many cases it can be observed that pesticide application results in short-lived success followed by recovery of the pest populations that are now able to multiply virtually unchecked by their natural predators. Consequently, the medium-term or long-term effect of pesticide use is, not infrequently, an even greater pest population density than at the outset. Another possible effect, which has frequently been observed in connection with weed control, is the following: once the target species population has been eliminated, other species are freed of competition from it. In this way, species which had previously been kept under control by natural means develop into pests themselves.
Higher doses of pesticide are then applied in an attempt to combat populations of pests that develop after initial pesticide application or reappear as a result of shifts in competition. This serves to stimulate the development of resistance among the target populations, permitting them to multiply again, and provoking the use of even more pesticide. This results in a vicious circle which escalates until the system collapses. The number of arthropod strains which have been proven to be resistant to different pesticides (mainly insects) increased from 182 in 1965 to 392 in 1978 (FAO 1979). On the whole, the effectiveness of pesticide usage is questionable: between 1904 and 1979, the crop losses caused in the United States by insects, plant diseases and weeds remained unchanged at approximately one-third of potential yields (PIMENTEL 1978). During this time, of course, productivity increased greatly and with it the yields. I doubt that this would have been possible without
plant protection in the broad sense of the term. Nevertheless, the development of resistant mosquito populations, in many cases within just a few years, has resulted in the control measures taken to combat the vectors of a wide range of tropical diseases being conducted ad absurdum in many places. These developments signify that those persons and institutions responsible for human health have many medium- and long-term interests in common with those who would like to conserve populations of free-living plants and animals in intact ecosystems. Even in the case of agro-industrial intensive farming enterprises, e.g. for cotton production, the costs incurred by pesticide application frequently develop into one of the limiting factors for profitable operation. In these and similar cases as well, it is clear that those interested in protecting nature share much with those wishing to utilize it.
In order for scientists to arrive at a well founded opinion on the side effects which pesticide usage can have in the environment, they need information on the amounts used of all important pesticides, as well as the places and times at which they are applied. In the interests of all, there is no longer any justified excuse whatsoever for withholding or disguising such information. Accordingly, the International Conference on Environmental Hazards of Agrochemicals in Developing Countries in Alexandria in November 1983 formulated the following recommendation:
"Taking into account the existing intemationally-agreed conventions concerning the safe use of pesticides and agrochemicals, we firmly believe that:
The present situation concerning agrochemicals is unsatisfactory, especially when the importing country has no necessary registration system and is not properly informed of the hazardous properties of the imported product or restrictions on its use:
a) There are too many cases of human pesticide-induced illness and death, especially in developing countries.
b) Adverse ecological effects resulting from pesticide use, overuse, and misuse are occurring.
c) The continued careless use of pesticides can lead to:
1. The raising of previously insignificant pests to the status of major pest species.
2. Increase in pesticide resistance.
3. Increase in contamination of soils, water and air.
4. Increase in hazards to humans, plants and animals."
Following a similar train of thought, the "Mussel watch 11: chemical changes in the coastal zone workshop", which also took place in November 1983 (in Honolulu, Hawaii) and was independently organized as a joint activity by the Scientific Committee on Problems of Environment of the International Council of Scientific Unions, the International Federation of Institutes of Advanced Study, and the East-West Center in Honolulu, attended by experts on the ecology of marine coastal waters from 26 different countries, called for the "International Register of Potentially Toxic Chemicals of the United Nations Environment Program" to establish a data base which would permit international monitoring of production and use of persistent halogenated hydrocarbons. As early as April 1982, the World Working Group on Birds of Prey of the International Council for Bird Preservation demanded, at its conference in Thessaloniki, Greece, that an international conference be held together with
representatives of the WH0, the FAO, UNEP and UNIDO, as well as the manufacturers of pesticides and other toxic chemicals with the goals (among others) of:
"Involving themselves with the problems arising from chemical control of vectors of malaria and trypanosomiasis, and of searching for means of identifying a long-term solution with an aim to overcoming these diseases; and of finding possibilities for the long-term survival of healthy populations of predatory birds in habitats that also ensure that health of human beings and the maximum food production possible under the existing conditions."
Within this context, the existence of predators becomes generally important for biological monitoring approaches, regardless of whether we are dealing with parasitical hymenopters, insectivores, birds of prey, tree frogs, or other relatively long-lived organisms with a slow population turnover. We should keep this fact in mind when we practice biological monitoring for human beings, who after all belong to the longest-lived terrestrial predators in the broad sense of the term.
Natural ecosystems and those in a close-tonatural state have different functions for human society. Van der MAAREL and DAUVELLIER (1978) break these down into productive functions, carrier, information and regulatory functions. The productive functions include the provision of water and air, production of biomass in the water or on land, and under the influence of agricultural measures (in the broader sense: aquaculture, field cropping, pasture farming and forestry). The carrier functions are roughly divided into the following categories: urban industrial activities including traffic, rural activities such as settlements, dams, and other structures for regulating bodies of water, disposal of waste in water bodies or dumps, and recreational opportunities in the landscape itself, such as water sports or rock climbing. The information functions comprise the utilization of information for orientation, research, education and teaching, or also as signals, i.e. as indicators; it
is impossible to overlook a hitherto unexploited reservoir of information in the biotic domain. Regulatory functions primarily involve cleaning and stabilization; cleaning can be, for example, the filtering out of dust or biological self-purification in water bodies and soils; and stabilization is performed in connection with regulation of the climate, retention of soil and water in the system, and biocenotic regulation. It would appear to be worthwhile to learn about the different degrees to which the various ecosystems perform the above mentioned functions under specific conditions for human society. It is only within this context that biological monitoring can gain true usefulness. In order to conserve the information and regulatory functions of ecosystems, these should be disturbed as little as possible.
Biological monitoring is not primarily a matter of measuring the concentrations of toxic residues in organisms - and thus a chemical issue. Instead, it is principally based on differences in the developmental rate of organisms, changes in the population dynamics of species, and shifts in the competitive relationships among populations in ecosystems. The role of physiology and chemistry is relegated to subsequent clarification of the causes of observed changes of this type.
If, after pesticides have been used for a lengthy period of time and resistance has developed among the target populations, other pesticides also fail to have the desired effect, at least two sensible strategies are available to local human populations: the attempt can be made to breed plants that are genetically resistant to the pests, or to employ more sophisticated methods of ecological pest control. Both approaches can be successful, and then, at least temporarily, lead to a solution of the problem. If they are not successful, then production and potential yields drop. In response to this the attempt is then made to cultivate other plants or to change the agricultural system. This can be done at various input levels: "cash crops" require relatively high inputs in terms of energy, fertilizers and, possibly, pesticides, and often require intensive use of machinery. With a relatively low population density, this system may be successful, as well as under certain ecological
conditions, e.g. in situations where only large organizational units can operate profitably. With high population densities, however, in the medium and long term it is possible that complex socioeconomic problems arise. Since ancient times, both phenomena have manifested themselves again and again in flood areas. If, however, it is no longer possible to profitably sell surplus produce, then the only remaining alternative is subsistence farming. Provided that the population density is not too great, it is possible to survive under these conditions. But if - especially following a period of temporarily improved conditions at the beginning of the pest and disease control phase - the human population density becomes too large to be supported by a subsistence economy, then poverty and misery are unavoidable. Exhaustion of the soil, emigration, malnutrition and hunger are the results. Provision of food aid is a charitable act at this point, to be sure, but does not overcome the
basic problems. Here we run up against the limits not only of Christian ethics; many areas, particularly in the poorer developing countries and not just in Africa, appear to have already reached this state of dire need. Where such overburdened ecosystems are concerned, a discussion of the additional load imposed by the accumulation of pesticides down through food chains would appear to be beside the point. Both BALK and KOEMAN (1984) and MATTHIESSEN ( 1984) stress, based on their extensive experience in various parts of Africa and Southeast Asia, the importance which biological monitoring of fish-eating fish has because of their major role as a source of human nourishment. I would like to extend this by stating that not only fish-eating fish as human food, but in particular also fish-eating mammals and birds - including predatory birds in such ecosystems - play a vital role as indicators in the place of human beings. They are valuable because of their sensitive status as the
terminal links in food chains, and because their individuals, in spite of being territory holders and therefore sedentary, roam over wide areas, as a result of which they can reveal much about the contamination of entire landscapes.
Attention has also been directed, within the scope of German development cooperation for controlling tsetse flies in Cameroon and other West African countries, to the ecological impact of such measures. One working group, headed by the Department of Biogeography of the Saarland University, devoted several years of intensive study to the side effects which tsetse fly control measures have on lower animals and many small vertebrates. They arrived at the conclusion that, with the exception of shrews, no animal group has suffered any significant adverse effects of a lasting nature. However, those groups of animal species characterized not only by BALK and KOEMAN but also by MATTHIESSEN as being particularly valuable for monitoring purposes were nearly completely ignored by this working group. Moreover, in my view neither the working group nor the organizations sponsoring its activities bothered to ask the more fundamental question as to whether tsetse fly control truly makes
sense: does the opening up of a landscape which has previously been largely protected - by the tsetse flies! - from overgrazing genuinely represent an advantageous development at the national and supraregional levels?
5.3.3 Use of birds as "biomonitors" of pollutant burdens in landscapes - a survey
The aim of this section is to present and discuss the possibilities for utilization of certain vertebrates - illustrated by the example of birds - for monitoring the contamination of areas with toxins. Compared to most other organisms used for biological monitoring, vertebrates assimilate contaminants not only over periods of time (like plants, for instance), but also from significant expanses of territory; depending on animal species, these can range from less than a hectare to several hundred square kilometers or more. Scandinavian golden eagles, for example, cover their habitats with nearly regular networks, at the nodes of which - approx. 17 km apart - their eyries are situated, preferably atop pine trees aged 300 years or older (TJERNBERG 1983).
Scientific and practical reasons provide us with motivation to shed light on this assimilatory ability and to place it in our service, although a diversity of factors related to how the investigated organism is embedded in space and time can influence its specific ecology - and thus also the pollution levels which it can be used to detect. These structures appear to grow in complexity in more highly organized animal species.
To deal with this, the expertise of field ecologist is needed. Between 25 and 15 years ago, it was their knowledge and their concern about the survival of animal populations threatened by exposure to pollutants that led to more intensive investigation of toxins accumulating in food webs. Since then, however, this topic has increasingly become the province of the "measuring" natural sciences and of (veterinary) medicine. We have witnessed the advent of chemical and physical analysis methods that are capable of detecting not only - metaphorically speaking - a single Apache among a million Norwegians (parts per million = ppm), but even the much more elusive and physiognomically less conspicuous single Eskimo among a billion Chinese (ppb). Such developments were also an indispensable prerequisite for accurate identification of toxins and their concentrations and in order to assess their global distribution. Nevertheless, it seems to me that this striving for precision and focus
on details has obscured our perception of the biological context and the ecological relevance of the results. Because of the enormous variability in these domains, thousands of analyses have been performed, primarily in response to statistical criteria.
Here, I would like to attempt to focus more strongly on applying ecological principles to the complex of related phenomena "environmental pollution - contamination of organisms - endangerment of populations". It can be safely assumed that ecologists need the support of laboratory analysts and viceversa.
Not many birds are suited for use as test organisms. Quails are particularly well-suited as laboratory animals, since they attain sexual maturity when only a few months old. Nevertheless, even with their aid the disruptive effect which DDT has on insect-, fish- and bird-eating bird species was not recognized in time. It is improbable that DDT, to take just one example, would have been approved for use as an insecticide if the - herbivorous - test mammals and birds had been harmed by relevant concentrations of it in experiments. On the other hand, the responsible authorities were aware at quite an early stage that many non-homoiothermal terrestrial vertebrates react very sensitively to DDT pollution. Apparently, at that time (in the late 1940s) this problem was regarded as unimportant, a view which persisted for a considerable time (GEIGY 1947; HOFFMANN and LINDUSKA 1949; MUNROE 1949).
The use of birds as biomonitors will be dealt with in greater depth below. Bird species that have been used as bioindicators (in the restricted sense), initially for detection of unspecified harmful influences, include the peregrine falcon (Falco peregrinus), the sparrow hawk (Accipiter nisus), the osprey (Pandion haliaetus) and the sea eagle (Haliaetus albicilla), the fate of which over the course of the last three decades in the so-called "developed countries" is sufficiently well-known (cf. ELLENBERG (ed.) 1981). The situation in other parts of the world continues to give cause for alarm (BALK and KOEMANN 1984; specific examples from Zimbabwe and other parts of the earth will be discussed below). An indication of the geographical scale of the problem has been provided by the observations of East German scientists who, for a number of years now, have been conducting faunistic studies of vertebrates in Mongolia (STUBBE, PIECHOCKI, personal communication). For years, they
have not seen any young birds at all being raised in the four sea eagle nests known to them. Instead, the adult birds have been observed to sit on rotting eggs far longer than the usual time required for them to hatch. Other nests have been abandoned, presumably because the eggs had broken apart. It is probable that the Mongolian sea eagles winter in the lowlands and coastal areas of southern East Asia. A few remain in Mongolia. According to reports from travelers - some of whom have a background in zoology - during recent years intensive and indiscriminate use has been made in southern China of organochlorine pesticides, with the aid of which the local populations have attempted to solve their hygienic and nutritional problems - just like in large parts of West Africa and elsewhere (BRUNIG, FITTKAU, P. MULLER, personal communications).
Some species react indirectly to pollution of other kinds, like the kinglets (Regulus regulus) observed on sample plots in the Saxon Forest (Sachsenwald) near Hamburg. There, they inhabit stands of spruce (Picea abies) afflicted with needle loss of varying severity related to the forest dieback of recent years in Europe. The extent of needle loss is inversely proportional to the population density of the kinglets. The concurrent increase in coletits (Parus ater), another bird species which is highly adapted to spruce trees, thus seems confusing at first glance. This appears to be a reaction to diminishing competition from the other tit species, which are larger and stronger. As the overall supply of food declines in the afflicted forest stands, the latter occupy fewer nesting cavities. As this example shows, the relationship between the indicandum) and the indicator can be quite complex. In such cases, it can only be understood by bringing to bear a wide range of knowledge
and expertise. Nonetheless, as I have already pointed out, the effects of some new kinds of pollutants have been discovered only with the aid of indicator species.
Biomonitoring can only be meaningfully applied for surveillance of substances which have already been recognized as being hazardous or potentially dangerous. In this sense, biomonitoring as a method is in direct competition with technologically oriented programs involving physical and/or chemical analysis. Biomonitoring is not being read fly accepted and integrated by those in charge of such programs; instead, its proponents are having to painstakingly work towards its acknowledgment by calling attention to the advantages it offers over technological approaches. I believe that both points of view have their justification. Each is dependent on the other, and they complement each other mutually. Biomonitoring will be able - once it has become firmly established - to achieve results more easily, more quickly, less expensively and with a greater integrating effect, but it nevertheless relies upon precise calibration by technological means. Conversely, technological precision by
itself - i.e. without additional information from the fields of biology and medicine - is incapable of letting us understand, control, monitor and assess the biological and ecological relationships involved.
The greatest problem associated with attempts to capture the temporal and spatial trends of pollution in defined regions with the aid of biomonitoring is caused by the fact that the measured toxin concentrations vary greatly, even in specimens of the same species collected at the same time and (nearly) the same place. This makes it essential to standardize specimen-collection procedures and carry out studies for the purpose of "internal" biological calibration of the species used as biomonitors. At first glance, both tasks appear much more difficult for highly evolved, warm-blooded animals than for lower organisms or plants. Extensive and well organized research efforts are needed in order to detect temporal trends within the range of DDT concentrations exhibited by sparrow hawks (Accipiter nisus) in the British Isles, for example; the pollutant concentrations in individual eggs can vary over 4 powers of ten (COOKE et al. 1982). And even in the eggs of sparrows or great
titmice living in the same park, up to 100-fold variations in organochlorine concentrations are common (MAY et ELLENBERG, 1985).
My coworkers and I have therefore focused our inquiry on the causes of these large variations in measured contaminant concentrations - and intentionally avoided efforts to statistically get a handle on this "scattering" effect by studying a large number of specimens. Interspecies comparisons suggest that is it primarily caused by differences in the unique "physiology" of each species, i.e. in the way the organism physiologically deals with an assimilated toxin. Other obvious factors include gender, age and social status, as well as the stress levels to which individuals are subjected (cf. LEWIS et al. 1984).
5.3.3.1 A field experiment on the ecology of the contamination of birds with pollutants
For the reasons discussed above, a field experiment should be conducted in each case to clarify the following question: Are the measured contaminant concentrations due to "species-specific physiology" or to the feeding habits of individuals? When using organisms as "instruments" for monitoring environmental pollution levels, it must be possible to obtain clear and unambiguous answers to this and other questions. This is a prerequisite for reproducibility and interpretability of the analysis results. Otherwise biomonitoring programs are doomed to fail, even if they are based on years of preparations and conducted with the assistance of environmental specimen banks or other facilities.
The experiment must incorporate individuals of different species that eat exactly the same diet under field conditions at the same time and place. If a different contaminant concentration is measured in each species under these conditions, then it may be concluded that physiology is playing a much greater role than feeding habits. In the opposite case, different food chains would be responsible for the observed phenomenon.
For ecological reasons, situations of this kind are relatively rare. Typically, organisms living concurrently at the same place tend to avoid competition for food by specializing. A usable situation occurs with the cuckoo (Cuculus canorus) and one of its host species, the reed warbler (Acrocephalus spec.): in the homogeneously structured reed banks in which they dwell there is not likely to be any significant difference between the food of nestling reed warblers (Acrocephalus scirpaceus) and that of young cuckoos in nests located just a few meters away. However, because these species are rare in the area which my coworkers and I were studying at that time, and in response to nature conservation considerations, we were forced to create a similar situation experimentally. In 2 study areas, namely the "Deutsch-Franzosischer Garten" (DFG) and the "Hauptfriedhof" (HFR) in Saarbrucken, we exchanged newly hatched nestlings of great titmice (Paws major) and tree sparrows (Passer
montanus) for one another. The great titmice readily adopted the young tree sparrows introduced into their nests and raised them together with their own young until they reached the fledgling stage. The tree sparrows rejected the intruders, however. At the end of the nestling period, it was possible to collect the following specimens from 10 pairs of the manipulated nests:
a) Great titmouse and tree sparrow nestlings raised together in great titmouse nests on the same diet.
b) Pairs of tree sparrow siblings, one of which had been raised in a great titmouse nest and one in a tree sparrow nest, in each case on the diet typical of the corresponding species.
The livers and stomach contents of the nestlings were analyzed in the laboratory in order to determine the presence and concentrations of 15 different organochlorines. The nature of the food eaten by the two species had been previously identified by attaching "throat rings" to a few young birds that prevented them from swallowing the food brought by their parents. The food (insects and spiders) was examined with the aid of binoculars, identified as far as possible down to the genus, and quantified. The results showed that the young birds fed by great titmice received very similar nourishment from nest to nest in both study areas. By contrast, the food given to the nestlings in tree sparrow nests varied considerably depending on the situation.
With the exception of lindane, for all detected organochlorines present in sufficiently high concentrations (greater than 0.005 mg per kg of live weight, for apparatus-related reasons the lower measurement limit), the liver analyses consistently yielded the following picture:
- Great titmouse and tree sparrow nestlings that grew up together in the same nest, tended by the same parent birds and receiving the same food - which was different from that usually eaten by young tree sparrows did not exhibit any significant differences in contamination with organochlorines.
- The livers of tree sparrow siblings raised in different nests, one by its natural parents and one in a great titmouse nest, and receiving different food, showed significant differences in organochlorine concentrations. In the case of PCBs (polychlorinated biphenyls) and DDE, the differences were often 20 or more times as great as those between nestlings of different species raised in the same nest. On the other hand, the differences between the young birds in a given nest were insignificant and must be regarded as coincidental or a reflection of the measurement error inherent in the equipment used. Depending on situation, the young tree sparrows '`adopted" by great titmice can exhibit lower, equivalent or higher pollutant concentrations than their natural brothers and sisters in the original nest.
On the basis of these results it c an he excluded that species-specific physiologic al factors - and thus differing accumulation rates - play a major role in accounting for the varying levels of organochlorine contamination measured in the livers of young great titmice and tree sparrows. Rather, any "species-specific" differences in pollutant concentrations are due in this case to feeding habits.
This has the following implications for biomonitoring:
1. The results we obtained with great titmice and tree sparrows demonstrate that individuals of two different species at the same time and place can be contaminated to differing degrees because of different feeding habits.
2. Species whose individuals can exhibit a heterogeneous diet are less well-suited for biomonitoring of environmental pollution than species whose members are characterized by uniform feeding habits.
However, individuals belonging to species of the first type - with heterogeneous diets - can at some locations be at particularly great risk due to their differing food chains.
3. Organisms used as biomonitors should therefore have very uniform diets (e.g. great titmice), or else it must be possible to identify their individual feeding habits (e.g. goshawks).
Consequently in-depth study of important ecological relationships, especially those of the food web to which the animal species used as a biomonitor belongs is required. This effort is necessary, but is likely perceived by some as being discouragingly difficult.
5.3.3.2 How to identify suitable species for biomonitoring
It is essential to concentrate on "usable" species with the aid of generally applicable criteria. Such species must meet a large number of different theoretical and practical requirements. Catalogs of criteria for selection of "usable species" have been under discussion for a long time, particularly in connection with the preparations for establishment of an environmental specimen bank (LUEPKE 1979; LEWIS et al. 1983, 1984). In our "Working Group on Vertebrates" at the Saarland University, in the years following 1978 we succeeded in structuring a projected catalog of this kind (ELLENBERG 1981); Edmund HAHN (1984) subsequently applied this approach to Central European owl species. Other approaches are certainly conceivable and possible, involving the deletion of certain criteria, the collection of individual criteria into broader categories, or the addition of new criteria. What concerns us at this point is the basic principle involved.
Table 1: Assessment of the suitability of owl species for use as biomonitors. From E. HAHN (1984).
CRITERIA
Weight
Tyto
Otus
Bubo
Asio
Asio
Glaucidium
Athene
Aegolius
Strix
Strix
factor
alba
scops
bubo
otus
flammeus
passerinum
noctua
funereus
aluco
uralensis
Geographical correlation
Demonstratable food composition
Adequate pollutant tolerance
Ubiquitous occurrence
Low population fluctuations
Accumulation of toxins
Legal problems involved
Standardizability of specimen collection
Structurability of data according to age and gender
Knowledge about habits and radius of activity
Integration of useful time spans and geographical areas
Geographical correlation of food organisms
Suitability for experiments
Comparability with other species
Ease of detection
Ease of classiffication
Ease of manipulation, handling and specimen collection
Comparison of actual and possible food
Identifiability of individuals' food
Wide distribution
Euryoecia
Totals
An important prerequisite for spatial mapping of monitoring results is adequate knowledge of the movements of the species used. Of fundamental importance for the comparability of results is that specimen collection be largely standardized. Here, knowledge of individual animal diets - as we have seen - plays a major role: either the individuals of a species at different locations must have nearly identical diets, and/or it must be possible to obtain information on their individual feeding habits.
Table 2: Species which are more or less suited for biomonitoring. From E. HAHN ( 1984).
Species
Points^1)
Score in %^2)
Tawny owl (Strix aluco)
up to 108
up to 95
Honey bee (Apis mellifica)
Black-billed magpie (Pica pica)
Goshawk (Accipiter gentilis)
Little owlet (Athene noctua)
Roe deer (Capreolus capreolus)
Stone marten (Martes foina)
Fox (Vulpes vulpes)
Barn owl (Tyto alba)
European hedgehog (Erinaceus europaea)
Wood pigeon (Columba palumbus)
Earthworm (Lumbricus terrestris)
Brass beetle (Carabus auratus)
Homo sapiens
1) The assessments by different experts vary.
We passed the Central European vertebrate species - including Homo sapiens - through our sieve of criteria. Each criterion was weighted (with a point system) by assigning it to one of the categories "essential", "important" and "useful". Then the extent to which a given species fulfilled each criterion was evaluated - this could range from "unsuited" to "neutral" and on to "very wellsuited" (cf. Table 1). Finally, an exclusion system was defined, according to which a given species could be eliminated as a potential biomonitor of environmental pollution if it was classed as "neutral" in one or more "essential" criteria, as "difficult" in one or more "important" criteria, or as "unsuited" in at least one "useful" criterion. This system has the further advantage of clearly revealing gaps in our knowledge on which future research can concentrate.
Our approach, which permits calculation of results on the basis of the point system employed, yielded only a very few Central European species that can be regarded as basically suited for biomonitoring. They include the tawny owl (Strix aluco), the goshawk (Accipiter gentilis), the carrion crow (Corvus corone) and the black-billed magpie (P. pica). By comparison, human beings and earthworms rate rather poorly (cf. Table 2).
One aspect which definitely deserves to be given greater consideration in the catalog of selection criteria discussed above is the current state of general knowledge about the causes of distribution and abundance of the organisms in question. This knowledge is, as I have already pointed out several times, in most cases greater in Central Europe than in most developing countries. Yet, it seems to me that the knowledge and experience which many "locals" in the Third World possess as a result of a lifetime of interacting with their natural environment is still given too little attention. Systematic questioning of such "experts" could bring to light invaluable information useful as a basis for directed further study. This method is already being applied by the Nairobi-based ICRAF (International Council for Research in Agroforestry) within the scope of efforts to promote and disseminate agroforestry as an integrated land-use system in suitable tropical regions. An important
aspect of such untertakings is, however, that the questioner must already possess extensive knowledge of the topic under study.
Because of the great importance of selecting suitable species for successful biomonitoring, at this point I would like to discuss in detail a system of selection criteria that goes further than HAHN's approach (1984); it is described in GAST ( 1984), and was also elaborated by our "Working Group on Vertebrates" under my intensive supervision.
1. Spatial representativeness:
Distribution: The species should be widespread, permitting large-scale comparisons.
Abundance: Enough individuals must be available for field and laboratory studies.
Site fidelity: A prerequisite for making area and site-related statements.
Euryoecia: If a species is not broadly limited by ecological conditions, this permits identification of site-specific characteristics and gradients. - Caution: Beware of different food webs (cf. above)!
2. Availability, practicability of specimen collection, and experimental suitability:
Obtainable biomass: The size or number of individuals must be sufficiently large to permit taking of samples for laboratory analysis.
Experimental suitability: In order to corroborate findings made in the field and study special aspects (physiology, diet-related effects), it must be possible to manipulate the species for experiments in captivity under controlled conditions.
Longevity: Changes over the course of time can be interpreted best in the same individuals.
3. Ecological representativeness:
Reference characteristics: The physiology and annual and daily rhythms of the species must be known, at least in principle, and the gender and age of individuals must be readily determinable.
Sensitivity: The population must be tolerant to the pollutants under study, yet at the same time react sensitively to them (e.g. by physiologically adapting to the toxins, which are accumulated or excreted).
Similarity to humans: A high degree of physiological similarity to human beings is useful, being the real point of this kind of biological monitoring ("bioindication").
4. Trophic level and role within the ecosystem:
Feeding habits: The trophic level occupied by the species in the ecosystem must be known. If the make-up of the diet of individuals can be ascertained, then its specific role within the ecosystem can be identified with greater precision.
5. Reproducibility of specimen collection:
Standardized specimens: Standardized specimen-collection procedures are a prerequisite if it is wished to compare results from different areas or regions. They permit direct comparisons with studies that have applied the same specimen structures at other locations.
5.3.3.3 A routine example of detection of spatial variations in pollution levels
Years ago, pesticides containing organochlorines precipitated the controversy about the environmental hazards of such substances. In the early 1970s, PCBs were recognized as being similarly toxic. So far, attention has focused on the disruptive effects which these pollutants have on the terminal links of food chains. For this reason, I would like to sumarize here the monitoring results obtained using magpies which were described by Fernando GAST (1984). The black-billed magpie (Pica pica) fulfills most of the above criteria that must be met by a suitable biomonitor. Since magpies are pantophagous, i.e. eat a wide variety of foods, and obtain their nourishment from areas where our own food grows in the immediate vicinity of human settlements, my coworkers and I regard the results of our study as disquieting:
- Nearly all of the examined magpie eggs exhibited PCB concentrations higher than the maximum permissible level prescribed in the United States for chicken eggs intended for human consumption. PCBs appear to be less toxic to birds than to mammals. In some carnivorous mammals they can cause - even under experimental conditions - conglutination of the uterine mucous membrane, thus impeding implantation of the blastocyst (Statens Naturvardsverk 1982; BERGMANN et al. 1981).
- Widely differing concentrations of DDE, a metabolite of DDT, were found in 5 study areas: in the Saarbrucken area and in Lorraine, for the most part concentrations were measured that were below the maximum level permitted by law for chicken eggs intended for human consumption. In three winegrowing areas - around Trier (Trèves), near Landau in the Palatinate, and west of the city of Ludwigshafen - by contrast, very high DDE concentrations were still found in magpie eggs, in spite of the fact that use of DDT had been banned in the Federal Republic of Germany more than 10 years earlier (in 1974).
- The measured concentrations of hexachlorobenzene (HCB) and other substances exceeded the defined threshold levels either only locally or not at all in the 82 magpie eggs which were analyzed. Consequently, black-billed magpies appear to be particularly well-suited for monitoring of pollutant levels in areas populated by humans in Central Europe. This statement holds true not only for chlorinated hydrocarbons and HCB, but in equal measure for heavy metals that can be measured e.g. in magpie tail feathers (GAST 1984).
By referencing the measured toxin concentrations to (essentially arbitrarily chosen) levels, namely the "threshold" levels valid for human food, we have employed a way of depicting our study results that is roughly analogous to the system commonly used for measuring temperature. This permits quantification and thus direct comparisons, similar to values expressed in degrees Celsius or degrees Fahrenheit. However, we are not familiar with any quantifiable biomonitoring system used to date which is based on absolute measurement values or calibration as a system of reference. An approach to achieving this goal is presented in the next section.
5.3.3.4 Quantitative biomonitoring of heavy metal pollution with the aid of bird feathers
When employing biomonitors, the clear and unambiguous correlation between indicandum and indicator required by the definition of a bioindicator must be analyzed with particularly great care. In a great many cases, such a correlation has simply been assumed on the basis of its plausibility. My coworkers and I, however, endeavored to experimentally verify this correlation in at least one concrete instance, and for this we choose to study the heavy metal concentrations in defined feathers molted by brooding female goshawks. Goshawks remain loyal to sites integrating an area spanning many square kilometers - and are found nearly everywhere in Central Europe. It was therefore to be expected that at least one goshawk nest could be found in the immediate vicinity of each of the stations which the Julich Nuclear Research Facility (Kernforschungsanlage Julich) has been operating for a number of years in order to study the deposition of heavy metals via atmospheric precipitation. In
spite of certain analytical difficulties, measurement of lead (Pb) and cadmium (Cd) in precipitation and in goshawk feathers is nevertheless sufficiently practicable. We thus felt justified in attempting to demonstrate the suspected correlation.
Jorg DIETRICH, who during his years in our working group had extensively studied the ecology of goshawks (DIETRICH 1981, 1982), systematically located the feathers in the vicinity of the pollution-monitoring stations, and also carried out the analyses at the Julich Nuclear Research Facility. It would go beyond the scope of this article to present in detail the results of his measurements and of our evaluations, calibrations and interpretations. They nevertheless left no room for doubt (ELLENBERG et al. 1986; DIETRICH and ELLENBERG 1986): if collection of the specimens is thoroughly standardized - as regards the portion of the feathers which is analyzed, the anatomical location of the feathers, the gender and age of the bird from which it is derived, time of year, and geographical location- then the contamination of defined feather parts cast off by brooding female goshawks possesses a very close statistical correlation with the rates of introduction of the studied metals to
the environment via atmospheric precipitation (cf. Figure 9). The identified correlations between the rates of lead and cadmium influx (measured in micrograms deposited in moisture per square meter per day and averaged over the course of a year = mg/m²d) on the one hand and the concentrations of these elements in defined feather parts on the other are very close, at r greater than 0.9 on 17 sites containing precipitation collection stations in a wide variety of urban and rural landscape types in the Federal Republic of Germany.
As a result, it is now possible to measure pollution of the environment with lead and cadmium by analyzing only a few, or even a single goshawk primary (quill on the distal joint of the wing), and the accuracy and degree of differentiation of this diagnosis is in no respect inferior to the results obtained by automatic rain-collection apparatus with subsequent analysis of a large number of rainwater samples and statistical processing of the measurement values. It is nevertheless necessary to first perform such physicochemical analyses using suitable technology in order to absolutely calibrate goshawk feathers as highly integrative environmental indicators:
The results referred to here (Fig.9) are based on studies performed during a single season. Since then, they have been confirmed by repetition and their accuracy improved. It is also important to investigate the underlying physiological mechanisms which lead to a certain contamination level in a defined feather part. Both the seasonally fluctuating composition of the food ingested by the birds (ELLENBERG and DIETRICH 1982) and endogenous, presumably hormonally regulated annual cycles (COOKE et al. 1982) are likely to contribute to the observed phenomena. However, now that consistent trends have been identified in the varying contamination of individual feathers the attempt can be made to substantiate them by means of calibration and definition. We have undertaken to do this, of course without prematurely venturing an explanation of the physiological processes involved, by basing our results on the third primary quill, counting outward from the middle of the wing (ELLENBERG
et al. 1986; DIETRICH and ELLENBERG 1986). Recent studies of black-billed magpies have provided us with evidence to support the hypothesis that most of the measurable heavy metals contained in the feathers are actually collected directly from the air. The birds themselves may indeed play an active part in "working in" these substances as they clean themselves and prune their feathers each day (ELLENBERG and HAHN, forthcoming). This would elegantly explain the unusually close correlations between heavy metal concentrations in the feathers and the measured deposition rates. At correlation coefficients of 0.9 and above, significant food-chain-related effects were in any case unlikely, in spite of the apparent great individual variance in feeding habits among goshawks.
These results justify hopes that similarly close correlations will be found between pollution levels of other contaminants and their concentrations in goshawk feathers, as well as in other types of biological specimens. Biomonitoring and specimen banking are therefore useful concepts. With relatively little research at the biological and ecological levels, existing approaches could be considerably improved and understanding of them enhanced. Biological monitoring of all kinds cannot, however, dispense with calibration by means of physicochemical measurements.
Prospects and potential for applications in developing countries:
In the above, I have related how the close correlation between indicandum and indicator required by the definition of a bioindicator was established in a case that had initially been regarded as discouragingly complicated. The standardization of a highly organized warm-blooded vertebrate as a biomonitor of environmental pollution proved to be not only possible, but practicable as well. These results encourage us to venture the following hypotheses:
- Goshawks integrate the pollution levels in their territories, expressing them in one (or a small number of) specimen(s) - presumably not just lead and cadmium in feathers.
- Other organisms that roam large territories but remain loyal to specific sites possess similar attributes in this respect.
- Biomonitoring of environmental pollution is possible using animals with different ecologies, to corresponding degrees of temporal and spatial resolution.
- Migratory animal species can be used within the scope of remote sensing for biomonitoring of relatively inaccessible regions, provided that it is known where they dwell at certain defined times.
- Studies of specimen collections in museums or privately owned - which can have been gathered either systematically or at random - can grant us retrospective insights into past temporal trends and spatial patterns in pollution levels.
Based on the statements just made, concrete approaches with good prospects of yielding usable results with justifiable inputs in terms of time and funding can be formulated. I do not believe that this is the right time and place for this; nevertheless, I would like to stress - at the risk of repeating myself - that new hazards posed by the introduction of toxins to ecosystems cannot be detected by biomonitoring alone. The reason is that this kind of monitoring can only be applied to substances which have already been recognized as dangerous. New threats can only be discovered by surveillance of populations that can be assumed to be sensitive, e.g. birds, and in particular predatory birds. In many tropical settlement areas vultures (e.g. of the genera Necrosyrthes and Neophron in the Old World and of the genus Catharthes in the New World) are obvious candidates. Other organisms occupying highly specialized niches in food chains also deserve mention here: insect-eating shrews
and bats, for instance, as well as certain aquatic animals, especially fish-eating mammals and birds.
MATTHIESSEN's (1984) documentation of the situation in western Zimbabwe in connection with the use of DDT for tsetse fly control vividly portrays the threats which this has posed to free-living biota there, backed by objective analysis and data which THOMSON (1982) had presented in a concise and highly motivated manner at a conference of the International Council for Bird Preservation in Thessaloniki, Greece. Both THOMSON and MATTHIESSEN call attention to the hazards this entails for human beings who participate in local food chains. Human maternal milk samples taken from an urban population group in Salisbury contained on average 0.562 mg of DDT (and derivatives thereof) per liter. By way of comparison: in 1974 the highest DDT concentration ever measured in the milk of a single woman was rated at 0.569 mg per liter in the Federal Republic of Germany.
Direct studies of human beings are, without a doubt, just as important as biological and environmental monitoring efforts. Nevertheless, they fall within a different field of responsibility. Statistical and functional correlations between contaminant concentrations in human beings and those in wildlife populations must be systematically sought Specialized laboratories certainly also already exist in cities in developing countries that are capable of performing chemical analysis of pollutant residues in tissues. For collection of specimens and interpretation of the results astute field ecologists with galoshes and binoculars are needed who possess a thorough theoretical background and a knowledge of local conditions. Their aim should be: within the context of ecosystem research to carry out long-term monitoring of populations of carefully selected animal species to detect and document population fluctuations and to sound alarm if observed population fluctuations cannot be
explained with conventional theories. It is also important that capabilities be available for measuring the influx of substances into the ecosystem whether these are biocides or other toxins, or simply so-called nutrients. I have already sketched an example of how fertilization and the release of nutrients into the environment have led to a shift in the species composition of plant communities in Central Europe.
Such monitoring approaches, conducted within the scope of long-term ecosystem studies for the purpose of calibrating bioindicators that can aid in detecting and documenting environmental trends, even in less intensively researched areas, have already been under way for years in Sweden (SNV PM 1980). Discussion of similar approaches for application in the Federal Republic of Germany began towards the end of the International Biological Program (IBP), culminating in a comprehensive study published in 1978: ELLENBERG sen., FRANZLE, MULLER (1978) "Okosystemforschung im Hinblick auf Umweltpolitik und Entwicklungsplanung" (Ecosystem Research for Environmental Policy and Development Planning). This study, commissioned by the German Federal Ministry of the Interior, has consistently been quoted and acknowledged in appropriate contexts, yet for many years virtually nothing at all was undertaken to put into effect the measures and activities strongly recommended by the authors, who
had stressed that there was no time to lose. Only relatively recently have any such steps actually been considered, specifically in the form of a "man and the biosphere" program in the Alpen National Park (near Berchtesgaden) and in connection with the establishment of an environmental specimen bank (LEWIS 1984). Even more recently (in 1986), the Council of Experts on Forest Damage and Air Pollution (Sachverstandigenbeirat Waldschaden/Luftverunreinigungen) of the German federal government and the states has called for the establishment of a permanent institution for ecosystem research devoted to observing and investigating the ecological impact of the diverse substances which are released into the environment. Such an institution has not yet been established, however, unless one counts the working groups that are active at various university-affiliated institutes.
Other tasks must take priority' in many developing countries, however; there, it is first necessary to study and survey the status quo. My own personal opinion is that preference should be given to carefully prepared, systematic, large-scale - and therefore necessarily extensive - studies (with subsequent application of a catalog of criteria for selection of suitable biomonitor species) instead of too intensive local studies. However, such intensive studies are also needed to clarify local conditions, and their planning should begin without delay, since many unexpected obstacles to their implementation in the field are certain to be encountered. The study by ELLENBERG sent et al. (1978) provides concrete guidelines for the establishment of ecosystem study areas in response to environmental policy and development planning needs, as well as for calibration of bioindicators and biomonitors. The authors define a so-called "minimum program" which can be supplemented by other
measures that are also important but require greater inputs in terms of staff and equipment. The study is rounded out by 3 further papers that describe application of the approaches to aquatic ecosystems (FRANZLE et al. 1978), urban ecosystems (MULLER 1978) and terrestrial ecosystems (ELLENBERG sent and RUTHSATZ 1978). In spite of its relatively small size - 60 pages - I particularly recommend the paper on terrestrial ecosystems because of its pragmatic and practical orientation. Unlike the other two papers, many of the proposals made in it can be transferred with only minimal modifications to other parts of the earth (see the article by RUTHSATZ in this volume).
<section>5.4 Potential for use of biological monitoring techniques in developing countries</section>
The biological monitoring approaches which have been sketched so far, along with the results and prognoses which they yield, are concentrated on the levels of the ecosystem and the biocoenosis, as well as on those of populations and individuals. The coauthors in this volume present additional examples, some dealing with other biological monitoring levels. In this section, the author would like to briefly discuss the question as to the suitability of these and other approaches for application in developing countries. In the previous section, a few related aspects were already touched upon.
The problems associated with the use of pesticides should be a cause of concern in many countries. And they are indeed increasingly being recognized and the need for action acknowledged. But less violent and destructive methods for coping with nature and bothersome organisms are only slowly being adopted in the fields of agriculture and livestock management. For much too long, the industrialized nations have set a questionable example. Here, the shift away from "hard" poisons to use of traps made of blue cloth for selective capture of tsetse flies is an example of an apparently practicable and environmentally sound solution. This gives us reason for hope.
As long as persistent organochlorines continue to be used - and everywhere that they have been employed on a large scale in the past - biomonitoring (in the restrictive sense) is useful. This involves the assessment of the degree of contamination of food chains and the associated risks to human beings. For this purpose, attention is focused on predatory fishes and birds - at the terminal rungs of both aquatic and terrestrial food chains - because of their temporal and spatial integrative ability and because our knowledge of them is relatively great, but many other groups of species may also be suitable. Initial exploratory analyses of pollutant residues in the tissues of selected animal species can, in principle, be performmed on an ad hoc basis in any operational laboratory, even in the developing countries. In the beginning at least, advice from experienced ecologists is indispensable for selection of suitable animal species and tissue samples, and for interpretation of
the analysis results. This statement also applies to planning and implementation of systematic monitoring programs on the basis of what is reamed.
In addition to persistent pesticides, other pollutants in the environment can also be measured with the aid of biomonitoring techniques. The use of animals, which integrate pollution levels not only over the course of time - like plants - but also from large or small areas, can be advantageous, particularly for large-scale, extensive monitoring programs. Physicochemical measurements of pollutant deposition like those described above should be performed concurrently for calibration purposes.
In the sections on the future hazards posed by continued use of pesticides and on the use of birds as biomonitors of environmental pollution, I have sketched the interconnections and possibilities for action in sufficient detail. In connection with the contamination of food chains with toxins that cannot be readily metabolized, it should be kept in mind that in many developing countries most people nourish themselves from locally raised crops and domestic animals. Situations of this kind are particularly vulnerable to pollution of all kinds.
There is every reason to expect that biological monitoring techniques at the levels of individuals and populations can be directly transferred to the developing countries. Appropriate preliminary measures are needed to ensure selection of suitable species, adaptation of specimen-collection methods in the field, correct interpretation of the results, and adequate responses at the socioeconomic and political levels in the developing countries. Cooperation and the prospects of success of projects are enhanced if the donor countries provide continuous backstopping. It is also advantageous to link projects to existing institutions that are engaged in bilateral and/or multilateral cooperation.
At the population level, besides acute poisoning of individuals, other reactions to pollution are detectable, e.g. diminished reproductive success. Years ago, concern about such - initially inexplicable - declines in populations enhanced awareness of the necessity of in-depth studies, ultimately culminating in biomonitoring of the type sketched above. Yet, changes in population parameters can have a diversity of causes; in a great many cases they are related to changes in the availability and quality of species-specific food. For methodological reasons, hitherto unknown factors having an injurious effect on the environment can only be deduced from observations of the ecology of populations. For this reason, timely selection of animal species for monitoring of their populations is certainly warranted in many countries. Such a selection could be performed parallel to the other activities mentioned in the preceding paragraph.
Of important bearing on long-term monitoring of animal populations are the behavior and attitudes of the local population vis-à-vis the animal species in question. For example, fewer difficulties of this kind need be expected from persons whose worldview has been shaped by Hindu influences than is the case in some areas dominated by southern Europeans or their descendants. Biomonitoring programs oriented towards the ecology of populations do not present any fundamental methodological problems. Of course, they can run up against some practical difficulties at the local level, the severity of which must be individually assessed in each case. Nonetheless, monitoring programs of this kind represent invaluable "insurance" against the emergence of unknown "new" environmental problems, which can otherwise creep up on us, not making a full-fledged appearance until it is nearly too late to deal with them. Moreover, these programs can also greatly contribute to increasing the
environmental awareness of local population groups.
At the level of biocenoses and ecosystems, the approaches outlined above can, in principle, undoubtedly be transferred to the developing countries. In many cases, however, efforts to do so will be hampered by a lack of information on local conditions and/or practical obstacles. The phenological mapping techniques for land-use planning were developed specifically for the climate of Central Europe with its distinct seasons, in which temperature and heat dissipation gradients play the dominant role. In tropical countries, with their climate characterized by daily instead of seasonal cycles, these gradients will be important above all with respect to elevation and degree of exposure. Mapping of the distribution and developmental phases of selected wild - and local crop - plants can yield important data in this context. Other gradients, e.g. availability of water and/or plant nutrients, can also be described in this way. Just like in the case of temperature gradients, here too
studies employing measuring instruments are indispensable for calibration of the findings in the field. For these purposes, assistance from development cooperation projects active at the local level is more than just helpful and useful.
Although assessment of gradual changes in entire groups of flora or even fauna and their interpretation within the context of an ecosystem is a desirable goal to strive for in most cases, as a rule practical implementation of such programs is initially hindered by a lack of information. The gaps are inherently much wider in climatically moist regions with their much greater diversity of species than in dry climes. Floristic and faunistic surveys and descriptions at the local and regional levels are therefore prerequisites for attaining an understanding of ecological phenomena, and must be supported. Nevertheless, it is fairly easy to map and interpret changes in the spatial structure of the plant cover in the light of their microclimatic and geomorphological context. Apparently, in the developing countries such changes are usually caused not by gradual deposition of plant nutrients from the air- although many forest ecosystems would be naturally susceptible to such processes
- but instead by direct, violent intervention. Erosion and climatic problems have been commonplace in many tropical countries for decades. And their contribution to altering the climate on a global scale is increasingly becoming a focus of discussion.
In connection with development cooperation, scientific cooperation is for the most part relegated to university partnerships. The difficulties experienced in connection with such university partnerships appear to be due less to problems at the scientific level than to personal and/or political conflicts. They provide a good illustration of the obstacles that apparently must be consistently reckoned with, and not only in the initial stages of cooperation programs. The fact that such schemes are giving rise at all to concrete scientific results with potential for practical application is due first and foremost to the personal motivation and commitment of a handful of researchers. The value of such motivation cannot be overestimated. It cannot be bought, only supported - or, all too easily, destroyed. I believe that one of the highest-priority tasks of the Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ) GmbH is, or should be, to do its utmost to provide favorable
working conditions for the investigators in the projects it supports. Also crucial is the selection of the local project executing agencies by the host countries: ecosystem studies and biological monitoring in connection with environmental policy and development planning suffer greatly if largely controlled by persons whose primary motivation is to further their own selfish interests and for this very reason draw attention to themselves for being dynamic, successful individuals. The same problem exists where selection of organizations in the donor country is concerned. Biological monitoring also opens up possibilities for detecting "crimes against the environment", gathering evidence against their perpetrators, and thus for subjectively "incriminating" them. There is reason to expect that this could provoke a powerful backlash on the part of political and economic interests, who will vigorously oppose the "new methods". This opposition will raise its head as soon as
biological monitoring yields the first tangible successes. At this point, I would like to stress that this potential conflict can only be overcome if the involved scientists can be sure of lasting support, including moral support. The problems at the personal and political levels which interfere with cooperation between individuals and countries also require attention. The success of all cooperation efforts depends on how these problems are dealt with.
<section>6. Conclusions</section>
Biological monitoring is, when applied creatively to uncovering new interconnections and links, a complex process. Routine pragmatic work with bioindicators can only develop on the basis of a thorough understanding of ecosystems and experience with nature at the local level. Many of the world's leaders today have been deprived of the chance to benefit from either of these during their formative years. Moreover, not everyone is capable of recognizing patterns and interconnections - as a rule, schools promote only rote memorization and analytical skills. Understanding of ecosystems as the foundation for local and regional economic development must therefore be systematically fostered for specific landscapes (cf. DASMAN et al. 1973). This is not only the task of research institutions, which after all generally produce primarily "new" results, but also and most importantly an indispensable prerequisite for appropriate large-scale, intensive action, and is thus of relevance for
organizations like those involved in development cooperation. An understanding of socioeconomic effects and limitations must be sought in connection with management of each ecosystem (HALLSWORTH 1982). A number of extremely interesting ideas are presented under the heading of "ecotoxicology" by the British biologist F. MORIARTY (1983). BALK and KOEMAN (1984) have provided a concise summary of the potential risks of continued pesticide usage, based on their experiences in West Africa and Southeast Asia. The strategy of excluding only national parks and other conservation areas from the all-pervading rain of pesticides cannot possibly be conducive to the aims in question. Problems like the development of resistant strains, harmful side effects, and extinction of species do not come to an abrupt halt at the borders of conservation areas.
Many idealistic persons and institutions all over the world are now being motivated to work for the protection and preservation of attractive plant and animal species. Indeed, it would be in the interests of the national economies of the industrialized nations and of the Third World as well - to promote such endeavors, particularly in those countries that permit, out of necessity or because they are still in the process of developing the expertise to assess the ecological implications, over-utilization of resources, use of toxins, and production of hazardous waste without imposing any restraints or obstacles. As more and more regulatory and restrictive ordinances and legislation are introduced in the "developed" countries, the temptation of interest groups and companies will grow to shift their environmentally hazardous operations to areas without such restrictions. Here, the economic interests of countries and businesses enter into a situation of conflict that can even lead
to countries or states vying to underbid one another, each boasting less restrictive environmental legislation than the next. We have witnessed this very phenomenon within Germany in connection with the industrial "development" of the lower course of the Elbe River. Within this context, biological monitoring is, strictly speaking, only capable of describing the same problems in other words. A long road remains ahead, in both the industrialized countries and the so-called developing countries, until we have available to us the required comprehensive catalog of ecological restrictions for economic development activities. Biological monitoring could play a central role here. The first steps have already been made in this direction, and further steps can now follow. I hope that the present volume at least succeeds in presenting enough of the possibilities to serve as a source of inspiration.
Improved environmental policies, biological monitoring, protection and preservation of ecosystems in a natural or close-to-natural state, and the promotion of all of these within the scope of development cooperation in the world's developing countries are justified by direct, idealistically motivated interest in the species, biocenoses and humans living there. But a direct economic motivation to act is also beginning to take shape: as long as no consideration is given to the environment (or need be given, due to a lack of regulations) in connection with production and recycling of goods, industrial production in the developing countries will have a competitive edge over the domestic economies of the industrialized nations. Economic reasons therefore also exist for exporting awareness of the necessity of conserving intact ecosystems and the know-how required to do so from the industrialized countries to the countries of the Third World. This represents a rare opportunity to
clonely link idealism and pragmatism for the good of the greater whole.
Both the idealistically and the economically motivated would be well-advised not to set their hopes too high, however. Understanding and management of ecosystems must be based on in-depth, object-oriented and long-term observation and research. If ecological insights are fed back to the economic sphere, in the long term it is possible to expect better cooperation between the two. It is not enough for the basic biological needs represented by healthy air, healthy water and healthy food for human beings, including infants and the elderly, to be met; in the future it is also vitally important for the threshold values for utilization and management of the environment to be increasingly determined at the sociological, economic and political levels - and this must be done within the scope of international cooperation.
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<section>Concept for a biological monitoring study:</section>
by Barbara Ruthsatz Coauthor: Hildegard Wey
Determination of the extent and long-term impact of pollutant discharges from mining and metallurgical operations on croplands and pasturelands on the central Andean plateau by means of biological indicators and analysis of their vital processes.
<section>1. The nature of the problem and background information</section>
<section>1.1 The conflict between mining and agriculture on the Andean plateau</section>
The Andean plateau or tableland, variously called the Altiplano, altoplanicie or puna in Spanish, has been populated and altered by human beings for thousands of years (ELLENBERG 1979; RUTHSATZ 1983; TROLL 1943). Ever since the emergence of the Tiahuanaco and Incan civilizations, population densities have been determined by the humidity of local climates, since livestock raising, field cropping and horticulture represent the principal sources of livelihood. Even today, this basic pattern remains virtually unchanged, in spite of the fact that administrative and commercial centers have developed at the junctions of transportation routes.
The only major exceptions to this are the mining and metallurgical industries. Precious and semiprecious metals (gold, silver, copper and tin) were already being extracted and processed by the first advanced Indian civilizations. Following the conquest of the region by Spain in the 16th century, mining became the driving force behind the exploitation (and overexploitation) of all of the natural resources of the Andean plateau. Manpower, food and fuel had to be supplied in order to sustain the mining activities (e.g. in Potosi). The availability of new energy sources such as petroleum later reduced the dependency of the mining industry on the recruitment of laborers from elsewhere adapted to the high-elevation climatic conditions, and a supply of food coming in part from the Andean plateau.
During the past centuries, the focus of mining activities has shifted several times. Today, extraction of industrially used metals such as Sn, Zn, Pb, Sb, W, etc. has become far more important than mining of precious metals, with production rates being largely governed by the going prices on the world markets. As a consequence of the long history of mining activities of various kinds, in addition to active mining operations the remnants of abandoned or temporarily shutdown mines can be found scattered throughout the Andean plateau. Contamination of the Andean plateau with pollutants emanating from these thus has, in addition to a current spatial distribution, a temporal component which is much more difficult to assess.
The contaminants from mining operations and associated processing and metallurgical plants include, most importantly, heavy metals, Jluorides, sulfur dioxide and various secondary substances, such as sulfates and other salts which result from processing of the minerals. The contaminants can be discharged either into the air or into aquatic systems. Frequently waste and tailing dumps can act as secondary sources of contaminatian. since fine materials can be blown out by the wind or leached out by percolating water. Contaminants can also be scattered from the roads and railways along which ore and waste are moved; frequently, ore which has been concentrated in flotation processes and/or pulverized is transported in open-top trucks and railway cars.
Figure 1: Mining area near Uyuni (southern Bolivia). Here mining and agricultural activities are conducted side by side.
Figure 2: Mina Aguilar (in thc Argentinian province of Jujuy). Shown here: the mineral processing plant (molino) and tailing dump (cola) on the lower right.
The toxicity which heavy metals, fluorides, and sulfur compounds and other secondary substances have Jor the affec ted plants animals ecosystems and/or humans varies considerably depending on the class of contaminants and the overall pollution situation. The most important deleterious effects of many different contaminants are fairly well-known, however, and have been extensively discussed in the literature (ADRIANO 1986; FOWLER 1983; HUTCHINSON, MEEMA 1987; LANGARD 1982; LEPP 1981; LONERAGAN et al. 1981; MERIAN 1984; MISLIN, RAVERA 1980; NRIAGU 1986; MURRAY 1982; TRESHOW 1985; TSUNODA, YU 1986: UBA 1976, 1977, 1983; VETTER 1982; WALDRON 1980).
One of the paths by which gaseous and particulate contaminants are transported is through the air. Depending on the substances involved, the prevailing wind directions and velocities, and the morphology of the terrain, once contaminants have been released into the environment they can remain locally contained or spread to affect large areas. The second important transport path is by way of effluents which are channeled into rivers and streams. The thus contaminated water may occasionally be used further downstream for irrigation of pastureland or crops, or spreads beyond the banks to flood extensive valley floor areas during the rainy season. In this way, the contaminants reach and penetrate yet more terrestrial ecosystems. Moreover, during the dry season large quantities of contaminants which have accumulated in sandbanks in these rivers and streams can be scattered by the wind.
In the long term, long-range transport of contaminants and low but chronic pollution lelvels probably represent a more serious problem than acute contamination with high concentrations of toxins in the immediate vicinity of mining and metallurgical operations.
The population of the Andean plateau is either not at all or is insufficiently aware of the dangers which this poses (Fig. 1). The reason we selected this particular aspect for study, out of the broad spectrum of environmental problems amicting developing countries today, is because of information which we received from herdsmen and farmers in the puna of Argentina and Bolivia. They had noticed that their sheep and goats no longer found suitable forage on the pastureland of the leeward side of the Mina Aguilar (Jujuy province, Argentina) and were developing diseases (Fig. 2). It is there that fine dust enriched with heavy metals (Zn, Pb, Cd, etc.) from the waste sludge of flotation processes is scattered on windy days during the dry season (over distances of at least 30-50 km) and deposited.
On the Altiplano of Bolivia, we received reports that the water of certain rivers, along the upper course of which a number of mining operations are situated (e.g. the Coro Coro River), is no longer suitable for irrigation purposes, and that the rivers have also lost their previously abundant fish populations. It has not been possible to confirm these observations, but we regard them as credible. The poisoning of important links in the food chain, e.g. of primary producers such as algae, can in turn threaten the existence of those groups of organisms which depend on them as a source of nourishment. The accumulation, or biomagnification, of contaminants as they are transferred through food chains can have similarly drastic consequences for the populations at the end of the chains. In all probability, the unsuitability of the water of these rivers for irrigation purposes can be initially attributed more to salts which have been channeled into it, in particular sulfates, than
to increased heavy metal concentrations. In many cases, the deleterious effects of the latter are not likely to be immediately recognized as such, but in the long term they pose an equally great threat to grazing livestock and human beings. Reports from the fertile river valleys in northern Chile of heavy metals and other pollutants being present in drinking water and agricultural crops have recently been increasing.
All of the rivers overflow during the rainy season, inundating large areas of the central Bolivian tableland and the Guayatayoc-Salinas Grandes basin in northwestern Argentina, which has no outlet to the sea, and deposit their sediments there. Within certain limits, this can be observed along the middle and lower courses of all rivers of the region. The best pastures of the Andean plateau are located on just such annuallyflooded or percolated alluvial lands. Their gradual enrichment with contaminants of low solubility, which accumulate in fine-grained humic soil, could eventually impair the natural productivity of the soils. The same applies to pastures and croplands with a deep water table that are polluted by airborne contaminants.
Today, the principal long-term threat to ecosystems caused by heavy metal pollution is regarded as being the disturbance and inhibition of dec omposition and mineralization processes in the soil. As a result, availability to the plants of the nutrients locked in the organic matter of the soil diminishes or ceases altogether, and the productive potential of the sites diminishes. This is a self-amplifying vicious cycle. The most sensitive link in this food chain is probably that comprised by soil fauna, which initially serve only to more or less break down the plant litter (EDWARDS 1982; EIJSACKERS 1983). Because they reproduce so rapidly, many soil microorganisms, namely algae, bacteria and fungi, exhibit a high degree of genetic adaptability. Within just a few days or weeks, contaminant-resistant populations can develop among them (BABICH, STOTZKY 1985; DOELMAN 1986; DOMSCH 1984; TYLER 1981). However, they too are subjected to a reduction in numbers of species and diminished
growth rates.
But the human population of the Andean tableland is dependent on the natural productivity of the pastures and croplands, since predominantly subsistence farming is practiced and, after the most basic needs have been satisfied, not enough income is left over for purchase of fertilizers. Even more so than the immediate acute threat to plants, animals and human beings posed by pollutants discharged by mining and metallurgical operations, we therefore consider this long-term harm to the ecosystems of the Andean plateau, which are overexploited in any case, as giving particular cause for concern.
The Andean tableland is of varying significance for the economies and populations of the countries of the region. Bolivia probably has the greatest interest in maintaining the fertility of the soil, since most of its population lives there and the economic stability of that country is also highly dependent on the mining industry (above all tin and silver extraction). The Andes play a similarly important role in Peru, but the more or less flat tableland in the strict sense of the term as used here ends in the north at the watershed of the Lake Titicaca basin. Only a relatively small portion of the A/tipluno proper is in Peru. although that portion is densely populated because of its favorable, high-rainfall climate, which permits agricultural produclion on a significant scale (meat and wool from alpacas, llamas and sheep). In Argentina, it is above all the provinces of Jujuy and Salta which contain areas of the puncl. The agricultural activities practiced there can be
described as marginal, and today arc barely sufficient to meet the nutritional needs of the local population. The younger male members of nearly all of the families work partor full-time in the mining industry or in the sugarcane plantations and similar large-scale farming operations h1 the neighboring lowlands. On a national scale, the importance of the Argentinian punu is derived solely from exploitation of the mineral resources which occur there (Zn, Pb, S, Cu, sodium chloride. potassium salts, borates. etc.). The minim industries, is nevertheless still dependent on laboreres native to the Altipicino. since lowland residents are barely able to adjust to the high elevations (4,000-5,000 m) while performing heavy labor (BAKER. LITTLE 1976). The Argentinian puna is very sparsely populated, however, because of the extremely unfavorable living conditions there (undernourishment, high child mortality, the long distances that must be traveled to market wool, etc.), and it is
therefore becoming necessary to recruit miners from Bolivia and Chile.
Because the Bolivian plateau is so densely populated and plays such an important economic role, highest priority really should be placed on studying heavy metal pollution there; unfortunately, however, the prerequisites for successful implementation of such a pilot study there are not satisfactorily met (due to lack of an adequate scientific and technical infrastructure).
<section>1.2 Scope of the case study concept</section>
To date, no scientific publications whatsoevcr have appeared dealing with the local, regional and large-scale impact which mining and metallurgical activities on the Andean plateau have on the structure and function of the probably atf`ected ecosystems. This does not exclude the possibility. however, that the industrial operations being conducted there, the responsible authorities, the affected towns and villages, and possibly experts commissioned by these to carry out studies, possess information on thc levels and range of distribution of contamination in individual cases, as well as on its probable impact. Unfortunately, without official sanction it is impossible to obtain access to this information.
In all likelihood, legislation exists in the aft`ected countries that stipulates guidelines and requirements for mining and metallurgical operations. It is to be expected, however, that attempts to enforce such stipulations would encounter yreat difficulties in practice. The economic dependence of these countries. or at least some parts of them, on the prices commanded on the world markets by the raw materials found in their territory usually interferes with or prevents outright the putting into practice of legislation aimed at protecting the environment. The fear is that compliance with the requirements could increase the costs of production. The responsible agencies quite certainly possess the necessary know-how on the technical aspects of carrying out measurements of pollution levels and implementing measures to reduce introduction of contaminants into the environment. The larger operations in this branch of industry have been and continue to be, for the most part, set up
with the help of foreign capital, and are frequently run under the technical supervision of experienced foreign firms. The situation is likely to be different with small private enterprises, however (GTZ 1983).
A review of the scientific literature available on pollution of the environment with heavy metals revealed quite clearly that it is primarily in those countries of Europe, North America and Asia which already have a long history of successful industrialization that detailed studies have been performed on contamination of the surroundings of mining and metallurgical operations (ARCHIBOLD 1985; FREEDMAN, HUTCHINSON 1980; NRIAGU 1984; ROBERTS, JOHNSON 1978; VETTER et al. 1974; WOOD, NASH III 1976). In several other countries, studies of contamination of coastal waters with heavy metals from industrial operations have also begun (countries bordering the Mediterranean and North Seas). This also applies to the South American countries of Argentina, Chile, Brazil, Venezuela and Peru (cf. e.g. ARES et al. 1983). Apparently, other branches of industry (fishing and tourism) are increasingly being affected by the pollution of seacoasts and are able to audibly voice their interests. The
growing worldwide "environmental awareness" thus also has a basis in the material interests of certain sectors of the economy!
The lack of basic information on pollution emissions and effluents and their impact on the ecology of the surroundings of mining and metallurgical operations on the Andean plateau is therefore not an indication of the insignificance of this problem complex, but instead merely an expression of the current lack of possibilities for working towards its solution. We therefore considered it to be important to concern ourselves with this topic, and to point out in this context - responding to the urgent need for such approaches - how plants can be meaningfully used as biological indicators for assessing the extent of pollution and its impact on ecosystems.
During the last 10 to 15 years, an enormous amount has heen learned ahout the suitability of methods involving the use of plants as biological indicators for evaluating the spatial and temporal gradients of contamination of the environment with toxins. In addition to a plethora of publications dealing with locally restricted studies, several general surveys and compendia dealing with this field have also appeared (ARNDT et al. 1982; BEST, HAECK 1983; BURTON 1986; GUDERIAN, REIDL 1982; MANNING, FEDER 1980; MARTIN, COUGHTREY 1982; SALANKI 1986; SCHUBERT 1985; STEUBING,JAGER 1982).
On the basis of this literature and the personal familiarity of one of us (RUTHSATZ) with the Andean plateau, we have been able to develop a study approach for bioindicator-assisted evaluation of healy metal contamination originating from identifiable sources.
The elaboration of such a pollution survey requires, first and foremost, thorough preliminary information on the local and regional physical structure of the area under study and the anthropogenic factors influencing it. This includes data on the relief, climate, vegetation, soils, current land use and land-use history of the area. This must be supplemented by basic data on the physical and chemical behavior of the contaminants in the atmosphere, water, soil and selected bioindicators.
Up to a certain point, in this way quite different classes of contaminants can be monitored together using the same phytomonitoring methods. This approach has already been successfully applied to heavy metals and some persistent organic compounds (ELLENBERG 1987; SCHRIMPFF 1984; THOMAS 1983). Interpretation of the results must then be performed separately for each individual contaminant, however.
Such a pollution survey must not be the final goal of a biomonitoring study, however. On the contrary, it only represents the necessary basis for investigation of the impact of the contaminants on the affected ecosystems and groups of organisms.
While a pollution survey can be performed using physical methods or techniques of analytical chemistry - although these are usually associated with considerably greater costs and by no means yield absolutely reliable results - this is not possible when elaborating an environmental impact inventory. Both the choice of the ecologically relevant functional parameters of the studied ecosystems and the interpretation of the results obtained in this way call for thorough familiarity with the structure and function of the ecosystems. Moreover, such investigations on the effects of contaminants depend greatly on the specific properties of these substances and the specific reactions of the organisms in the individual ecosystem compartments to different contaminant concentrations.
If it is possible, by means of comparisons with other, thoroughly studied ecosystems that are sufficiently similar in structure, to identify particularly important and contaminant-sensitive organisms and/or processes (ELLENBERG et al. 1983; SHEEHAN et al. 1984), then the biomonitoring approach used can be confined to these.
Depending on whether protection of species and ecosystems per se is the goal, or whether attention is focussed on the possibilities for short-term and long-term use by humans of the affected ecosystems, it will be necessary to investigate additional compartments of the system. These include, for example, contaminant concentrations in plants used by humans and domestic animals and the long-term effects of contamination on their growth. Even if there is no deleterious effect on plant growth, high concentrations of substances that are transferred through the food chain, ultimately becoming toxic to domestic animals and human beings, make it imperative to take precautionary and remedial action.
While we were developing that part of the study model intended to focus on the long term effects of contamination (cf. section 3.3) the lack of hasic informalion on the structure and function of the ecosystems of the Andean plateau and on the ways in which they are influenced by climatic factors and soil properties proved to be a particularly major disadvantage (BAKER, LITTLE 1976). Similar semiarid tropical highaltitude landscapes exist, above all in Mexico and Ethiopia. But no transferable analyses of the ecosystems of those countries are available either. The continental steppes and semiarid high-altitude landscapes of the temperate zones of North America and Asia have a similar outward appearance, but due to the seasonal alternation of summer and winter their production rhythms possess different ecologically relevant attributes.
This dearth of directly related and transferable information on important aspects of the steppe and semidesert ecosystems of the Andes makes it essential for this deficit to be compensated for hy conducting hiomonitoring case studies of the impact of contaminants on the affected ecosystem functions on a correspondingly inroad scale.
In spite of the fact that we have so far stressed the impact - especially the long-term effects - of contamination on the structure and function of the ecosystems of the Andean plateau, by necessity we have been forced to leave a number of major aspects entirely or largely out of consideration. This applies especially to the important functions performed by arthropods, spiders and many other soil fauna in connection with the predominantly mechanical processing of accumulating dead organic matter (litter), as well as all aspects related to transmission of contaminants through food chains. This is, without any doubt, a major drawback of this study, and could and should he overcome hy supplementary zoo-ecological investigations.
Because of our professional specialization in the field of plant ecology, we have been obliged to confine our investigations to the use of plants as hioindicators for surveying and cataloging pollution and its effects, supplemented by the necessary meteorological and vegetation studies and chemical physical and microhiological soil analyses. Within the scope of the proposed model for study of the long-term effects of contaminants, the focus is on the reactions of the primary producers in the affected ecosystems and of certain microbiologically controlled mineralization processes which are involved in the decomposition of organic matter and play a relevant role in the recycling of nutrients in the soil. These aspects are rounded out by studies of microclimatic and soil attributes affecting plant growth and the mobility of contaminants within the ecosystems.
The study concept presented here has been developed as a model for studying the semihumid to semiarid, subtropical Andean plateau, and within this context is tailored to investigations of the effects of heavy metal pollution. With some modifications and/or additions, it would probably also be applicable to other tropical or subtropical landscapes and classes of contaminants. A few examples of this are listed below:
a) In the Lake Titicaca region, in the vicinity of large Andean cities such as La Paz or Cochabamba, and in the arid warm Andean valleys where intensive irrigated farming of vegetable and fruit crops is practiced, the use of chemical pesticides has become increasingly widespread. Like in many other tropical countries, the use of these substances does not appear to be subject to any effective controls or restraints. Due either to insufficient knowledge or irresponsibility, the amounts of pesticides applied and the times of application only rarely comply with health regulations governing the sale of products intended for human consumption. These products then make their way to domestic - and to some extent even foreign - markets without any checks or controls. The health hazards which these practices pose for the populations of the farming regions themselves are probably even more serious. Therc can be no doubt that it would be important and worthwhile to carry out studies
with bioindicators to assess the degree of contamination of food chains with heavy metals (e.g. from fungicides) and organic compounds in these regions.
The arid warm Andean valleys in which irrigated farming is practiced are situated at elevations between 2000 and 3000 m, and from the biogeographical angle are of an insular nature. They are flanked by precipitous mountain slopes, and as they descend into the lowlands they merge into the permanently moist tropical rain forest areas. Depending on the morphology of the valley floor, the transition to the punu region is more or less abrupt. Gradients of contaminant concentrations have therefore developed perpendicular and parallel to the longitudinal orientation of the valleys. Here, special mountain-valley-wind systems are likely to have a differentiating effect on the distribution of contaminants. In particular, these probably contribute to transporting airborne particulate matter and gases more strongly in an ascending direction following the course of the valleys than in the opposite, descending direction.
b) Similar conflicts exist between mining and agriculture in much of the moister parts of the Andean highlands, which in Peru are more strongly dissected. There, overall precipitation is greater and distributed more evenly over the course of the year, and this influences both the transport and the impact of contaminants. The accumulation of contaminants in plants and soils is probably also affected. The vegetation of these areas is more luxuriant and richer in species. The plants used as bioindicators and the sampling dates would have to be adapted to the prevailing climatic conditions there in order to ensure results that lend themselves to meaningful interpretation.
c) In principal, the study model presented here can be applied to all treeless grasslands and heath-like landscapes in which low shrub vegetation predominates. The same holds for the formerly forested, now treeless rangeland and areas used pnmarily l`or growing field crops at places in the chaco lowland and elsewhere. The main sources of pollutants there are the petroleum industry, sugar refineries, etc.
<section>1.3 Major criteria for biomonitoring of pollution caused by mining and metallurgical operations</section>
In view of the apparent lack of available infomlation on the topic of concern here, the first step would have to be a preliminary study. Plants that are suitable for use as bioindicators would have to be looked for, and their response ranges calibrated. So much is already known about the use of bioindicators for assessing pollution levels, however, that such studies could be performed in a highly directed and efficient manner.
First, representative polluted areas around typical contaminant sources must be selected. The following criteria should be applied:
- National and/or regional importance of industrial operations.
- Exploitation and/or processing of frequently extracted minerals (e.g. Zn, Pb, Sn, Cu).
- The extraction and processing methods typically used in the region (e.g. flotation, calcination, roasting).
- The known historical development and current production volume of operations.
- The typical location of operations in the region and the relief of the probable polluted areas (e.g. mountain slope descending onto a plain).
- The ways in which the probable polluted areas are typically utilized in the region (e.g. pasture only, mixed pasture and arable, primarily arable).
The next step is to delimit the range of contamination and determine the extent of its environmental impact (by elaborating a catalog of contaminants and their ecological effects). For this purpose, plants are suitable that have a high degree of resistance to the contaminants under study, filtering them out of the air and accumulating them in or on their leaves. It is initially irrelevant whether the plants capture the heavy metals from the air or (also) absorb them from contaminated soil horizons. Widely occurring low shrubs and grasses enter into consideration for passive monitoring, and the so-called moss bag test or barley crops grown under standardized conditions are suited for active monitoring. This should be supplemented by studies of the uppermost soil horizon. As soon as the main direction of dispersion and the effect of the relief on contamination levels can be approximately assessed, instead of testing in a grid pattern covering the entire area it would be
possible to use pollution gradients selected on the basis of this information. This would significantly reduce the number of samples which have to be taken.
On the basis of experience with similar mining and metallurgical operations, the series of those contaminants which can definitely be expected and those which may possibly also be present should be determined, and if possible the presence and concentration of all of them investigated in the bioindicators and the soil. The intensity and type of the discharged contaminants can vary considerably depending on the mineral composition of the mined ores and the ways in which they are processed. Elements that fail to be accumulated or only occur in low concentrations can then be excluded from subsequent studies. At the same time, this permits more realistic assessment of the risk of synergistic effects occurring among different contaminants.
All contaminant concentrations measured in soils, plants and animals must be calibrated against the background contamination levels from natural sources in the area under study. This poses no problems for a number of substances of overwhelmingly anthropogenic origin, such as many pesticides, provided that long-range dispemion does not play a role. When studying the heavy-metal contamination of an area, it is essential to possess accurate knowledge of the chemical composition of the rocks in the area as a benchmark for measuring the proportion of anthropogenic pollution.
Once the nature and intensity of contamination in the area surrounding a pollutant source are approximately known, more specialized studies must follow. To this end, it is necessary to search for bioindicators that react differently to different pollution levels so that the degree of contamination over the entire area can be mapped in greater detail (calibration of sensitive bioindicators) and an inventory can be compiled of the effects of contaminants on plants, animals, human beings and key attributes ot the affected ecosystems, above all in order to be able to assess the long-term consequences of the contaminant burden (long-term area studies).
The search for organisms that respond with varying degrees ot sensitivity along largely known pollution gradients can be conIined to recording their presence or absence in relatively unpolluted anti highly polluted areas, or also incorporate the degree of damage which they suffer. A well-known example of this approach is mapping of lichen distribution in densely populated areas. Lichens react very sensitively to SO2 pollution, but are also harmed by fluorine and high concentrations of certain heavy metals (FEIGE 1982; KERSHAW 1985). Lichen mapping could conceivably be carried out, at least in the moister northern part of the Antlean plateau.
Nothing is yet known about sensitive organisms native to the study area. It is most likely that sensitive herbaceous plants exist. Vegetation surveys carried oul by one of us (RUTHSATZ 1977) on the plateau area adjacent to the Mina Aguilar showed that the typical formation there namely semidesert with low shrubs, is particularly poor in annual and perennial herbs. We had previously attributed this exclusively to the prevailing unfavorable climatic coliditions (i.e. Iack of warmth and frequent below-freezing temperatures). There could also be a connection with heavy metal contamination, however.
Where very high contaminant concentrations are present in the immediate vicinity of sources, it may be possible to expect the occurrence of so-called geobotanical indicator plants which are also utilized for prospecting of ore deposits. Unfortunately, much too little is still known about heavy-metal indicator plants in the Andes region, which means that here too there is no body of knowledge on which to draw.
The use of bioindicators should focus on analysis of the ettects of contaminants on crop plants. domestic animals and utilized ecosystems, in other words without losing sight of the fact that human beings are the final link in the chain of transference of environmental pollutants. On a long-term basis, chronic contamination of more distant areas with lower pollution levels is more serious than acute short-term damage to plants, animals and soil fauna in the more heavily contaminated immediate vicinity of sources.
Initially, it is not so much the higher plants (primary producers) that are affected by such conditions, but instead those organisms which are responsible for decomposition and mineralization processes in the soil, thus ensuring an adequate supply of anorganic nutrients from decaying organic matter (litter, etc.), as well as autotrophic and heterotrophic soil algae. Soil-biology methods have proven to be effective for investigating the activities of these organisms (BECK 1968; NOVAK 1972; STEUBING, KUNZE 1980). Higher plants are indirectly affected by the lack of nutrients resulting from diminished microbiological activity in the soil, and herbivores in turn suffer from the lack of forage. An overall reduction in production can gradually take place. The full extent of these injurious effects does not become visibly apparent until after contamination has persisted for some time, however. Even then, it can only be accurately assessed by means of long-term monitoring and/or
comparisons between polluted and unpolluted areas. For the purpose of clarifying this important aspect, we recommend monitoring of long-term study plots. Such studies could, at least to some extent, make use of the methods which have been tried and proven on the Andean tableland by the Institute of Ecology in La Paz (a GTZ bilateral project).
It is also very important to obtain information on the historical development of contamination on the Andean plateau. In a number of parts of Europe, during past centuries methods have been tested for detecting contamination within a historical time frame. The following are examples of objects which have been used to determine heavy metal concentrations:
- moss samples from Scandinavian herbariums and outdoor sites: RUHLING, TYLER 1969,1971,1984
- annual rings of trees: ARNDT, WEHRLE 1982; HAMPP, HOLL 1974; HOLL, BAUCH 1977; HOSTER 1979
- lake and river sediments: MICHLER 1984
- peat strata: DAMMAN 1978; GLOOSCHENKO 1986; LIVETT, LEE, TALLIS 1979; WANDTNER 1981.
Of these methods, analysis of peat deposits would be most likely to yield usable results in connection with studies on the Andean plateau.
In addition to using approaches involving bioindicators for determining contaminant levels in the ecosystems and their living elements (compartments), it is also essential to carry outfurther studies of local and microclimaticiactors and of soil attributes in the study areas in order to gain an understanding of the overall picture. The pathways and rates of contaminant dispersal, pollution levels, rates of accumulation, the mobility and availability and the acute or chronic toxicity of contaminants are greatly dependent on climatic and edaphic conditions in the affected areas. Unless this background information is available meaningful interpretation of the results of bioindicator studies is impossible. In view of the present lack of relevant information on the climate and soil of the Andean tableland, such accompanying studies are indispensable.
The study program proposed here is organized in such a way that, depending on local requirements and the available time and funds, different investigatory methods can he derived involving va~ying expense and efforJfor use of bioindicators to detect heavy metal contamination. It would go beyond the scope of this paper, however, to describe these analytical methods in detail. For many plant and soil studies, it is possible to choose from among several different methods depending on the objective of the study and the available laboratory equipment and/or outdoor measuring instruments. The references made to the literature are therefore restricted to a few standard works on methods of plant and soil analysis, as well as certain special methods which have proven their effectiveness in the fields of plant ecology and soil microbiology.
Parallel to the measurements of contamination levels with bioindicators, standardized technical procedures for determination of wet and dry contaminant deposition should also be used. Although these cannot be reliably used to "calibrate" the results of biomonitoring, since all of them are only accurate within certain tolerances which can be large or small depending on the method used, it would at least permit comparisons with pollution measurements made in other regions.
<section>2. Study area: the central Andean plateau</section>
<section>2.1 Location and extension</section>
The great mountain system of the Andes extends the full length of the western part of South America, being nearly 8000 km long and occupying an area of over 2 million km2. To the west, it drops off steeply into the narrow coastal plains along the Pacific. The eastern cordillera, by contrast, is partially fringed by hilly country which merges into landscapes consisting of extensive basins and river systems.
The cent/al Andes comprise that part where, approx. between 130 S and 23° S, the mountain ranges broaden to an overall width of 400 km. The central Andes entend from southern Peru across parts of Bolivia and Chile all the way to northern Argentina. In the following, those major attributes of this region are described which are of relevance for the topic under discussion.
<section>2.2 Natural features</section>
2.2.1 Geology and relief
2.2.2 Climate
2.2.3 Soils
2.2.4 Vegetation
2.2.1 Geology and relief
In contrast to the more strongly dissected southern and northern Andes, the central Andes are characterized by high plateaus at elevations hetween 3400 and 4300 m above sea level (GOMEZ MOLINA, LITTLE 1981). This Altiplano or altoplanicie is bounded on the west and east by cordilleras with peaks rising to between 5000 and over 6000 m above sea level. Mountain ranges running in a north-south direction divide the Altiplano up into a number of basins which, depending on their respective climatic conditions, have either a lake (e.g. Lake Titicaca, Lake Poop6) or salt marshes (e.g. Salar de Uyuni, Salinas Grandes de Jujuy) in their middle, if they have no outlet to the sea. Geologically, the study area forms a trough filled with sedimentary material up to 15 km thick. Its present topographical structure is only about 4 million years old. It is believed that the Andes were formed, and continue to be formed, by underthrusting of the Nazca Plate beneath the South American Plate.
This process began about 200 million years ago, accompanied by violent volcanic activity. As a result, the Paleozoic schists, sandy shales and sandstones were joined on the surface by andesitic igneous rock rich in deposits of various ores (AHLFELD 1,967; PUTZER 1976). The volcanic activity took place in several phases. It was most intense 50 to 60 million years ago, resulting in formation of the western flank of the Andes. The western cordillera (Cordillera Real) is younger than the eastern cordillera (Cordillera Oriental), and its surface structure is still not fully stabilized, as is evidenced by the continued presence of active volcanos at a number of points. During the Tertiary (about 15 million years ago), siliceous magma was pressed to the surface in the central and northern parts of the Altiplano and in northern Chile, thus further increasing the diversity of rock types and parent materials for soil formation.
2.2.2 Climate
Descriptions of the climate of the high-elevation regions of the Andes are contained in PROHASKA (1976) and JOHNSON (1976); climatic diagrams and further references are provided by RUTHSATZ (1977, 1983) and ERIKSEN (1986).
The climatic situation of the Andean zone is determined by its location within the zone of subtropical summer rains, enormous land masses extending to considerable elevations, proximity to the Pacific Ocean, and the Humboldt Current. The combined effect of all of these factors is to give the Altiplano a dry and a wet season, a gradient of increasing overall precipitation and number of months with rainfall (an increasingly pronounced continental climate) moving from the northeast towards the southwest, as well as a succession of different climatic zones depending on altitude and direction of exposure. At elevations of 3700 - 3800 m above sea level, the northern portion of the Andean plateau, in the vicinity of Lake Titicaca, receives annual rainfall of between 600 and over 800 mm, most of which falls during 7 to 9 months of the year (subhumid climate). Extensive periods of complete dryness or drought do not occur during the remaining months of the year, however. The mining
city of Oruro, at about the same elevation but located further to the south, receives annual precipitation of just under 400 mm - there,7 months of the year can be classified as dry (semiarid climate). In the southern portion of the northern Argentinean puna, the total annual precipitation of about only 100 mm is concentrated in just 2 months (subarid climale).
The flora and fauna of the Andean plateau must be adapted to periodic lac k of water, as well as to a general lack of warmth and below-freezing temperatures which are of brief duration but occur almost daily. The mean annual temperature in these high-elevation zones rarely exceeds 10 °C. Daily temperature fluctuations between +40 °C and -10 °C at ground level are common, even during the growing season. The average daily minimum temperature in Oruro (3708 m above sea level) is -11 °C in July (during the dry season) and +4 °C in January (during the rainy season). The corresponding daily maxima are 14 °C and 19 °C, respectively.
During the rainy season, easterly and northeasterly winds prevail, which can become quite strong and gusty during thunderstorms. During each dry season, several windstorms sweep in from the west, sometimes continuing unabated for days at a time. They blow dust and sand out of the dry river beds, the vegetation-poor salt marsh landscapes, and degraded pastureland, and can sometimes cause the formation of extensive dune fields. They also pick up dust containing ores from the dried-out decantation basins and waste dumps of mining operations, and disperse them over large distances and extensive areas. On a local scale, mountain and valley wind systems play a major role, especially during the dry season. Following a calm period during the morning hours, by noon at the latest strong winds arise that blow up through the valleys and do not lessen in intensity until late in the evening. The reciprocal katabatic winds during the night are much weaker.
The other typical characteristics of high-altitude climates include increased insolation, especially of the shorter wave lengths (ultraviolet), reduced air pressure, and thus less available oxygen, carbon dioxide and nitrogen than in lowland areas.
2.2.3 Soils
A detailed discussion of Andean soils in Bolivia is given by COCHRANE (1973), and specific aspects of the soil nutrient cycle are dealt with by SALM (1983a, 1983b). All of the other publications which have appeared on the soils of the central Andes are very general treatises.
The principal parent materials for soil formation in the Andes are volcanic ash and metamorphic and igneous rock. A typical attribute of Andean soils is their short developmental history. A number of factors have a negative effect on soil development, including extreme temperature fluctuations, lengthy dry periods, high wind velocities, and an almost complete lack of closed vegetative ground cover. The diversity of soil types occurring in the region under study is further enhanced by the wide range of elevations and climatic zones. On a regional scale, the relief (affecting water-induced erosion and sedimentation) and the degree of exposure both play an important role.
In very broad terms, the western slopes of the central Andes are covered with desertic soils (Regosols, saline soils), while on the eastern slopes the moister climate has permitted the development of Brown Forest soils. The central portion of the Altiplano exhibits soils which are transitional between these two types. Deposits of volcanic ash are superimposed on the soils of the southern, semiarid part of the central Andes. Azonal soils occur in dune, salt marsh, alluvial plain and bog areas.
The arid climate inhibits leaching of the soils. The result is generally a good supply of bases (WINTERHALDER, THOMAS 1978). Soil humus content is frequently low, however, and the production of inorganic nitrogen and phosphorus compounds available to plants is moderate to low.
Degradation caused by overgrazing has been going on for centuries everywhere on the Andean plateau. In addition, in arable areas the extensive fallows contribute to loss of topsoil by sheet erosion.
2.2.4 Vegetation
Scientific descriptions of the vegetation of all or parts of the Andes exist dating back to the beginning of the century. A bibliography of references for the Andean plateau is provided by RUTHSATZ (1983).
In general, the vegetation formations of the Andean plateau can be described as montane semideserts in which the plant cover rarely grows higher than 40 to 60 cm, usually with ground coverage of less than 50% (Fig. 3). With increasing overall precipitation and shorter dry seasons the proportion of bunch grasses and various herbaceous plants grows. With increasing aridity, there is a greater percentage of mostly evergreen, sclerophyllous, small-leaved shrubs. In extremely arid areas there is a conspicuously high proportion of low thorny shrubs, which at the same time usually have a greater tolerance of saline soils.
Above 4500 m, the prevalence of lou'shrahs rapidly decreases. At even higher elevations, the mountain slopes are generally covered with hunch-grass steppes, which are more or less open depending on the supply of water. Above about 4900 m the plant cover becomes patchy, with cushion plants and specially adapted hardy herbaceous plants inhabiting more favorable local sites where warmer temperatures prevail.
Azonal alluvial land and flood plains have a dense gramineous cover which often merges directly into the halophytic plant communities of the extensive, more arid basin landscapes. Dune areas can, depending on their salinity levels, be populated by shrubs or distinctly sclerophyllous grasses. In depressions and on moist slopes which derive their water from springs or seepage, so-called hard-cushion bogs have developed, which are composed not of mosses like many bogs of the temperate zones, but instead of stunted, cushion-forming sedges, rushes and herbaceous plants.
Taller shrubs, trees or even forests are very rare today, but originally were probably much more widely distributed on the semihumid northern plateau and on well-protected sites in the central and southern regions. They have fallen prey to logging and extensive livestock grazing practices. The extent to which anthropogenic influences have shaped the current vegetative cover of the Andean plateau is greatly underestimated by foreign visitors and the population of the region itself, occasionally even being denied completely.
Figure 3: Semidesert brush formations in the puna near Abra Pampa (in the Argentinian province of Jujuy). The dominant plant is the shrub Fubiana densa. In between grow various perennial grasses and other shrubs.
As a consequence of the relatively unfavorable climatic and soil conditions, as well as overutilization of the vegetation by humans, the plants which predominate today exhibit a high degree of resistance against:
- Periods of dryness.
- Low nutrient availability (N, P).
- General lack of warmth.
- The ground frosts of brief duration which occur throughout the year.
- Soil salinity.
- Browsing by animals.
As a consequence of their morphological (small, rolled and folded leaves, low and stunted growth, low shoot/root ratio, etc.), anatomical (leaves with thick cuticles, multiple-layer palisade parenchyma, high stomatal density per unit of surface area, pilosity, etc.) and ecophysiological adaptations, most of the dominant plant species can be described as highly xeromorphic and/or sclerophyllous.
<section>2.3 Population</section>
The central Andean plateau covers parts of 4 countries: Peru, Bolivia, Chile and Argentina, of which Chile has the smallest part and is therefore not dealt with in the present study. Only in a few cases is it possible to correlate the statistics on the national demographic and economic structures of these countries with this natural geographical region. Since the Altiplano is most important for Bolivia in terms of population and economic activities, data on this country will be taken here as the basis for depicting the Andean plateau. Unless otherwise indicated, all of the data presented here on social and economic structures have been obtained from the STATISTISCHES BUNDESAMT (1984).
The population densities of the Andean countries are low compared with European countries (Table 1). There are considerable regional variations, however. While the coastal regions of Peru and Argentina have the highest population densities, the population of Bolivia is concentrated on the Altiplano.
On the Altiplano, local population densities are principally determined by the possibilities for growing food crops. These in turn depend on the distribution of precipitation and the frequency and intensity of nocturnal frosts (PRESTON 1973; RUTHSATZ 1983; the latter source also contains maps).
Even today, Indians still account for most of the population of the Andean plateau. The reasons for this are in part historical; the advanced civilizations of the Incas were based there. Another reason is the remarkable physical adaptation of the Indians of the Altiplano to life at high altitudes (BAKER, LITTLE 1976).
Table 1: Population densities in Bolivia, Peru and Argentina
Population
Inhabitants
Population in the Andean region
in mill.
per km
per km²
% of overall population
Bolivia
Peru
Argentina
Table 2: Employment structures in Bolivia, Peru and Argentina
Employment by economic sectors (%)
Economic sector
Bolivia (1976)
Peru (1981)
Argentina (1977)
Agriculture, forestry, fishery
Manuracture and production(mining)
commerce, banks, etc.
Administration, public services
Miscellaneous
Compared to the contribution of agriculture to Bolivia's gross domestic product, a relatively high proportion of this country's working population is employed in this sector of the economy, namely nearly 50%. In Argentina, where the chief exports are agricultural products, productivity in this sector is significantly higher than in Bolivia. The relatively high percentage of the gainfully employed population working in Bolivia in the mining and quarrying sectors reflects their great importance for the export-dependent Bolivian economy (Table 2).
On the Bolivian Altiplano, landownership is characterized by a high degree of fragmentation, especially near settlements, and communal pasturelands in areas that are unsuited for arable use. Prior to the Bolivian revolution of 1952, part of the land was owned by public institutions, with private individuals rarely holding title to land. In most cases, "comunidades indigenas" performmed the dual function of owning the land and organizing land use. The effect of the agrarian reform on the settlement structure was decentralization (establishment of scattered settlements), and where ownership structures were concemed it led to transfer of land titles to the rural population itself, especially in the central departments of La Paz, Potosi and Cochabamba. One factor which still interferes with definitive clarification of the landownership situation on the Altiplano is the continued existence of traditional grazing rights in certain areas, a fact which must be taken into account
when applying for land to be used as study plots, especially for longterm projects.
<section>2.4 Agriculture</section>
The major source of livelihood of the population of the Altiplano is agriculture. Productivity is constrained by a number of natural factors, above all:
- extreme climatic conditions (dryness and cold, frosts)
Figure 4: The mosaic of agricultural land use on the Bolivian Altiplano near Huaraco (north of Oruro). Dry farming predominates in thc scmihumid part ot the Altiplano, with long fallow periods during which the fields are pastured.
Figure 5: Pastureland on the alluvial plain of the Rio Desaguadero south of` Huaraco on the Bolivian Altiplano.
- infertile soils (poor nutrient availability, low humus content, risk of salinization) - the susceptibility of vegetation-poor areas to soil erosion.
The population has adapted to conditions on the Altiplano by developing a mixed and highly diverse system of crop and livestock raising (Fig. 4). At higher elevations, the lower rainfall, greater aridity and lower temperatures cause extensive livestock raising to gain in importance over the growing of crops.
In addition to indigenous crops, especially tubers and Andean orache, several European crops are also grown (RUTHSATZ 1983). Livestock is grazed on mountain slopes at elevations of up to above 4500 m above sea level. During the winter dry season, the "hard-cushion bogs", which are to some extent artificially irrigated, and alluvial plains represent the most favorable pasturelands (Fig. 5). The intensive grazing practiced in these ecosystems, which are relatively unproductive in any case, can lead to serious damage by erosion (ELLENBERG 1984; MILLONES 1982; WENNERGREN 1975).
The food produced in the Andes is barely sufficient to meet the nutritional needs of the farmers and shepherds themselves. A few products make their way to local markets, but with the exception of wool (alpaca, lame and sheep), the agricultural products of the Altiplano are of virtually no importance for export.
Besides the above-mentioned natural constraints on agricultural production, other negative factors are an inadequate network of roads and a lack of capital for purchase of fertilizers and pesticides. The only exceptions are areas in the immediate vicinity of larger cities, and the climatically more favorable area around Lake Titicaca.
While production of barley, potatoes and dried beans increased sufficiently between 1963 and 1972 to keep pace with population growth, the supply of the indigenous crops of oca, quinoa and papalisa has significantly worsened (WENNERGREN 1975). Bolivia's population is expanding so swiftly, however, that much higher growth rates are needed in the agricultural sector. Iligh priority must be assigned to conserving soil fertility, which is being jeopardized by European farming methods that aggravate the ongoing erosion, by overgrazing and possibly, an aspect which remains to be investigated, by the influence of environmental contaminants.
<section>2.5 Mining and industry</section>
The Andes are rich in ore deposits of many kinds. Major deposits are centered in the mountainous country of southem Peru, Bolivia and northern Argentina (PUTZER 1967, 1976) (Fig. 6). The Chilean ore deposits are located on the western slopes of the Andes.
The number of mines currently in operation in Bolivia is estimated by AHLFELD (1965) at 2200, although only 2% of these can be regarded as large operations. In Bolivia today, most of the large-scale mining operations are owned by the state mining corporation (Corporacion Minera de Bolivia, COMIBOL). The total number of mines has probably declined in the last 20 years, since many veins have already been exhausted. In Argentina as well, the mining operations of major economic importance are also state owned. Many small and frequently unprofitable mines are operated by private owners, with production rates that are subject to great fluctuations (GTZ 1983). New developments in the field of ore prospecting indicate the presence of uranium deposits on the Altiplano which could feasibly be exploited (PARDO 1981).
In descending order of importance, the following metals are extracted on the Altiplano: tin, zinc, silver, tungsten, antimony, lead and copper; all other metals account for only an insignificant proportion of the extracted ores (Fig. 7).
In order to evaluate the economic value of a mine and decide on the most appropriate processing technique, the most important criterion is the ore content of the extracted material. As a rule, this declines at increasing depths below the surface and thus with the amount of time during which a mine has been operated. When mining of tin first began in Bolivia (in 1905), only ores with tin concentrations of at least 12% were subjected to further processing. By the time between the two World Wars, the tin content had dropped to 4-6%, and since 1960 in general only low-grade ores with 0.5-0.6% of tin are extracted (AHLFELD 1965). It can be reasonably assumed that the metal content of the waste and tailings of the ore dressing processes in each case has decreased proportionally. Many old mine dumps and mill-tailing piles, originally regarded as worthless, are now again regarded as valuable, especially since the treatment methods have also been improved.
During recent years, the decline in productivity has spawned intensive, internationally supported prospecting activities which have also led to the discovery of rich mineral deposits in many locations, with the consequence that new mines are currently being established.
The extracted low-grade ores are dressed prior to transport in order to concentrate their valuable constituents into products of smaller bulk. This process, in which the various different ores are separated from one another and as much worthless material (gangue) is collected out as possible, is energy-intensive and therefore also very cost-intensive in the Andean plateau region, which has little wood and no coal deposits or petroleum reservoirs.
The roasting, flotation and filtration methods used result in discharge of contaminants into the atmosphere (often liberating considerable amounts of airborne dust), and contaminants find their way from waste dumps into the soil and aquatic systems, also being blown into the air once the sludge has dried.
Since the tin deposits of the "Bolivian tin province" are associated with considerable amounts of sulfides and arsenic, these compounds can be emitted into the atmosphere during the course of the separation processes, in part in gaseous form, and in part as particulates. Very little information is contained in the literature on the composition and amounts of emanated contaminants and their impacts on the terrestrial and aquatic systems of the Andean plateau. The only exception we were able to find is the description given by MILLONES (1982) on water contamination (fish mortality in the Mantaro river) and the deleterious effects caused by atmospheric contaminants on 700,000 ha of pastureland in the vicinity of the tin mine and ore mill at Oroya, Peru.
<section>2.6 Special aspects of environmental contaminants, their effects on living organisms and ecosystems, and their detection by means of bioindicators on the Andean plateau</section>
In many respects, living conditions on the Andean Altiplano are extreme and comparable with those of only very few other regions on the earth's surface. Because of these special conditions, a number of questions arise which can only be answered by experts specialized in other disciplines, although they are very likely to have a major bearing on studies involving bioindicators. In the following, afew of these problems are briefly discussed.
It is difficult to assess the extent to which the much lower atmospheric pressure at elevations between 3,500 and 5,000 m above sea level has on the dispersion of gases, particulates and aerosols, in particular the question as to whether this fact tends to shorten or extend the range of contaminant distribution, all other conditions being equal.
Extremely high levels of insolation occur for brief periods during the rainy season on clear and slightly cloudy days. During the dry season the peak insolation values are somewhat reduced, but of longer duration. This fact could enhance the oxidation of photochemicals, thus leading to synergistic effects that compound the harm already being done to organisms by other toxic substances. The literature available to us contains no data on ozone levels on the Andean plateau. It is possible, however, that such data exists for Mina Aguilar in Argentina, where a measuring station for cosmic rays is operated.
The short-term, considerable temperature fluctuations, which can amount to as much as 50-60 °C at ground level, cause intensive mechanical weathering and disintegration of rocks and minerals. We are not in a position to judge whether this has any effect on chemical reactions involving contaminants in the air and in the soil.
Frosts and lack of water have a similar desiccating effect on plants, as a consequence of which the indigenous plant species have developed protective adaptations. It is also known that sclerophyllous plants frequently have a particularly high resistance to atmospheric contaminants, since they are able to effectively regulate and/or greatly reduce the exchange of gases with the ambient air, thus also preventing absorption of the pollutants. This applies especially to SO2 and HF contamination, but could possibly also influence their degree of resistance to heavy metals.
The periodically occurring dry periods on the Andean plateau cause the organisms living there to interrupt their activity. During times of extreme dryness, most of the plants and many animals as well go into a state of latent vitality. They are then also largely insensitive to contaminants, since they either do not absorb them at all or at least do not actively metabolize them. Although the intensity and range of contamination can be greater during periods of dryness for a number of reasons, it is quite possible that they do not actually affect the organisms until during the following growing season, probably most strongly following the flrst rains in the spring (September to November).
Where the nutrient situation of higher plants and soil microorganisms is concerned, contamination with heavy metals can reduce phosphate availability, which is very low in any case, even further, thus slowing growth even before injurious effects are caused directly by the heavy metals themselves. Although the soils generally contain an adequate to good supply of bases, in many places calcium availability is quite low due to the chemical composition of the parent rock. Fluorine interferes with metabolization of Ca and Mg by the plants by binding with the calcium to form the relatively insoluble compound caF2, which then precipitates. Consequently, where there is already a deficiency in native calcium reserves in the soil fluorine contamination can result in damage to otherwise relatively insensitive plants. It is to be expected that other interactions between nutrient supply on the one hand and resistance to contaminants on the other hand will occur in the plant life of the
Andean plateau.
Little is known about the volcanic ash content of the soils of the Altiplano. Soils rich in ash, however, have a high sorption capacity for organic substances and certain anions, especially phosphates, molybdates and sulfates. On the other hand, within certain limits it can be expected that fixation of cations will be less than in other soils lacking in volcanic ash. Accumulation of heavy metals is thus also unlikely; instead, they would probably be washed out into enrichment horizons.
In general, erosion by water and wind play a much greater role in semiarid areas than under moist climatic conditions. The development of a closed vegetative ground cover on the Andean plateau is inhibited in any case by the general scarcity of water, and this has been aggravated for centuries by overgrazing and farming practices involving extensive fallows. Convective rain showers in the rainy season and windstorms during the dry season can everywhere lead to secondary redistribution of already deposited contaminants, and hence secondary contaminant sources must also be expected in pollution areas.
The intensive year-round grazing practiced in all parts of the Andean plateau makes it difficult to carry out comparative studies with healthy, intact rangeland plants, since there is insufficient vegetation for investigation purposes. In order to obtain cumulative bioindicators, therefore, it is necessary to resort to certain widely distributed plants species that are ignored by grazing livestock during the rainy season. Due to a general shortage of forage during the dry season, however, nearly all of the plants are then eaten. One possible alternative is to fence in study plots to protect them from browsing by grazing livestock.
The result of the prevailing dry farming practices with extended fallow periods is that, in the semihumid to semiarid portions of the Altiplano, there are few areas that remain unploughed for longer than 10-15 years. Long fallows indicate that the sites involved are infertile. The only soils that are not farmed are those that are very shallow and stony or clayey with a tendency to salinization. As a consequence of these farming practices, any accumulated contaminants are spread through the upper 15-20 cm of the soil profile, thus making it difficult to obtain evidence of long-term contamination. When selecting study plots it is essential to take this fact into consideration. If necessary, the local residents should be asked; it is not always possible to clearly distinguish between older fallows and pastureland that has never been ploughed.
<section>3. Study approaches</section>
<section>3.1 Studies of the range of distribution and relative intensities of current environmental contaminatron emanating from a source</section>
3.1.1 Moss bag accumulation test for contaminants
3.1.2 Accumulation of contaminants in shoots and leaves of living plants
3.1.2.1 Evergreen low shrubs
3.1.2.2 Summergreen deciduous shrubs
3.1.2.3 Perennial bunch and rhizome grasses
3.1.2.4 Perennial herbaceous plants
3.1.2.5 Annual grasses and herbs
3.1.2.6 Annual crops
3.1.2.7 Mosses and lichens on the ground and on rocks
3.1.3 Exposure of barley culture pots (active monitoring)
3.1.4 Contaminant enrichment in the topsoil
3.1.5 Mapping of contamination zones by means of damaged lichen vegetation
3.1.6 Animals as accumulative bioindicators (brief survey)
3.1.7 Accompanying vegetation studies
3.1.8 Accompanying soil studies
3.1.9 Accompanying climatic studies
When choosing the methods to be used, the unique aspects of each pollution situation, the dispersion behavior of the pollutants which are probably being discharged into the environment, the relief of the surrounding landscape, the local climatic conditions, the vegetation cover of the area probably affected by the contaminants, and its use by human beings must all be taken into account. The greater the number of factors included in the preliminary study phase and the denser the network of sampling sites is, the easier it will be to develop a monitoring program from the measurement results which will be suited to the situation at hand.
In Central Europe, good results have been obtained by superimposing a grid of squares on the area surrounding a source; each of the squares should measure 500 m on a side, and the total area of the grid should be 16 km² (STEUBING et al. 1983). Such a grid approach is well-suited for preliminary studies on the long-range dispersion of contaminants. It may provide insufficient accuracy, however, for differentiating the environmental impact of the contaminants in the immediate vicinity of the source, and in general if the terrain has a particularly high relief ratio. Depending on the object of investigation, the lay of the land, and the possibilities for study, either this method or that described in the following may be better suited for assigning the sampling sites.
As an absolute minimum, at least two different indication methods should always be used and their results compared. The samples for this can also be taken from two (or four) transects approx. 30 km long running SW - NE and SE - NW (as well as possibly also S - N and E - W) which cross at the contaminant source. The sampling sites can be 200 m apart up to a distance of I km from the source, 1 km apart up to a distance of 5 km, and 5 km apart up to a distance of 30 km from the source (Fig. 8). With this density, 52 (or 104, depending on the number of transects) samples are taken at each sampling date. All of the sampling sites should be at least 100 m from the nearest heavily travelled road in order to minimize contamination of the samples with toxins from automobile exhaust. If mountain ridges cross any of the transects at right angles, then the sampling sites must be selected in such a way as to give adequate consideration to both the leeward and windward slopes. It can be
expected that there will be a higher incidence of contaminants on the slopes facing towards the source.
If great precision is desired, then the most straightforward approach is to investigate contamination levels in the vicinity of a source by using sampling sites distributed in a grid pattem; the reason is that local wind conditions may not always pemmit easy derivation of the principal dispersion pathways. With this sampling scheme as well, the density of the sampling sites can be varied in inverse proportion to the distance from the contaminant source, e.g. with grid squares measuring 250 m on a side within a radius of 1 km, 500 m on a side within a radius of 5 km, and 1000 m on a side within a radius of 10 km from the source. In this way, more than 500 samples are obtained for each test series. It is of course also possible to combine this approach with the transect method at even greater distances from the source.
In the following, a number of biomonitoring tests are briefly discussed which have proven their worth in Europe and North America for detection of heavy metal and fluorine contamination, and which provide an even greater wealth of infommation when used in combination. In order to permit at least a rough distinction between assimilation of contaminants by plants from the soil and from the atmosphere, we suggest beginning by studying plants that are not rooted in the ground. Since there is a lack of trees and thus also of epiphytic plants in this area, there is no altemative to hanging out plant specimens in which the substances under study will accumulate (moss bags, cf. section 3.1.1). For the most part, this technique can only be used for monitoring of current atmospheric contamination levels. Other tests are available for analysis of atmospheric contaminants that accumulate over varying periods of time in plants and parts of plants without producing visible hammful effects
(cf. sections 3.1.2 and 3.1.3).
In addition to discharging heavy-metal dusts into the atmosphere, smelting operations also emit gaseous contaminants such as SO2 and HF. The rates at which this occurs must be measured using either the same (HF) or other tests with bioindicators. Since enrichment of sulfur in leaves does not necessarily correlate with SO2 emissions (FREEDMAN, HUTCHINSON 1980; KNABE 1981), one way of obtaining information on the distribution of this contaminant is by mapping lichen distribution. Unfortunately, however, this is probably only possible in the moister parts of the Andean plateau, where sufficient numbers of lichen species occur (cf. section 3.1.5). Lichens are ideal indicators, however, since different species also react sensitively to fluorine and heavy metal contamination.
In order to pemmit meaningful analysis of the test data, a number of additional studies on climatic and soil factors must also be perfommed. The distribution and impact of pollutants are greatly dependent on weather conditions, and their accumulation in plants depends on water and nutrient availability (cf. sections 3.1.7 and 3.1.8). In the case of a number of heavy metals, the soil can also be regarded as a source for their enrichment in plants that root in it (cf. section 3.1.9).
3.1.1 Moss bag accumulation test for contaminants
This approach makes use of moss species that exhibit a high order of branching and are not protected by an outer coat or layer. Samples of the same size and shape are placed in fine-meshed plastic bags and hung between bushes or stakes, and the rise in their contaminant content determined after a predefined exposure duration (MARTIN, COUGHTREY 1982; GAILEY, LLOYD 1986). The moss varieties which have been much used in Europe for this include Sphagnum spp., Hypnum cupressiforme, Hylocomium splendens and Rhytidiadelphus spp. In the Andes, epiphytic mosses of the sub-Andean cloud forest zone (between La Paz and Coroico) or Sphagnum samples from other parts of the country could be used. The moss bags should be hung on a level with the top height of the vegetation (20 to 50 cm above the ground) or, if necessary for their protection, on posts 2 m above the ground, so that livestock cannot reach them and also so that wind values measured at weather stations can be directly
correlated with the accumulation rates. The duration of exposure of the samples can be fixed at 4 or 6 weeks, or extended to a period of months. The criteria for this decision should be the specific attributes of the expected heavy metal compounds, contamination levels and climatic rhythms likely to affect accumulation, in order to permit meaningful interpretation of the results.
Prior to placing the samples in the field, their initial contaminant concentrations must be measured. Heavy metal, fluorine and sulfur compounds have varying propensities to being accumulated and/or leached out again (e.g. by acids, during the rainy season), depending on their particle size, chemical properties and the concurrent presence of other pollutants. Consequently, for the most part the accumulation values only provide an indication of the relative intensities of the individual elements at different distances from the source. Mosses have a large cation absorption capacity, however, so that useful information can be obtained on various heavy metals, especially lead and copper, and possibly also for zinc, cadmium, etc.
3.1.2 Accumulation of contaminants in shoots and leaves of living plants
Numerous studies have demonstrated that the leaves of higher plants also collect contaminants. These are filtered out of the air and accrete on external and internal surfaces. Epidermal structures and substances (hairs, scales, resins) are particularly likely to play a part in this process (FREEDMAN, HUTCHINSON 1980; PRINZ, SCHOLL 1978; VETTER, MAHLHOP, FRUCHTENICHT 1974).
Because of the differences among plant species, each study should include several, but consistently the same, species. A number of plants found on the Andean plateau are suitable for this, including certain widely distributed evergreen and deciduous shrubs, perennial and annual grasses and herbaceous plants, as well as epigeic and epilithic lichens and mosses. The leaves of different plants persist for varying periods of time, thus probably permitting collection of data on shorter and longer pollution periods. The leaves of most of the shrubs are quite small, however, and hence it is necessary to analyze shoot tips with scale leaves of known age. Interpretation of the accumulation rates is made more difficult by weather conditions and differing displaceability of the contaminants in aqueous media, in diluted acids, as complex organic compounds, by transport or fixation in plant tissues, etc. The usefulness of the results can be significantly improved by prior determination
of the initial contaminant levels in the plants, by making use of overlapping accumulation periods, and by simultaneously studying the levels of several contaminants in different plant species (LEPP 1981). It is essential to ensure that the exposure conditions of the studied plant parts on the external surfaces of the selected shrubs, grasses, cushion plants, etc. are comparable (height above the ground, the direction they face (e.g. north, south, east, west), degree of coverage by neighboring plants, etc.). Nothing is known about passive or active assimilation of contaminants by the plants of the Andean plateau from polluted soils. In the case of Cd and Zn, however, this is likely to play a role (MISLIN, RAVERA 1986). All of the mentioned species are more or less avoided by livestock, and thus can probably be found even in heavily grazed areas. Examples of suitable plant species and collection times are discussed below:
3.1.2.1 Evergreen low shrubs
Baccharis incarum: dioecious; develops ecotypes; widespread on sites with very low or absent water table, growing throughout the entire puna from Argentina to Peru.
Parastrephia lepidophylla: in subarid to semiarid areas confined to alluvial plains with an accessible water table, in subhumid zones also occurring together with other low shrubs on normal sites; ubiquitous in the dense and higher-growing vegetation of the river plains. The other Parastrephia species occurring on the Andean plateau stock on other sites, and the structure of their leaves varies. Some of them may exhibit similar accumulation rates, however, although this would first have to be experimentally confirmed.
Collection dates: at the end of the main growing season (April-May) and at the end of the dry season (September-October).
3.1.2.2 Summergreen deciduous shrubs
(Some are only facultatively deciduous, depending on the intensity of dryness).
Fabiana densa: shrub with acicular leaves. Widespread in the subarid and semiarid regions of the puna on sites far from the water table. Other Fabiana species are nearly leafless, have more pronouncedly resinous shoots, and colonize extremely arid sites. The accumulation rates of the various species of this genus cannot be readily compared with one another because of the differing size and structure of their surfaces. Determination of the age of the shoot apices could possibly be difficult, thus making it harder to correlate the accumulation data with a defined time span.
Baccharis boliviensis: low shrub with acicular leaves. Widespread in the subarid and semiarid areas of the puna on sites far from the water table, somewhat more demanding than Fabiana densa with respect to summer warmth and water supply, but nevertheless often associated with this species. Forms leaves that are resistant to dryness and possibly also to cold (var. latifolia).
Tetraglochin cristatum: low shrub with clusters of needles on short shoots. Widely distributed throughout the entire puna on sites with clayey, to some extent compacted, soils. It is probably represented by subspecies with varying degrees of resistance to aridity. Determination of the age of the leaves and shoot parts could possibly be difficult.
Collection date: end of the main growing season (April to May).
3.1.2.3 Perennial lunch and rhizome grasses
In the case of grasses, it is essential to make a distinction between vegetative (leaves) and reproductive (flowers and fruits) organs, since they store different quantities of contaminants. There is a great diversity of gramineous species on the Andean plateau, and hence it is very possible that other species may be suitable for sampling purposes besides those widespread ones mentioned below. The aerial parts of most of the grasses die back during the dry season, which has a higher frequency of nocturnal frosts; only on sites with accessible water tables do the lower portions of the leaves and shoots occasionally remain green throughout the year.
Stipa ichu: a widespread pasture weed that grows in bunches on sites far from the water table in the puna, with very narrow, flexible leaves that grow densely together.
Festuca orthophylla: a pasture weed which grows in bunches on sandy sites in the puna, with or without the influence of the water table, with very stiff, hard leaves. Represented by subspecies with varying degrees of resistance to cold and dryness (in the alpine zone in the distinctly continental south: F. eriostoma). Its accumulation ability is possibly low; moderately salt-tolerant.
Festuca dolichophylla: a moderately good forage grass that grows in bunches in the semihumid to subhumid areas of the puna up into the lower alpine zone; this range is probably made possible by the existence of ecologically distinct subspecies.
Pennisetum chilense: a soft-leaved rhizome grass that grows in patches in the semiarid to subarid parts of the puna, with high fodder value; occurs on sites with deep, sandy soils and periodically accessible groundwater.
Collection dates: end of the main growing season (April to May) and if required at the end of the dry season (September to October).
3.1.2.4 Perennial herhaceous plants
The diversity of the perennial herbs is so great, and their distribution often so limited, that it is difficult to recommend suitable species that could be used throughout the region. The frequently occurring clustered and semiclustered species are not likely to be suitable as cumulative indicators, since the exposed surface area of their leaves is small and any enrichment with contaminants would probably be derived from the soil which they grow upon.
Regionally common, upright pasture weeds which are avoided by livestock, such as Astragalus garbancillo and several Senecio species (e.g. S. adenophyllus) could also prove to be suitable. Astragalus garbancillo is reported to actively accumulate selenium from the soil.
Collection dates: end of the main growing season (April to May).
3.1.2.5 Annual grasses and herbs
The same statements hold for this class of plants as for the perennial herbs. A wide diversity of species exists in the Andes, and the distribution of the individual species is for the most part regionally restricted. However, since some of them represent an important food reserve for livestock during the winter months, their contamination levels could also be of interest. Possible sampling plants: Aristida adsc ensionis, various Cumochaeta species, etc.
Collection cute: end of the main growing season (April to May).
3.1.2.6 Annual crops
A number of indigenous and European annual crop plants are cultivated on the Andean plateau as a source of food for humans and fodder for cattle, and occasionally also for sheep. Dry farming is practiced where there is sufficient precipitation, and elsewhere with supplementary irrigation, especially during the spring and early summer. The most widely grown crops are barley, potatoes and Chenopodium quir?oa. Since these plants, either directly or indirectly, provide nourishment for humans, their concentration of contaminants in the vicinity of corresponding pollutant sources is of particularly great concern. It is therefore important to include them in studies as cumulative bioindicators, especially since a great deal is already known about the absorption, distribution and storage of contaminants in the individual organs of barley and potato plants (LEPP 1981; UBA 1976, 1977, 1983).
It should be taken into account, however, that the fields are not uniformly distributed over the land; instead, cropping depends on the presence of suitable site conditions and the fallow rotation practices in the individual communities. In the area around Lake Titicaca and on the central Bolivian plateau adjoining to the south, at elevations between 3600 and 4100 m above sea level up to about the elevation of Oruro it will be necessary to make finer distinctions with barley, potatoes and quinoa nearly everywhere, since the different varieties certainly exhibit varying accumulation properties and degrees of resistance. It would be highly advisable to restrict studies to one or a limited number of varieties.
When taking samples and subsequently analyzing them, it will be necessary to distinguish among leaves, shoots, fruit bodies and tubers, since the accumulation properties of these organs generally vary for the different contaminants, and the contaminants also wind up being channeled into different food chains.
Collection date: usual harvest date of the crop.
3.1.2.7 Mosses and lichens on the ground and on rocks
In the semihumid and subhumid central and northern parts of the puna, as well as in the vegetation zone above it, mosses and lichens occur frequently enough to be used as accumulative bioindicators. Because of their slow growth, their low growth form which closely follows the substrate on which they are found, and difficulties in distinguishing between the annual growth zones, it is rarely possible to draw conclusions on contaminant absorption from the soil or the air, or during a defined time span. Exceptions to this rule could be large-lobed foliose lichens (SCHWARTZMAN et al. 1987). Nevertheless, it is likely that some species with a high degree of resistance to heavy metals are able to accumulate and store increasing amounts of certain contaminants over lengthy periods of time. They could therefore be useful for determining the relative contamination of different parts of an area, an approach which has been successfully utilized in several investigations in densely
populated parts of Europe and in the surroundings of metallurgical operations (mosses: CAMERON, NICKLESS 1977; MASCHKE 1981; RICHARDSON 1981; THOMAS 1981, 1983; lichens: ADDISSON, PUCKETT 1980; FOLKESON 1979; GARTY 1985; cryptogams in general: RASMUSSEN et al. 1980).
Nothing is yet known, however, about the interrelationships between enrichment and washing out of substances; each of these processes is liable to vary depending on the substance under study, the plant species, its specific growth situation, and the climatic and weather conditions. For these reasons, the sampling procedures should be standardized as far as possible in order to obtain comparable data on accumulation rates.
Collection dates. end of the rainy season (April to May) or end of the dry season (September to October).
3.1.3 Exposure of barley culture pots (active monitoring)
In order to ensure genuinely comparable accumulation conditions, genetically uniform and standardized plants must be raised. These are then exposed in the field along contamination gradients. In Central Europe, good results have been obtained with the grass Lolium multiflorum for study of accumulation of heavy metals, sulfur and fluorine (PRINZ, SCHOLL 1978; VDI 1978, 1979).
In the semiarid to subhumid parts of the Andean plateau, it would probably be possible to use the variety of barley which is cultivated in those parts of the puna with the highest precipitation. There, it serves as a source of food for humans (grain) and animals (green fodder, straw). Care would have to be taken to make sure that uniform seed is used, since between 5 and 10 different varieties are cultivated on the Andean plateau.
Similar to Lolium, the barley could be raised in pots in uniform soil, and then exposed in the field for several weeks to a few months. A sufficient water supply for a period of time could be secured by placing the pots on top of storage containers filled with water into which wicks lead (Fig. 9). The accumulated contaminants are determined at the end of the growing season. Because of the unfavorable growth conditions, it would probably not be necessary to utilize several overlapping, staggered exposure periods. The potted plants would also have to be protected from grazing and nibbling livestock, which could be done either within the established long-term study plots (section 3.3) or inside of fields where crops are grown in any case, since the herdsmen keep their animals out of them. The disadvantage of this is that it can interfere with random or systematic assignment of measuring points over a study area. The potted plants should not, however, be placed up high on posts
as recommended for moss bags (section 3.1.1), since the microclimatic conditions there deviate too strongly from the natural situation close to the ground.
3.1.4 Contaminant enrichment in the topsoil
The vegetative cover of the Andean plateau is for the most part quite sparse (between 20 and 60%), as a result of which most of the emitted pollutants come into direct contact with the soil. Because of the extreme climatic conditions (in particular lack of water and warmth), most of the soils are poorly developed. Their humus content is low even in the uppermost few centimeters of soil, and rapidly approaches zero at greater depths. Here and there, however, soils with varying peat content have been able to develop on moist azonal sites (cf. section 3.2). The soils generally contain very small amounts of mineral nutrients. Depending on the degree of aridity or moistness of the climate, the soils have a tendency towards either superficial enrichment (due to rising vapor currents) or depletion (due to leaching) of readily soluble substances.
Since heavy metals form particularly stable bonds with organic substances with high cation exchange capacities, and to some extent also with mineral cation exchangers (clay fractions and iron compounds), it is also to be expected that the highest heavy metal concentrations will be found in the top few millimeters to centimeters of the soil. As a consequence of this, the uppermost soil layer could provide information on the spatial distribution of contaminants in the area affected by a source, similar to the way in which passive plant bioindicators work. The drawback is that it would be impossible to draw any conclusions on the period of time during which accumulation has taken place.
When selecting the comparable sampling sites, it is important that they fulfill the following criteria:
- level terrain (so that neither soil loss nor soil deposition need be expected)
- uniform vegetative cover in the surrounding area (no windward or leeward situation)
- as far away as possible from plants which could shield out contaminants (a distance equal to at least 3 times the height of the plants)
- certainty that the soil has not been ploughed or mixed by mechanical means over a long period of time; if possible, the length of this time should be known (large fossorial animals, e.g. burrowing mammals, arable plots fallowed).
3.1.5 Mapping of contamination zones by means of damaged lichen vegetation
In many densely populated areas in industrialized countries, mapping of lichen communities has been successfully applied for delimitation of zones with differing levels of contamination (Frankfurt, Saarbrukken, Stuttgart, Freiburg, the Ruhr, Netherlands, etc.). In general, SO2 emissions are regarded as having the greatest impact. Lichen maps would therefore be a useful aid for assessing the impact of this contaminant, which is exhausted into the environment by metallurgical operations along with the heavy metals.
Lichens could also be used to demonstrate the injurious effects of heavy metal and fluorine contamination. It should be taken into consideration, however, that no definitive conclusions on the type and amount of specific contaminants can be drawn from a mapping without having first performed precise tests, usually by means of comparative experiments, to determine the reactions of individual species (KERSHAW 1985). This statement holds all the more true in view of the fact that, in addition to the impact of individual substances, synergistic effects can also be expected, and have indeed already been demonstrated in a few cases. Thus, mapping of zones around a source that offer varyingly favorable living conditions for lichens can only yield a general picture of the gradation of contamination levels. This could be very useful, however, in connection with preliminary studies to gain a general orientation.
Many gaps still remain in our knowledge about the lichens of the Andean plateau. Fortunately, both in the Federal Republic of Germany and in other countries as well (United States, Great Britain) there are a number of expert lichenologists who could provide valuable assistance in identifying and classifying the lichens of the Andes. It is important for the field workers doing the actual collection to be able to distinguish among different species, however. In other words, a certain amount of basic knowledge is essential.
In order to minimize the influence of differing lichen substrates, mappings of the type mentioned above have typically been restricted to epiphytic lichens growing on tree trunks. The difficulties associated with mapping of epilithic lichens have been repeatedly discussed in the literature (FEIGE 1982; HOPP, KAPPEN 1981). Since trees are fairly rare on the Andean plateau, in many cases growing only because of supplementary irrigation or on fenced-in plots, the study of epiphytic lichens does not enter into consideration at all. Stones and rocks bearing lichens occur widely, however, and are certainly also suitable substrates, since they are usually composed of low-pH minerals, and the products formed by their weathering or decomposition would not offset the deleterious effect of SO2, F and heavy metals. For study purposes, however, lichens would only be comparable that grow on mineralogically similar rock substrates.
3.1.6 Animals as accumulative bioindicators (brief survey)
Animals are also suited for evaluating contamination levels over time. Although they are not restricted to a single place like plants are, the radius of activity of individual species can usually be quite well defined and delimited. By selecting suitable species, different classes of animals (herbivores, firstorder and higher-order predators) can be used to study the concentration of contaminants up through food chains. A number of different phenomena make interpretation of the results very difficult, however, such as elimination processes that vary from substance to substance and species to species, unknown diversity or selectivity of food, differences in developmental patterns, etc. (see ELLENBERG jun., this volume).
A relatively large number of studies has been carried out on accumulation of heavy metals in various classes of animals and animal organs in the vicinity of metallurgical plants (MUNSHOWER 1977; ROBERTS, JOHNSON 1978; UBA 1976, 1977, 1983). On the basis of these experiences and preliminary data which has been collected on the fauna of the central Bolivian plateau (HANAGARTH, FISEL 1983), the following classes of animals would appear to be suitable:
- earthworms
- ants
- predatory insects of the order Hymenoptera
- spiders
- mice and other small mammals
- birds
- range livestock: kidneys for Cd, bones for F, livers for many heavy metals.
3.1.7 Accompanying vegetation studies
In the area around the sampling sites, the vegetation should be precisely studied and described with the aid of phytosociological surveys, in order to identify plants which are sensitive to contaminants. Each vegetation survey should include an overall list of all occurring species, as well as the following data on each plant species:
- proportion of total phytomass
- degree of vitality (expressed in terms of a 5-point scale)
- quantity of flowers and/or fruits (expressed in terms of a 3-point scale)
- proportion of young seedlings and juvenile plants
- incidence of disease (e.g. rust in grasses)
- injurious symptoms (discoloration or desiccation of leaves, etc.).
Repeated occurrence of characteristic external signs of damage or reductions in the vitality of certain plant species should be closely observed. It is advisable to establish a herbarium for purposes of comparison.
If possible, local residents should be asked if they have observed the decline of any pasture plants or damage to crop plants. For this purpose, it may be necessary to obtain the services of an interpreter who is fluent in Spanish and Aymara or Quechua.
3.1.8 Accompanying soil studies
Enrichment of heavy metals in the soil, their assimilation by vegetation, and their transport into deeper soil horizons are influenced by the following soil attributes:
- organic matter content
- chemical properties of the organic matter (degradability, C/N ratio, exchange capacity)
- particle size distribution and composition (in particular the proportion and type of clay fractions)
- pH value
- concentrations of other cations (Na, K, Ca, Mg and other heavy metals)
- total and available phosphates
- concentration of oxides of Fe and Mn
- water content and its fluctuations through time
- maximum water capacity
- intensity of small soil fauna activity - intensity of microorganism activity.
Of the above-mentioned factors, the most important are pH value, the cation exchange capacity, the organic matter content, the concentrations of oxides of Fe and Mn present, and the availability of phosphates. These parameters should be measured at every sampling site, and not just on longterm study plots (section 3.3.6). It is possible to confine these measurements to the topsoil (0-5 cm) within the scope of a minimal program. In addition, however, at the very least the root zone should be studied. The presence of hardened or differently colored horizons can indicate layers of the soil profile in which pollutants have accumulated.
3.1.9 Accompanying climatic studies
All of the parameters dealt with above are dependent on general climatic and short term weather conditions. Because of this, at least in the vicinity of the source it is necessary to carry out climatic measurements so that the results of analysis can be interpreted in a more differentiated manner.
As a rule, large mining operations operate their own weather stations, since their production depends on a sufficient supply of water. Because of this, it will probably be possible to set up supplementary measuring facilities that could be supervised and regularly monitored there.
The weather stations should be equipped with protected recorders that continually register the following data:
- air temperature
- relative humidity
- precipitation
- wind direction
- wind velocity
- solar radiation (or at least the duration of sunlight)
- soil temperature (at depths of 0-2, 5 and 50 cm).
The best approach is to distribute stations throughout the area under study; these should continually measure precipitation and wind and record them in graphic form, so that local variations in precipitation events and wind intensities can be better evaluated. This is only feasible if it is possible to ensure regular checks and maintenance.
<section>3.2 Studies of the regional history of contamination by means of peat profiles</section>
In many of the areas which today are considered to contain ores of sufficient value to make extraction worthwhile, mining operations go back as far as prehistoric or colonial times. Over the course of the centuries, the preferred minerals, the volumes extracted, and the processing methods have continuously changed and evolved. These have in turn influenced the pollutants released into the environment and the patterns of their impact on the ecology of surrounding areas. It is often impossible to distinguish between the effects of pollutants which are being currently discharged and the impact of contaminants which accumulated long ago. It is therefore important to be familiar with the historical background of pollution in each individual case. On the Andean plateau, analysis of peat profiles would probably be a promising means of doing so.
Throughout the Andean plateau - with the exception of the subarid to arid areas in the southwest - in the Andean to sub-Andean zones so-called "hard-cushion bogs" have formed, under some of which there are peat strata up to several meters thick. The species composition of peat-forming plant communities are not uniform. They depend on precipitation and evapotranspiration conditions, on temperatures, and on the composition and flow rates of spring waters (GUTTE 1980; RUTHSATZ 1977). In contrast to the bogs and moors of temperate climates, no mosses are involved in peat formation in the hardcushion bogs, but instead exclusively sedges, members of the Compositae and Plantaginaceae and other plant families. As a consequence, the peat generally contains a high proportion of large plant remains which do not readily decompose.
In recent years, such peat deposits of the Andean plateau have been investigated both in Argentina (MARKGRAF 1983, 1984) and in Bolivia (GRAF 1979, 1981) using pollen analysis methods. The age of the various peat strata has also been determined using carbon- 14 dating. The data which these studies have yielded on the climatic and vegetational history of the Andean plateau are to a certain extent inconsistent, but nevertheless permit a relative temporal correlation of the peat strata. Studies of the heavy metal concentrations in such hardcushion bogs should always be accompanied and corroborated by pollen analysis of the corresponding peat horizons.
Not all heavy metals are immobile enough in bogs and fens to be used as indicators of the contamination processes which were going on at the time the peat was being formed. The most suitable metal has been shown to be lead, and to a lesser extent also copper. In an acidic milieu, zinc is leached out in a downward direction, and it can also be extracted by plants as a micronutrient from deeper soil levels and thus accumulate in the growing plant cover (LIVETT et al. 1979). It would have to be studied whether these processes also apply to the hard-cushion bogs of the semiarid to subhumid Andean plateau.
There is little reason to expect mobilization of heavy metals by particularly low pH values, since the Andean hard-cushion bogs rarely have pHs of less than 5. Nevertheless, most of these hard-cushion bogs dry out superficially during the dry season. The more arid the climate is, the more intensive is the upward movement of water during these months. In extreme cases, a salt crust can form on the surface. Such bogs would probably not be suited for studies of the kind required. Fortunately, wherever such salinization phenomena regularly occur this can be readily detected from the floristic composition of the living bog vegetation.
When investigating these historical processes, the following aspects should be given consideration:
- A comparison should be made between presumably unpolluted and polluted bogs.
- Profiles should be selected for test purposes that are no longer directly exposed to flowing spring water, which can be subject to significant seasonal variations.
- Parallel analyses of heavy metal and pollen contents should be carried out in the same peat strata.
- Those physical parameters of the peat should be measured which can affect the mobility of the heavy metals: pH value, cation exchange capacity, the concentrations of other cations and oxides of Fe and/or Mn, and water-level variations in the peat profile.
- The present bog vegetation should be studied to determine the concentrations of heavy metals it contains, separately for each species and plant organ (leaves, shoots, fruits, rhizomes).
It appears difficult to assess the extent to which the structure of the peat has been influenced by the wild (vicuna) and domesticated (Hama, alpaca) members of the camel family that live in the Andes; their preferred grazing grounds are the bog areas. The habit which these animals have of leaving their feces at common defecation sites may have led to changes in the spatial distribution of heavy metals derived from atmospheric contamination.
<section>3.3 Studies of the long-term effect of contamination on the agriculturally utilized ecosystems of the Andean plateau</section>
3.3.1 Determination of plant biomass and primary production in natural pastures
3.3.2 Determination of contaminant concentrations in major groups of plants
3.3.3 Determination of the biomass and activity of soil microorganisms which play a major role in breakdown and decomposition of organic matter and mineralization of plant nutrients
3.3.4 Determination of contaminant concentrations in the soil
3.3.5 Studies of general soil properties (cf. section 3.1.8)
3.3.6 Weather documentation during the study period and evaluation of whether the meteorological data collected are representative for the study area
In addition to the short-term deleterious effects of contaminants on flora and fauna, the long-term effects of chronic pollution are also significant. One of the reasons behind the gradual decline of agricultural productivity on much of the Andean plateau is soil erosion provoked by overutilization (in particular overgrazing) (ELLENBERG 1979); locally, this decline is likely also being aggravated by contaminants discharged into the environment by mines and metallurgical operations. This is important, since the affected land represents the primary source of livelihood of the population of the Altiplano.
Due to their generally low nutrient contents and, at least in the moister areas of the Andean plateau, predominant acidity, the soils there are readily affected by contaminants, and therefore highest priority must be attached to ascertaining the damage which this is causing to ecosystems.
During the last several years, much discussion has focused internationally on approaches for studying the environmental effects of contaminants, and especially those of heavy metals (ELLENBERG et al. 1983; HUGHES, LEPP, PHILIPS 1980; MARTIN, COUGHTREY 1981; SHEEHAN et al. 1984). To be sure, ecosystem studies such as those which have been carried out within the scope of International Biological Programme (IBP) and MAB projects are only possible with enormous investments in terms of time and labor. But the Institute of Ecology in La Paz, at which Bolivian and German scientists are cooperating, has carried out investigations on the Andean plateau which can serve as a model of how it is possible, with limited means, to obtain useful information on the functioning of grazed and agriculturally utilized ecosystems (HANAGARTH, FISEL 1983). Similar investigations with long-term study plots could also shed light on the environmental impact of contaminants from mining and metallurgical
operations. The ecosystem parameters chosen for study should fulfill the following criteria (ELLENBERG et al. 1983):
- They should play a major role in the ecosystem concerned.
- They should exhibit an adequate degree of constancy or follow a repeating annual pattern.
- They should react sensitively to the contaminant concentrations which can be realistically expected.
- They must be simple to measure and document with a sufficient degree of accuracy.
Nothing is yet known about the tolerance to contaminants of the flora and fauna of the Andean plateau and the ecosystems characterized by them. Because of this, all investigations must be conducted on the basis of prior comparisons between unpolluted areas or areas that can be expected to have low contamination levels on the one hand, and more strongly polluted biotopes on the other. To this end, a number of parameters must be monitored over long periods on agriculturally utilized and nonutilized experimental plots. The most important parameters deserving of consideration are:
- plant biomass and primary production
- contaminant levels in those groups of plants which play an important role in the ecosystem and account for most of its primary production
- biomass and population densities of fauna which play a major role in the disintegration and decomposition of living and dead organic matter
- contaminant levels in animal populations that play a major role in the typical food chains of the Andean plateau
- activity of soil microorganisms
- contaminant levels in the soil profile
- general soil attributes which have an important bearing on plant nutrition and metabolization and/or distribution of contaminants
- weather conditions over the course of the year.
When selecting and establishing the long term study plots, the following site types should be included:
- for purposes of comparison, plots that can be assumed to have no, low, moderate and high contamination in the vicinity of a pollutant source
- study plots on flatland sites with an accessible water table (the vegetation of which is heavily grazed, especially during the dry season)
- study plots on sites with a very deep groundwater horizon and natural pastures typical of the region (usually dominated by low shrubs or bunch grasses)
- study plots on currently farmed and fallow cropland.
The long-term study plots should be sections (0.5 to 2 ha in size) of more extensive areas that have more or less uniform attributes throughout. Supplementary subplots (new ones each year) can also be fenced in and included in the study. At each site, one larger plot should be permanently fenced in so that the secondary plant succession which develops after grazing has ceased can be monitored. The studies discussed in greater detail below should be carried out at greater intervals, e.g. every 2 to 4 years, including on these "succession plots". Over the course of time, this should yield data that will illuminate the influence of grazing, the vegetation and the pollution situation on the Andean plateau. The gradual changes in the plant cover could be charted by means of detailed annual phytosociological surveys.
3.3.1 Determination of plant biomass and primary production in natural pastures
The net primary production of the affected ecosystems is the starting point for diverse food chains. It can serve as an indicator of the extent of nutrient recycling and recharging. That portion of the biomass of the Andean plateau pasture ecosystems which survives the dry season is not great, and essentially comprises the following categories:
- evergreen and deciduous low shrubs (10100 cm)
- shoot and leaf bases of perennial grasses and herbaceous plants
- rhizomes and roots of all perennial plants.
During the dry season, when there is a general shortage of forage, the grazing livestock is forced to depend exclusively on this remaining phytomass for its nourishment, and the animals then also eat plants and plant parts which they avoid during the rainy season. Especially the woody plants are affected by this; in other words, parts of their shoots are also able to pass on contaminants to domestic animals. The amount of intact plant biomass at any given time is largely dependent on the intensity of grazing, and as a rule is significantly smaller than that which the sites are potentially able to sustain. It is nevertheless important for identifying the annual production rate.
When choosing the collection method for determination of biomass and net primary production, the usual rhythms of utilization of the vegetation by the local population and livestock should serve as a model. Biomass and production can only be determined on plots which livestock is prevented from entering. Of course, this is also likely to gradually change the contamination situation, since the plant cover becomes increasingly dense once browsing by livestock has been eliminated. To compensate for this, new subplots must be fenced in each year.
In order to obtain an initial rough picture of production conditions in the pasturelands of the Andean plateau, it is sufficient to determine aerial biomass and net primary production. The second step is to estimate the subterranean production of those plant species which are most important in terms of volume; this is done on sample plots. In semiarid areas, the shoot/root ratio is usually clearly
shifted in the direction of increased root biomass. The roots and rhizomes, in addition to uptake of nutrients and water, also play a major role as storage organs.
3.3.2 Determination of contaminant concentrations in major groups of plants
In order to reconstruct the ways in which contaminants are accumulated and transported or passed on in the ecosystems, their concentrations in the various ecosystem compartments must be measured. The choice of which compartments to study should be governed by the following criteria:
- the primary distribution pathway (air, precipitation, floodwater, etc.) and the points within the ecosystem which are first affected (leaves, topsoil, groundwater, etc.)
- biological metabolization of the contaminant and its transport and spread by chemical and/or physical processes
- the principal food chains in the ecosystem - the ways in which the ecosystem is utilized by human beings
- weather-related ways in which transport, spread, distribution, reactions and metabolization of contaminants change over the course of the year.
It is important to know the contaminant concentrations in individual plants and/or plant parts so that the physical, chemical and biological processes which the pollutants are subjected to in the affected ecosystem can be derived (ROBERTS, JOHNSON 1978; VETTER et al. 1974). The soil also plays a major role in this context.
For orientation purposes, initially the contaminant concentrations in the following compartments should be determined:
- leaves and/or shoot apices of dominant plant species:
- Summergreen deciduous woody plants, perennial and annual herbaceous plants in the middle (January/February) and at the end (April/May) of the growing season.
- evergreen woody plants and facultatively evergreen herbaceous plants in the middle and at the end of the growing season, as well as at the end (September/October) of the dry season
- roots and rhizomes of dominant plant species:
In the middle and at the end of the growing season, as well as at the end of the dry sea son (a standard root diameter must be established for the samples).
- Fruits and seeds of dominant plant species which play an important role in the food chains:
in each case at the times when they would presumably be eaten by animals
- branches and twigs of the dominant shrubs:
in the middle and at the end of the growing season, as well as at the end of the dry season (the sampling sites and diameter and age of the samples must be standardized)
- plant liner:
at the beginning and at the end of the dry season, provided that sufficient representative material is available for sampling.
3.3.3 Determination of the biomass and activity of soil microorganisms which play a major role in breakdown and decomposition of organic matter and mineralization of plant nutrients
In the long term, the production of an ecosystem is determined principally by the rate at which dead organic material is mineralized and recycled, its nutrients being made available to the plants again. A number of animals, bacteria and fungi play a major part in this process. The corresponding recycling rates and the seasonal variations to which they are subject must be studied on-site. The data thus obtained are the best reflection of the dynamic processes taking place in the ecosystem. These fluctuate widely from year to year, since they are influenced by weather conditions. It is therefore essential for comparisons between polluted and unpolluted ecosystems to be performed on study plots that can be expected to have the same weather patterns, i.e. that are located close together. In practice, it may be difficult to fulfill this prerequisite.
With the aid of standardized laboratory studies, the conditions observed in the field can be compared with the potential performance - under optimum or typical conditions - of the various classes of organisms. This approach does not permit realistic simulation of actual weather-related variations in open country, however.
Since each of these approaches has its merits and drawbacks, tried-and-proven methods of both should initially be applied to test the usefulness of the data they yield. The aspects which can be studied for this purpose include the nutrient mineralization processes themselves (i.e. production of NO3-N and NH4-N), the activity of the involved enzymes (urease, phosphatase, etc.), the rates of decomposition of artificially introduced organic substances (e.g. cellulose), and the respiratory activity associated with these processes (CO2 production). The following investigations enter into consideration:
A. In the field:
- nitrogen mineralization over the course of the year
- soil respiration over the course of the year
- cellulose decomposition during the growing season.
B. Laboratory incubation experiments under optimized conditions (usually 20 - 25 ºC, 60% soil water capacity):
- nitrogen mineralization
- soil respiration
- enzyme activity: urease, catalase, dehydrogenase, phosphatase, etc.
- decomposition of cellulose.
Relevant methods are described in the following publications: BECK 1986; GERLACH 1973; ISERMAYER 1952; RUNGE 1970; SALM 1983B; STEUBING, KUNZE 1980.
3.3.4 Determination of contaminant concentrations in the soil
In polluted areas, contaminants reach the soil either directly or indirectly by way of the plant cover and the litter formed by castoff plant parts; they tend to accumulate primarily in the humic topsoil. Depending on their chemical properties and the attributes of the plant roots, from there they can be reabsorbed by the plants and transported into their shoots. Soil fauna and microorganisms are also exposed to them to a greater or lesser extent. The soil usually has a very large storage capacity for contaminants of low solubility, thus entrapping them for long periods of time in the topsoil with its intense biological activity.
In spite of the fact that many of these substances remain relatively inaccessible and not readily available for assimilation and metabolization by living organisms, it is nonetheless of vital importance to know about this reservoir. Grazing animals ingest the contaminants not only indirectly from the forage plants which they feed on, but also directly as a consequence of their consuming large quantities of soil along with the fodder (THORNTON, ABRAHAMS 1983). The latter pathway of contaminant transport is likely to play an especially great role during the dry season. Suitable study approaches have already been discussed above in section 3.1.4.
3.3.5 Studies of general soil properties (cf. section 3.1.8)
The production of the plant cover, as well as accumulation and availability of contaminants in the soil, are dependent on a large number of physical and chemical soil properties. These must be thoroughly studied on every sample plot used, to permit meaningful interpretation of the data from sample plots with different pollution levels which has been obtained using the methods described in sections 3.3.1 through 3.3.6.
As an absolute minimum, the following parameters of the soil horizon corresponding to the root zone should be determined (MOORE, CHAPMAN 1986; SCHEFFER, SCHACHTSCHABEL 1976; SCHLICHTING, BLUME 1966):
- pH value
- proportion of organic matter - C/N ratio
- ration exchange capacity and base saturation of the fine soil
- plant-available nutrients: P, K, Ca, Mg - total nutrients: P, N
- concentrations of oxides of Fe and Mn - water storage capacity
- particle size distribution, at the very least determination of the clay fraction
- concentration of salts: e.g. NaCl, CaSO[4].
If possible, some of those soil properties which vary according to the amount of water present in the soil should be studied at the beginning and in the middle of the rainy season, as well as at the end of the dry season. This would make it much easier to assess the range of annual variations.
3.3.6 Weather documentation during the study period and evaluation of whether the meteorological data collected are representative for the study area
In semiarid areas, plant production is crucially influenced by the weather over the course of the growing season. Besides the amount and distribution of precipitation, temperature patterns are also highly significant on the Andean plateau. For assessment of the environmental impact of different contaminants, data on wind directions and intensities are also required. Since the weather can vary considerably from year to year, as a rule a single test series will be insufficient to provide reliable information on the mean climatic conditions prevailing in a study region. Data from test series lasting just a few years can only be correctly evaluated by comparison with long-term measurement data recorded by nearby weather stations.
The following aspects are absolutely essential for inclusion in test programs and accompanying climatic studies:
- monitoring of atmospheric temperature and relative humidity throughout the year 2 m above the ground and at ground level (using a thermo-hygrograph in a protected test station)
- monitoring of precipitation over the course of the year, using standardized recording equipment
- monitoring over the course of the year of soil temperatures at the ground surface and in the root zone with the aid of electronic equipment which permits continuous measurement and recording of data.
If possible, it would also be useful to monitor the following parameters over the course of the year:
- air temperature and relative humidity at the height of the plant cover
- wind velocity and direction at the top height of the plant cover (relevant for determination of pollution levels)
- solar radiation at the height of the plant cover
- the ozone burden of the ambient air at the height of the plant cover
- soil moisture in the root zone of the plant cover.
All of the meteorological measuring equipment should be installed in such a way that the collected data can be unambiguously correlated with the various long-term study plots.
<section>3.4 Time frame of study programs</section>
After selecting one single important or several typical pollutant sources, the first step must be to establish the concentrations of the various contaminants present in the environment. A complete annual cycle is necessary in order to select appropriate objects, sampling dates and analytical methods, which are then tested during the following 2 to 3 years in the entire study area.
In the second, or at the latest in the third, year the sites for establishment of the longterm observation plots should be selected. The sites must fulfill the following criteria:
- They must be representative of the affected natural habitat and current utilization of
- They must be representative of certain pollution situations.
- They must be accessible at all times of the year.
- Each one should be located close to a village community prepared to cooperate in the investigation.
The amount of time which will be required to initiate and develop the required contacts should not be underestimated. A time frame of at least 4 to 6, preferably 8 to 10 years, should be planned for the observations and measurements on the long-term observation plots.
<section>3.5 Required scientific and technical infrastructure in the field and in the country where studies are being performed</section>
In order for studies of the type described here to be considered a genuine success, they must lead to action on the part of local authorities, institutions and decision-making bodies. It is therefore absolutely essential to carry out all planning and implementation of measures jointly with state universities, research institutions and/or other organizations, as well as with the affected industries and landowners. If good relations with these parties are established and maintained, it will be possible to utilize the facilities of all of the participating institutions. At the very least, the following prerequisites must be fulfilled:
- use of a cross-country vehicle capable of hauling large amounts of materials and/or equipment
- permanent accommodations in the field or a nearby settlement (with electricity, water, refrigerator, work tables, drying oven, etc.)
- collaboration of an institution which has a well-equipped laboratory for studies of soil chemistry and plant ecology, and trained staff (for performing large series of routine studies)
- use of an atomic absorption spectrometer (AAS) for determination of trace element concentrations.
<section>4. Summary</section>
The aim of the present study is to point out the possibilities and limitations of the use of biological indicators - for the most part plants - for environmental monitoring in connection with mining and metallurgical operations on the central Andean plateau (Southern Peru - Bolivia- Northern Argentina).
First, the role played by mining and metallurgical operations in the social and economic structure of the study area is explained. The population of the Andean plateau lives primarily from agricultural practices of the subsistence type. A loss of value in the soil (cropland and pastureland) and water, the major production factors, cannot, as a rule, be offset by cost-intensive maintenance and fertilization measures. Mining and processing of ores cannot be dispensed with by the countries involved, since they represent a means for improving the income base of the highlands population and are also a source of much-needed foreign exchange. On the other hand, mines and metallurgical operations are known sources of pollution, particularly of heavy metals, gaseous (SO2, HF) pollutants and other toxic substances (e.g. arsenic). The ways in which these contaminants are transported through the air and via aquatic systems are discussed, as well as their possible environmental impact as
a result of accumulation and concentration in food chains, thus reducing the productivity of agriculturally utilized areas; these aspects are examined within the context of the central Andean plateau and illustrated by information supplied by members of the affected population.
As far as is known to the authors, no data is presently available from studies of the amount and composition of contaminant mixtures discharged by mining and metallurgical operations in the Andes. Neither does any information exist on the distribution of these contaminants and their impact on flora, fauna, and human health. In view of the situation, a number of general guidelines and principles for determining the environmental impact of pollution are discussed prior to presenting a concrete test program. Gaps in our knowledge about the specific situation as regards the transport and environmental impact of pollutants and possibilities for use of biological monitoring in the Andean highlands are pointed out and discussed.
On the basis of several vegetation studies carried out in the Andean highlands of Bolivia and Argentina and the large body of information which has been published on the use of biological indicators for assessment of the environmental impact of pollutants, the authors have elaborated a study program. This program is presented here.
It is recommended that researchers proceed according to the following steps:
1. selection of representative polluted areas;
2. determination of spatial pollution gradients for the contaminants under study by mapping the contaminant concentrations of highly pollutant-resistant plant species and the topsoil;
3. study of the vegetation along pollution gradients to assess the degree of damage to or complete absence of contaminant-sensitive plants (higher plants and lichens);
4. determination of contaminant concentrations in pasture and crop plants, these being the primary producers in food chains that, directly or indirectly, provide nourishment for human beings;
5. determination of heavy-metal concentrations in the peat strata of "hard-cushion bogs" to obtain information on the historical development of contamination in polluted areas;
6. establishment and monitoring of longterm observation plots with varying pollution intensities with respect to long-term damage to pasture ecosystems by heavy-metal contamination. The main focus here is on primary plant production and investigation of the decomposition and mineralization processes which organic substances undergo in the soil, and of the involved organisms. Animals are not considered here. Nevertheless it is necessary to investigate the impacts of heavy metals on food chains, at least via grazing animals to humans.
It would appear to be necessary, useful and feasible to carry out biological monitoring programs to investigate the environmental contamination caused by the mining industry in the Andean highlands. Nonetheless, because of the lack of relevant information on this part of the world, it is recommended that a preliminary study first be carried out in a selected sample area before planning more comprehensive projects.
It is absolutely necessary to cooperate with public research institutions, mining companies and the affected landowners. Only in this way can it be ensured that the scientific data and results yielded by such studies will culminate in concrete action being taken to control contaminant discharge and protect the affected population.
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<section>Bioindicators and biomonitors in aquatic ecosystems with special attention to potential applications in developing countries</section>
by Rainer Bretthauer
Dedicated to
H.-J. Elster
in honor of his 80th birthday
<section>0. Abstract</section>
In this article, biological water evaluation techniques are discussed in the light of their development and their current practical applications, illustrated by examples. A distinction is made between use of bioindicators, i. e. water quality evaluation with the saprobic classification system, and methods that make use of biomonitors or monitor species, i. e. species that assimilate and accumulate contaminants. The question as to the transferability of the methods used widely in Europe and North America to developing countries is examined and in general positively assessed.
<section>1. The context</section>
As the population of the world grows, human beings are placing ever-increasing demands on their environment. This also applies to the earth's bodies of water: oceans, seas, lakes, rivers. Water is not just used for drinking. In the "developed" countries enormous environmental problems have already been caused by contamination of bodies of water with excrete and substances used in agriculture (such as mineral fertilizers and pesticides), as well by the adverse effects of industrial activities, namely chemical pollutants such as heavy metals and organic compounds, and thermal pollution caused by the discharge of heated cooling water. Under the climatic and other conditions of the subtropics and tropics, increasing industrialization and population growth are leading to particularly serious problems of this kind, although they are often not recognized as such for lack of appropriate investigational means. The situation is further aggravated by the fact that numerous industrial
production facilities are being shifted, for cost-related reasons, from the "developed countries" to parts of the world in which wages are lower and less stringent environmental legislation exists. Moreover, many of these countries do not have sufficient financial resources for implementation of measures to combat water pollution.
71% of the earth's surface is covered by water, but fresh water- vital for human beings, animals and plants - accounts for only 0.6% of the planet's total water volume. The industrialized nations of Central Europe are situated in a climatically favorable zone, as a result of which they generally have a generous supply of water at their disposal. They also possess the technological know-how and economic resources required to supply drier areas with water from regions that enjoy a surplus. By contrast, many of the developing countries are located in parts of the world with low precipitation levels and/or long dry seasons, where water is inherently a scarce commodity. Rivers or lakes that carry water all the year round are thus rare in these countries. And "rivers and lakes that carry low water volumes", especially if subject to seasonal variations, "are characterized by a greater susceptibility to pollution" (1).
Both fresh and salt water also form the habitats for innumerable organisms that play a role in human nutrition, such as seaweed, shellfish, crabs and fish, just to name a few. In Europe and North America, years ago impaired health and reproductive disorders were observed in aquatic animals and animal species that derive their sustenance from the water (2). The causes were discovered to be contaminants in the water, such as organochlorines, e.g. DDT and other insecticides, and organic heavy metal compounds, e.g. methyl mercury, which had been assimilated by the animals via their skin and respiratory systems or through food chains with associated concentration (biomagnification). In Japan heavy metal accumulation in marine animals has caused health problems in human beings who have eaten them, in some cases quite severe, and even led to fatalities (as in the so-called Minamata and Itai-ltai diseases) (3). Nonetheless, these discoveries represented only the beginning: a large
number of other contaminants were subsequently diagnosed and their dispersal paths identified.
In addition to restrictions in the utilization of water bodies as sources of drinking water or otherwise, contamination of fresh water and marine water can also have a multitude of indirect deleterious effects on human beings. It is therefore of overriding importance to find and improve means of monitoring the quality of water and bodies of water as well as, if called for, changes in their pollution levels and of evaluating these factors, possibly combined with predictions for the future, in order to remedy and/or prevent harm to human beings and their environment.
<section>2. Means of detecting water pollution</section>
Even theoretically it would be impossible to keep all contaminants out of all water everywhere; even without human influences contamination of bodies of water has always occurred and will continue to occur. To take an example, we need only think of the compounds which can be formed in lakes under certain conditions, such as hydrogen sulfide (H2S), which causes most of the organisms within the affected zone to die off, or at the very least causing oxidophilic organisms to avoid such polluted aquatic environments. If there is excessive introduction of allochthonous organic matter and/or in-situ production of organic substances, hydrogen sulfide is formed, for instance on the bottom of lakes, when the oxygen content is no longer sufficient for mineralization of organic materials by aerobic processes. Studies of the earth's history have revealed that water pollution of this kind has often happened even without human beings playing a role. The question here is, what possibilities
are available for detecting temporary and longerlasting positive and negative changes in water bodies? What possibilities exist for identifying and, if possible, predicting latent and acute threats caused by water pollution and thus of offering means of dealing with or warding off these threats? Science is only capable of providing the know-how and tools. Conflicts of interests often lead to these warnings and indications being ignored, as is shown by the example of the salinization of the Nile delta and the resulting drastic decline in Egyptian marine fishery yields caused by the construction of the Aswan Dam. These repercussions were predicted by scientists of repute, but were ignored by the decision makers. The rerouting of the Nile in Sudan and the laying dry of the Sudd (the "Jongley Canal" project) would have had catastrophic effects for the population living there if they had not succeeded in preventing this measure at the last moment. That the industrialized nations
are also still burdened by problems of this sort is illustrated by the example of the Rhine. The quality of the water flowing in the Rhine has improved since the report of the Council of Experts for Environmental Issues (Rat von Sachverstandigen fur Umweltfragen) (4) in the Federal Republic of Germany, but it is still far from satisfactory. Heavy metal contamination of the river even seems to be increasing again. However, this fact does not relieve us of our responsibility to warn the developing countries of the dangers of water pollution and to call attention to means of detecting and avoiding such pollution. This of course also includes the provision of training and technological know-how.
<section>2.1 General review of assessment procedures and definitions</section>
2.1.1 Physical and chemical water analysis
2.1.2 Biological evaluation of water pollution
2.1.2.1 Evaluation of water pollution with the aid of bioindicators
2.1.2.2 Evaluation of water pollution with the aid of biomonitors
2.1.3 Remote sensing
It would go beyond the scope of this paper to present here an exhaustive discussion of all possibilities which are available for the use of bioindicators and biomonitors in aquatic ecosystems. Instead, in the following I will attempt to provide a number of positive and negative examples in order to call attention to methods which are used in the Federal Republic of Germany. I will therefore devote a considerable amount of space to the so-called "saprobity system" for classification of water pollution. To begin with, however, a brief review of the different types of evaluative procedures is in order. These are:
1. Physical and chemical water analysis
2. Biological procedures based on the use of
a) Bioindicators
b) Biomonitors
3. Remote sensing
2.1.1 Physical and chemical water analysis
With the aid of physical and chemical analysis techniques, it is possible to obtain information on the condition of water at the place and time that samples are taken. Depending on the quality of the investigatory methods used and the number of parameters studied, more or less useful data are yielded on the quality of the water at that point in time. How accurate and detailed the results must be naturally depends on the purposes for which analyses are performed (see also Chapter 3). In order to obtain more precise data, repeated analyses are necessary; these can even be aimed at identifying changes during the course of a single day.
A program conducted by the state of Baden Wuerttemberg is a good example: along certain flowing waters, above all in the navigable portion of the Neckar River, measurement stations were installed with devices for continuous collection of water samples and regular monitoring of their chemical composition (Figure 1) (5). A number of parameters are measured, including the amounts present of organic carbon, ammonium, nitrite, nitrate, orthophosphate and oxygen, as well as the biochemical oxygen demand (BOD). By means of additional tests, it is of course also possible to obtain additional information, for example on the concentrations of toxic substances. As is to be expected, continuous taking of samples and performance of analyses are associated with high technical, financial and labor inputs. The costs incurred grow with the number of samples taken and the range of substances, which are tested for. Even the industrialized countries can only afford to do this within certain
limits, as can be seen in Figure 1. Nevertheless, within the scope of major technical projects in developing countries it could be useful to carry out similar sample-taking and analysis programs here and there for monitoring purposes. This would have to be decided upon in each individual case.
For physical and chemical water analysis, the methods described in the following sections can be used. They are based on many years of experience, have been modified in accordance with the most recent scientific insights and discoveries, and continue to be developed further on an ongoing basis (713).
2.1.2 Biological evaluation of water pollution
Living organisms make certain demands on their environment, i.e. they are dependent on certain factors or groups of factors and their qualitative and quantitative configurations. Based on this observation, in Central Europe it is possible, for example, to classify the different regions of flowing waters (streams and rivers) on the basis of their dominant fish species; here, the primary factors of relevance are temperature, oxygen content, and flow. The uppermost region, for example, is characterized by cold, oxygenrich water populated by trout (Salmo trutta); this is referred to as the trout zone. At the opposite end of the spectrum is the bream zone in the lower courses of major rivers where the current velocity is greatly reduced, the water temperature is high in the summer, and the oxygen content is low. This zone is characterized by bream (Ahramis brama).
Over 140 years ago the first observations were published according to which domestic sewage is capable of changing the natural population patterns of flowing waters. The mechanisms of this change were not immediately understood, however. The important thing is that even then, as today, the ability of living organisms to react positively or negatively to changes in their environment was observed and made use of. Today the fact is also taken advantage of that many organisms are able to assimilate and sometimes accumulate substances present in the water.
2.1.2.1 Evaluation of water pollution with the aid of bioindicators
A short, precise and comprehensive definition of the concept of "bioindicators" is given by ELLENBERG, sent (14) with which I fully agree: "A bioindicator is a related group or community of organisms whose occurrence or an easily observed behavioral trait can be so closely correlated with certain environmental conditions that it can be utilized as a pointer or quantitative test." (see 15)
In other words, when evaluating water pollution with the aid of bioindicators the circumstance is taken advantage of that organisms react to changes in their environment; these reactions can take the form of growth and/or increased population density, modified activity, reduced growth, a decline in population. or even death. Depending on their degree of complexity, size, generation time and other factors, organisms or different species react faster or slower. Most bacteria adapt very quickly to environmental changes. Protozoa and algae take longer, and insects - many of which live for a year or longer as larvae in the same aquatic environment - require correspondingly longer to react to positive changes in their surroundings. As a rule, organisms with longer generation times respond also more quickly to negative changes - if they exceed the limits of what is tolerable - for instance by migrating to zones with satisfactory living conditions or by dying. Depending on the time
which bioindicators or indicator organisms spend in a body of water, they are subjected to the prevailing environmental conditions and any changes in them. That means that, as members of a related group of organisms or biological community, in contrast to physical or chemical analysis they integrate and reflect environmental conditions (and possible changes) over an extended period of time. Consequently, critical evaluation of the species compositions of a biocoenosis can yield sufficient data on the situation of a body of water and the range of fluctuations which the environmental conditions experience over a lengthy period of time. It is upon this recognition that the systems are based which are used in Germany for evaluation of aquatic ecosystems with the aid of bioindicators, foremost among them the saprobity system.
2.1.2.2 Evaluation of water pollution with the aid of biomonitors
As will be discussed in greater depth below (Chapter 3), relatively few organisms occur in aquatic habitats that are capable of indicating specific substances contained in the water. Because of this, in recent years more extensive use has been made of the ability of organisms to assimilate certain contaminants, such as heavy metals or pesticides, etc., through their gills or skin or in the food they eat and to accumulate it in their bodies. It has been possible to identify the above mentioned substances in such organisms just like in terrestrial organisms (cf. 2, 16). Such species are generally referred to as cumulative indicators (17), but will be called biomonitors or monitor organisms here. Biomonitors are also used for assessing brackish and marine water, in other words for waters for which it has not yet been possible to develop a "saprobity system". In addition, there are other organisms that can provide information on the kind and/or concentration of contaminants;
these are the so-called reactive indicators, in this paper referred to as bioindicators. To name a few examples: Metopus es, a ciliate, is a useful indicator species for hydrogen sulfide. Gnathonemus petersi, a fish belonging to the family of the Mormyridae, can be utilized for indication of certain toxic substances; in their presence it changes the electric discharges it emits (18). Such organisms can also be used for evaluation of drinking water ( 19).
2.1.3 Remote sensing
Aerial photography can yield qualitative and quantitative information on changes in environmental conditions. The studies of this type which have been performed on the expansion of dry regions (examples: Sahara, Sahel) are well-known. Changes in the condition of large bodies of water can be detected in the same way.
<section>3. Biological assessment</section>
"Biological water analysis can always be applied, regardless of whether the harmful wastewater is still present at the moment or not. The analyzed community of plants and animals provides an average value for the composition of the water which has flowed over them during a lengthy period of time. The chemist, by contrast, is obliged to directly obtain samples of the wastewater causing the contamination. In most cases, the biologist can obtain an average value with only one single study, while the chemist must repeatedly take samples. For this reason, biological evaluation of a body of water can usually be done much quicker than chemical analysis; and biological analysis is thus always much cheaper than chemical analysis." (20)
If it is wished to study the impact of contaminants on biological conditions in the water, in other words in connection with all questions related to fisheries and water hygiene, then biological water analysis is definitely to be preferred. (21 )
Nonetheless, biological water analysis is suitable for determining whether a given wastewater source contains substances which are harmful to organisms, but is incapable of identifying these substances. In general, only chemical analysis can reveal the nature of the contaminants; bioindicators are known for only a small number of substances, including hydrogen sulfide, iron and sodium chloride. (21 )
Decayable plant and animal substances, and others as well, have been accumulating on the earth's surface and in its waters for millions of years. Over the course of time, living organisms have adjusted and adapted to these. As a result, so-called indicator species exist for hydrogen sulfide, iron, manganese, sodium chloride and others. The - geologically speaking - relatively short period of time during which "artificial" water contamination has occurred, namely ranging from decades to a few centuries, has been insufficient to give rise to such adaptations. "In other words, while 'natural' types of contaminations are positively characterized by the occurrence of certain 'indicators' or by enhanced growth of certain water organisms at the cost of others, these 'strictly cultural' pollutants are negatively characterized by more or less complete obliteration of the community of organisms that inhabit clean water". (21)
Consequently, no "indicators" exist for sulfite cellulose, phenols, organochlorines, and the like. When anorganic pollutants, such as heavy metals, or nondecayable organic wastes (see above) are introduced into a body of water, their impact can usually only be measured in terms of their ability to destroy the living organisms present.
<section>3.1 Saprobic systems: evaluative techniques involving indicator organisms and related methods</section>
3.1.1 Historical background
3.1.2 Criticisms and counterarguments
3.1.3 Water quality evaluation using LAWA criteria
3.1.4 Indicators of the salinity of inland waters
3.1.5 Macrophytes as indicators of the ecochemical composition of fresh waters
3.1.6 "Coupling analysis"
3.1.7 The"species deficit" method
3.1.8 Biological-ecological water analysis (of flowing waters) using the DEV method (87)
3.1.9 Depiction of results
3.1.10 Special applications of biological water analysis for surveys of water pollution in the Federal Republic of Germany
3.1.11 The R-P-C system and BIP
3.1.12 Evaluation of standing waters
3.1.13 Drinking water
3.1.14 Application of biological water evaluation methods in developing countries (questions, problems, possibilities)
Biological water analysis methods are primarily based on changes in biocoenoses caused by contamination with decayable organic matter. After organic substances are introduced into a body of water, they are attacked by organisms and integrated into the ecosystem's chemical metabolism. Decomposers (e.g. bacteria and fungi) break down the organic matter into anorganic compounds which can be used in turn by producers (e.g. algae, etc.). Consumers utilize decomposers and flora as food. As originally stressed by KOLKWITZ and MARSSON (22, 23) and confirmed by other investigators (20, 24-26), biological water analysis must focus not on the individual organisms, but on the biological community as a whole, i. e. the biocoenosis. Within this, all possible rates of response to changes in the environment are exhibited, ranging from bacteria and protista to higher aquatic plants and animals. "Depending on whether it is wished to investigate the effects of pollution which has only begun
recently or dates back much farther, attention will necessarily focus from case to case on lower or higher organisms for the overall biological assessment." (20)
According to SCHWOERBEL (27), biological analysis of polluted bodies of water is particularly valuable for determining:
1. The current extent of pollution.
2. The capacity for biological self-purification, which cannot be properly ascertained by any chemical method.
3. Whether or not a situation of biocoenotic imbalance exists.
In flowing waters in their natural state, productivity - i.e. plant life - is usually at a low level. This applies particularly to the upper courses of streams. These zones are generally largely heterotrophic, in other words populated by organisms that derive the energy they require from organic matter. This organic material is for the most part allochthonous, i.e. of external origin, such as fallen leaves and substances collected from the stream's catchment area. The longer a stream is, the larger is the catchment area which it drains and consequently also the quantities of allochthonous organic matter entering it. For the same reason, the amount of decayable organic matter, and with it the contamination or saprobity level, is naturally greater downstream than upstream. Correspondingly, the number of heterotrophic organisms is also smaller in the upper areas, especially since tree litter does not decompose quickly. If this situation is changed by the addition of wastewater,
more food is available to the decomposers; they can reproduce at a faster rate, occupy more space, and induce further changes in the ecosystem. For instance, they utilize oxygen and release decay products. At the same time, the decomposers are the food of numerous consumers which, as soon as the abiotic environmental conditions permit, increase in number. As more and more organic matter is broken down, increasing amounts of nutrients are released into the water which can be utilized by autotrophic organisms. This overall process is referred to as selfpurification. As a result of the changing nutrient and food situation, in both polluted and unpolluted rivers a characteristic longitudinal succession of biocoenoses develops. This succession can be utilized to identify the condition of lotic ecosystems, and saprobic or saprobiont classification systems have been formulated on this basis.
3.1.1 Historical background
Over 140 years ago, KOLENATI (28) and COHN (29) made the discovery that the occurrence of certain species is associated with the purity or contamination of bodies of water. Then, in 1870, COHN (30) undertook the first attempt to classify aquatic organisms as indicators for water quality. He assigned organisms to 3 different classes related to the degree of water contamination. About 30 years later, one of his pupils (31) described a microscopic water analysis approach that utilized 4 different categories of organisms. LAUTERBORN (32, 33) then conducted studies which laid the foundation for subsequent work. At about the same time, KOLKWITZ and MARSSON (34) addressed this issue, coining the term of"saprobe" (German: Saprobier; also known as saprobiont) to refer to the indicator organisms discussed here. They initially distinguished three levels of self-purification:
1. Polysaprobic zone= predominantly reducing processes
2. Mesosaprobic zone = partly reducing decomposition, with oxidizing processes dominating
3. Oligosaprobic zone = exclusively oxidizing processes
At this point it should be mentioned that the term chosen to designate the third level is in reality a misnomer. The Greek word sapros (litere suspecte - grecesti sdflghadfklghasdfklgh) means "rotten, rancid", yet by definition only oxidizing processes take place in this zone, and consequently no decayable substances can be present (see also 66).
Soon afterwards, the same authors (22, 23) made a further distinction by dividing the mesosaprobic zone into the alpha mesosaprobic zone, where the water is more highly contaminated, and the beta mesosaprobic zone, with only mildly contaminated water. They also added a fifth level in the form of the katharobic zone, with absolutely clean water. Making use of about 800 plant and animal saprobionts, they formulated a saprobic classification system:
Grossly polluted = polysaprobic zone (p)
Heavily polluted = alpha mesosaprobic zone (am)
Moderately polluted = beta mesosaprobic zone (ßm)
Scarcely polluted = oligosaprobic zone (o)
Completely unpolluted = katharobic zone (k)
LAUTERBORN (35) provided detailed data on an even larger list of organisms, including ecological and physiological information. KOLKWITZ later (36, 37) revised the saprobic system, defining the various levels as follows: characterized by chemical reduction (p), incipient oxidation decay (am), predominant oxidation (ßm), and total oxidation (o). Finally, intermediate levels were introduced: polysaprobic/alpha mesosaprobic, alpha mesosaprobic/beta mesosaprobic, and beta mesosaprobic/oligosaprobic. Every species listed in the saprobic system is also represented in one or more neighboring zones. The numbers of species and individuals are used to draw conclusions on the extent of pollution. LIEBMANN (20, 38) carried the saprobic system developed by KOLKWITZ and MARSSON even further. Taking advantage of the work of other investigators (39-42), he improved its practical usefulness by reducing the number of indicator species to about 260 and adding ecological data. He also
introduced special indicator species for hydrogen sulfide (H2S). LIEBMANN also incorporated measurements of oxygen content, oxygen saturation, and biochemical oxygen demand into his system. In his system, LIEBMANN nominally at least also abandoned the approach of distinguishing the degree to which water is polluted with organic, decayable material, instead referring to "quality classes". This term is definitely not optimum either, in view of the fact that water quality can be defined in any one of a number of different ways depending on the uses to which it is put (e.g. drinking water, fishery, industry). That usage which places the heaviest demands on water purity, namely as drinking water, is taken as the standard here. Although today different demands are placed on the quality of water to be used for drinking than at that time, LIEBMANN's system of water quality classes continues to be used today; p = IV, alfam = 111, ßm = II, o = I (6). SRAMEK-HUSEK (43) and SLADECEK
(44) took the work of other investigators (45-47) who additionally subdivided the polysaprobic zone on the basis of biochemical oxygen demand, and extended the classical system to include particularly intensive pollution with organic waste (eusaprobity: isosaprobity = zone of ciliates, metasaprobity = zone of colorless flagellates, hypersaprobity = zone of bacteria, ultrasaprobity = abiotic zone, but not toxic). They also included toxic and radioactive contami nation as transsaprobity (antisaprobity = toxic zone, radiosaprobity = radioactive waste) (see Figure 2). The Czech system spans all of the pollution levels, although the abiotic zones cannot be biologically characterized.
Other authors (including 48-52) have concerned themselves with classification schemes and special groups of organisms, while others have developed mathematical formulas for the purpose of objectifying results, taking other directions (53-58). A major advance was achieved with the introduction of the concept of the ecological valence of indicator organisms to calculation of saprobity or water quality (59, 60).
In the Federal Republic of Germany the water quality of lotic systems is assessed by an agency operated jointly by the various states (the Landerarbeitsgemeinschaft Wasser = LAWA) using an approach based on the saprobic system of KOLKWITZ, MARSSON and later investigators. Beginning in 1975, water quality maps for the Federal Republic of Germany have been published every five years, the Gewassergutekarten der Bundesrepublik Deutschland. Since 1985 these no longer contain information on the quality of standing waters (see below); instead, the Lunderarbeitsgemeinschaft Wasser has released a special publication on the larger standing water entitled Seen in der Bundesrepublik Deutschland ("Lakes of the Federal Republic of Germany") (61). BICK (62) provides a survey of Central European methods for the biological estimation of water pollution level, and SLADECEK (63) devoted an in-depth analysis to this topic, both of which were written in English. Procedures for biocoenotic
analysis of the condition of bodies of water have also been developed in other countries. ILLIES and SCHMITZ (64) collaborated to write a systematic and critical review of biological methods for evaluating the quality of flowing waters.
3.1.2 Criticisms and counterarguments
There has been no lack of criticisms of biological evaluation of water quality - referred to by some as water quality estimation. These have been compiled and assessed essentially by SLADECEK (63), ILLIES and SCHMITZ (64), and ELSTER (65, 66). A few of these criticisms deserve to be singled out and examined here.
1. The saprobic system is (only) empirical.
The saprobic system was originally based on empirical observation, but has since been developed further; for instance, the ecological valences of a larger number of saprobionts have been tested or statistically calculated (cf. 63, 67, 68, 69). The Lunderarbeitsgemeinschaft Wasser (6) comments as follows: "Numerous studies conducted during the last 2 decades have shown that, as a rule, there is a close correlation between the finding of biological quality estimation and water chemistry data for organic compounds and their decay products." SLADECEK (63) replies to this criticism as follows: "The main criticism - that the system of saprobic organisms is only of an empirical nature - is simultaneously its greatest advantage. What is of an empirical nature, is in accord with the reality seen in the field."
2. The saprobic system is a simplification of natural conditions.
In nature, everything is more complex than our schematic representations of it, and yet this system has proven its worth in practice (70). To a certain extent, this simplification is also intentional: "This depiction in map form of the water quality situation in the Federal Republic of Germany is aimed at presenting the quality of individual bodies of water on the basis of as few parameters as possible in an easily understandable form that is sufficient for general assessment purposes." (6)
3. The assignment of indicator organisms to the various saprobity levels is subjective; the ecological valences of these species are not constant or are unknown; the same indicator organism can occur in different contamination levels.
Proposals made by various authors (including 59, 63, 67, 71, 72) and statistical calculation of species occurrence under different environmental conditions have closed considerable gaps here, with the result that the saprobic indices are now known for"standard" species (cf. 73).
4. The significance of current flow is not taken sufficiently into account.
This is correct. In the long run, where sufficient data is available or can be collected, so-called "coupling analyses" (74, 75) could be effective in remedying this drawback. This approach is currently only being used in Baden-Wuerttemberg. BUCK asserts that use of his method would eliminate errors resulting from the application of conventional saprobic classification schemes for assessment of the degree of contamination of waters with high oxygen influx (see below). With additional analyses, e.g. BOD, COD (KMnO4 consumption), an experienced investigator should be able to help out here (cf. also 76).
5. The species used in the saprobic system have a limited geographical distribution.
There are indeed problems associated with the use of the saprobionts employed in Germany for classification of aquatic ecosystems in other countries or even continents. In Europe alone, 25 different limnic fauna zones can be distinguished (77) in which the standard indicator species are more or less widespread. The expectation that many Central European indicator species will also be found to occur with frequency in tropical regions is no longer shared by many. An exception to this is posed by lower organisms. The more severe the pollution is and the more primitive the indicator organisms are, the less important is their geographical distribution (64). Many unicellular organisms, bacteria and protista are cosmopolitan, i.e. they occur all over the world. Some of them are dispersed by way of the air (78).
6. The techniques used for taking of samples, microscopic analysis and species identification are antiquated. The investigator must possess thorough knowledge of the species, etc.
A great deal has been done to introduce standardized sample taking, data sheets and other norms with an aim to obtaining comparable data (73). It must be stressed here, however, that well-trained staff is essential. Unfortunately, the number of biologists and limnologists with taxonomic expertise has greatly declined. Among others, RATHMAYER (79) has dealt thoroughly with this problem. On the other hand, the originally approximately 800 indicator species postulated by KOLKWITZ and MARSSON were reduced by LIEBMANN to about 260 species for practical and other reasons. And in full agreement with ELLENBERG (2), SLADECEK (63) also writes: "Training is inevitable in saprobiology. Bad work of untrained people does not give good service for science, generally spoken."
7. There is a lack of new classification keys.
This applies even to some parts of Europe, and all the more so in the developing countries. Relatively good literature is available on protista (e.g. 68), but on a global scale large gaps exist where invertebrates are concerned. Here, the "developed countries" are called upon to redouble their efforts by assigning scientists, training staff from "less developed" nations, and supporting studies in countries where little is yet known about these aspects.
8. The assignment of a given body of water to a certain quality class is subjective.
To be sure, study results in Europe have shown that pollution assessments made with different biological methods can only be compared with one another to a limited extent, if at all. Yet, evaluation of a given body of water according to one and the same system, e.g. that which is standardly applied in the Federal Republic of Germany, by groups of investigators from different countries has yielded deviations of only half a quality class or 0.5 saprobic index points. It should also be considered that multiple evaluations of the same section of a body of water by the same person over the course of a year also leads to results within similarly narrow tolerances, even without any changes in the contamination situation. This is due to the fluctuations in the occurrence and abundance of various species which normally occur under natural conditions in lotic systems at a given site during the course of a year (64).
9. In the lower contamination classes, the indicators are a measure of trophic level, not saprobity.
ODUM (80, 81), CASPERS and KARBE (82, 83), and others, have dealt with this topic, making use of vivid graphics to illustrate the correspondences between saprobic and trophic levels (Figure 3). Referred to as the "Prague Convention", the following definition has been accepted: "Within the bioactivity of a body of water, saprobity is the sum total of all those metabolic processes, which are the antithesis of primary production. It is therefore the sum total of all those processes which are accompanied by a loss of potential energy. In combination with the biogenic and physical oxygen component, it determines the saprobity level of a body of water. This level can be ascertained both by metabolic-dynamic measurements and by analysis of the living communities." (84)
That means: the relative proportions of autotrophic (producers) and heterotrophic (consumers and decomposers) organisms in the total biomass of an ecosystem permits conclusions to be drawn on the metabolic-dynamic situation and thus on its saprobity level (83).
I would like to conclude this discussion of the criticisms of the saprobity system with a few quotations:
"Nature distinguishes no systems. All systems are made by man and have the characteristics of human work." (85)
"A system is only a means of instruction, how to put into order the majority of our knowledge." (63)
"Each classification is an approximation of actual conditions and therefore must be viewed with caution." (86)
3.1.3 Water quality evaluation using LAWA criteria
Die Landerarbeitsgemeinschaft Wasser (LAWA) of the Federal Republic of Germany publishes a "water quality map" of the Federal Republic of Germany every 5 years. The most recent of these appeared in 1985 (6). For the purpose of preparing these maps, guidelines have been issued governing the methods to be used for studying bodies of water and evaluating the results. This water quality map only covers flowing waters. The standing waters of the Federal Republic of Germany are covered in a separate document (61). The aim here is to depict in map form the quality of streams and rivers in a readily understandable form that is sufficient for general evaluation purposes. The communities of organisms present are used for estimating the quality of river zones. In addition to biological aspects, a few physical and chemical parameters are incorporated. This work is based on decades of experience, leading to the recognition that, as a rule, close correlations exist between the findings of
biological quality assessments and water chemistry values for easily decomposable organic compounds and their decay products. In general, chemical and bacteriological analyses of randomly taken samples are insufficient for identification of quality classes. These analyses can serve to corroborate and support biological findings. Quality classification on the basis of a 7-level system is regarded as a compromise in which, for instance, natural factors such as differences in oxygen content between mountain and lowland streams are left out of account. Moreover, toxic wastes are only assessed in quality classes III/IV or IV, and then only if their adverse effects on the biological environment are so massive that they are similar to those of extreme contamination with organic material. Salt pollution is also only indicated if the population of organisms is greatly depleted. For this purpose, however, others have developed a so-called "halobic system" that can be used to identify
certain salinity levels and their impact (cf. 3.1.4). It is not possible to depict the presence of trace amounts of toxic substances or organic compounds that degrade slowly or not at all.
For assignment of river sections to quality classes, attention is focused on the level of contamination with organic substances that can be biodegraded with utilization of oxygen. The quality classes distinguished are based on the saprobic system developed by KOLKWITZ and MARSSON, as well as later investigators. The chemical parameters taken into account are the biochemical oxygen demand, and the ammonium (NH4+) and oxygen (O2) contents.
The quality classes are described as follows:
1. Quality class 1: unpolluted to very slightly polluted
River sections with pure water which is always nearly saturated with oxygen and low
in nutrients; low bacterial population; moderately densely populated, primarily by algae, mosses, turbellarians, and insect larvae; if cool during the summer, spawning grounds for salmonids.
2. Quality class I/II: slightly polluted
River sections with low influx of anorganic or organic nutrients without appreciable oxygen consumption; densely populated, usually by a considerable diversity of species; if cool in the summer, habitats for salmonids.
3. Quality class II: moderately polluted
River sections with moderate contamination and a good supply of oxygen; very large species diversity and number of individuals, especially algae, snails, small crustaceans and insect larvae; water plants cover large areas; high fish production.
4. Quality class II/III: critically polluted
River sections in which contamination with organic substances that are decomposed with consumption of oxygen has reached a critical state; fish mortality as a result of oxygen deficiency is possible; decline in the number of macroorganism species; certain species have a tendency towards intense growth; algae often cover entire areas. Fish production is usually still high.
5. Quality class III: heavily polluted
River sections with a high level of contamination with organic substances that consume oxygen as they degrade, and usually low oxygen content; local precipitation of sapropelf colonies of filiform bacteria and sessile ciliates cover entire areas and gain the upper hand over algae and higher plants; only a few macrofauna that are resistant to oxygen deficiency occur occasionally in large numbers, such as sponges, leaches, and water hog lice (Asellus aquaticus); low fish production; periodic fish mortality can be expected.
6. Quality class III/IV: very heavily polluted
River sections with greatly impoverished living conditions as a result of very heavy contamination with organic substances with attendant oxygen consumption, frequently aggravated by toxic wastes; occasionally total depletion of oxygen; turbidity caused by suspended waste matter; extensive accumulation of sapropel deposits, densely populated by chironomids or tubificids; decline in filiform bacteria; fish are encountered only locally for limited periods of time.
7. Quality class IV: grossly polluted
River sections with gross contamination with organic wastes that leads to consumption of oxygen; decaying processes predominate; most of the time the oxygen content is very low or completely lacking; populated primarily by bacteria, flagellates, and freeswimming ciliates; fish are absent; high toxic waste levels lead to complete biological depopulation."
The LAWA also provides a checklist of attributes for evaluation of flowing waters.
Where the details are concerned, the individual states of the Federal Republic of Germany have developed their own guidelines and procedures, all of which are essentially based on the saprobic system elaborated by KOLKWITZ and MARSSON (22, 23) and LIEBMANN, the so-called K-M-L (named after KOLKWITZ, MARSSON and LIEBMANN) system (20). The "guidelines for the determination of water quality classes" of the state of North-Rhine/Westphalia (73) will be dealt with here in greater depth; it provides a good illustration of the registration and evaluation processes involved.
The above-mentioned set of guidelines was developed for the state of North-Rhine/Westphalia on the basis of uniform criteria which were formulated by the Lunderarbeitsgemeinschaft Wasser (LAWA) for evaluating the quality of flowing waters. These guidelines also cover the use of appropriate forms for automatic data processing. Where required, reference is made to the "methods of biological-ecological water analysis" (Methoden der okologisch-okologischen Gewasseruntersuchung) (87):
Flowing waters are defined as all thermally unstratified bodies of water flowing in one direction at a velocity greater than 1-3 cm/s. According to DEV (German standard methods for the examination of water, wastewater and sludge) (87), a body of water does not cease to be a stream until its flow rate falls below I cm/s.
A given flowing water can be characterized by the fauna and flora that populate it, and by its hydrographic, chemical and physical status. Since every aquatic organism is dependent on certain attributes of its habitat and places certain demands on them, if these demands are known it is possible to derive information on the condition of a body of water from the community of organisms present in it.
At what times and how often studies are performed depends on the purpose to which the results are to be put. If it is wished to monitor the general condition of a body of water, to map its water quality and record longterm changes, then a single annual study is usually sufficient. It is best to choose a time when the water level is as low as possible. The reason is that the biocoenotic situation at the time of low water makes differences in the contamination of different river sections particularly apparent. If seasonal fluctuations can be expected and/or are regarded as important, it is necessary to perform separate studies in the spring, summer, autumn and winter. Even more thorough analysis, e.g. for obtaining data relevant to fish production or limnological investigations in connection with current flow regulation, construction of locks and the like, call for monthly tests.
Of particular importance is the choice of methods and sites for taking of samples; factors such as current flow and the form and chemical composition of the substrate are significant and make it necessary to take an appropriate number of samples. The number of sites at which samples are taken depends on the one hand on the motivation for conducting the study, and on the other hand on the relative uniformity or heterogeneity of the river section under investigation. If the river zone contains a diversity of microhabitats, more samples will be needed, e.g. if the current flow characteristics are different along the two banks, or if the river bottom consists of a variety of different materials, like large stones on a pebbly substrate with deposits of organic matter on their downstream side, etc. For evaluation of the impact of waste discharged into a flowing water, a minimum of sampling sites is required to study a waste-free stretch above where the waste enters and several
sites below the point of entry reaching far enough downstream until the stream has completely recovered and reattained its original condition.
Depending on what type of river or stream is being studied, different instruments must be used for taking samples (cf. 87). These must be suitable for obtaining samples of sedentary and substrate-linked macroorganisms and microorganisms, since as a rule only these are suitable for assessing water quality (cf. 66). It is often not easy to obtain large enough quantities of sufficient quality of all microorganisms for microscopic analysis. Here, a method has proven its worth which was used as early as 1916 (24), being improved later (88). We have successfully tried out several new developments. Pairs of glass slides are submerged in the water. Placed in appropriate receptacles, the slides can then be transported easily and subjected to microscopic analysis (89).
Biological-ecological studies are carried out at representative, hydrologically comparable sampling sites at low to medium water levels, giving consideration to all of the microhabitats characteristic of the flowing water under study (stones, mud deposits, areas populated by water plants, etc.). For purposes of evaluation, data is collected on the sedentary and substrate-bound macroorganisms and microorganisms. In addition, chemical and physical measurements can supplement the biological findings (Table I ).
Field and laboratory reports are used for data collection and evaluation:
1. Each sampling site is clearly described on a "master form" (cf. Figure 4).
Table 1: Comparison of biocoenotic and chemical parameters corresponding to the individual quality classes and saprobic levels (from 6).
Quality class
Extent of organic pollution
Saprobic level
Saprobic index
Chemical parameters
BOD5+
NH4-N+
O2 minima+°
I
Unpolluted to very slightly polluted
Oligosaprobic
I
Traces
I-II
Slightly polluted
Transition between oligosaprobic and beta mesosaprobic
Approx. 0.1
II
Moderately polluted
Beta mesoaprobic
II-III
Critically polluted
Alpha-beta mesosaprobic transitional zone
III
Heavily polluted
Alpha mesosaprobic
0.5 to several mg/l
III-IV
Very heavily polluted
Transition between alpha mesosaprobic and polysaprobic
Several mg/l
IV
Grossly polluted
Polysaprobic
Several mg/l
+ The chemical data given in this table only provide guidelines for frequently encountered concentrations.
° The minimum oxygen contents in rapidly flowing mountain streams of quality classes II through IV are frequently greater than the values indicated in the table.
2. In "field report 1" (cf. Figure 5) the physiographic conditions are entered, i.e. the factors of relevance for the plants and animals populating the site. These data are used both to check the plausibility of the biological data and to monitor any changes during the course of a series of tests.
3. In "field report 2 - macroorganisms" (Figure 6) all plants and animals are listed which can be detected at the study site with the naked eye. 33 frequently occurring species that can be identified in the field and which can be utilized for calculating the saprobic index are printed on the form. Species are also included here that provide data on other aspects, e.g. animals which are eaten by fish, etc. In addition, 77 further species with their corresponding saprobic indices and indicative weights (see below) are listed. When required for more detailed analysis of the occurrence of macroorganisms, samples are taken for laboratory evaluation.
4. In the "laboratory report form - microorganisms" (Figure 7) the results of microscopic analysis of the "Aufwuchs" or periphyton are entered. Here too, 68 frequently occurring species are printed on the form, as well as an additional 119 in a "list of microorganism species" together with their saprobic indices and indicative weights.
The frequency of occurrence of sedentary and substrate-bound organisms is estimated semiquantitatively and expressed in terms of the following levels:
1 = isolated findings (present)
2 = low occurrence
3 = low to medium occurrence (abundant)
4 = medium occurrence
5 = medium to high occurrence (characteristic)
6 = high occurrence
7 = massive occurrence (dominant)
Approximate figures can also be assigned to these levels (from 90) to give an idea of their quantitative significance (Table 2).
All of the species listed here and others that can be utilized as indicator organisms are designated by a number referring to a "key list" (91) valid for the Federal Republic of Germany. This can be utilized for automatic evaluation by an appropriate computer program.
Table 2: Comparative figures (compiled from 73 and 90).
Frequency
Macroflora
Macrofauna
Microscopic growth according to size classes
L <= 15 mium
15-50 mium
50-200 pm
200-1500m
From the raw data which have been collected, the "saprobic index" (S) at the sampling site is calculated either manually or with the aid of a computer program. This denotes the degree of contamination of the water with biodegradable organic waste on the basis of the 4-level system developed by SELINKA and MARVAN (59) (see above). The following formula is used:
Where:
s = saprobic index of each species
h = estimated frequency of the species (see above)
g = indicative weight of the species
The indicative weight gives consideration to the fact that most of the indicator organisms are not restricted to a single saprobity zone; instead, their distribution range is merely concentrated in one zone. The indicative weights and saprobic indices of the individual species can be obtained from the above-mentioned species lists. The following simplified examples illustrate calculation of the saprobic index for a sampling site:
Species name
hs
g
Acroloxus lacustris
Ceratophyllum demersum
Elodea canadensis
Planaria torva
Sphaerium corneum
Cocconeis pediculus
Cymatopleura solea
Litonotus cygnus
Synedra ulna
S= 1135 / 540 = 2.1
A similar approach proposed by PANTLE and BUCK (54) is also in use. Here, the saprobic index (s) is calculated according to the formula:
Where:
s = saprobic index of each individual species
h = estimated frequency of occurrence of each species expressed in terms of a 3-level scale (I = isolated finding, 3 = frequent occurrence, 5 = massive occurrence)
KNOPP (92) uses a 7-level frequency distribution scale together with species figures and their corresponding characteristics to calculate the "relative quality" (rQ):
and the "relative contamination" (rC), expressed as a percentage:
Parallel to biological studies, in the LAWA system several physical and chemical parameters are measured on the basis of random samples (Figure 8). This yields supplementary data which round out the picture obtained by the biological evaluation, corroborating certain aspects and possibly indicating special features. Table I incorporates several important parameters in the form of frequently occurring concentrations (from 6); this table lists both saprobic levels (22, 23) and quality classes (20).
3.1.4 Indicators of the salinity of inland waters
In the water quality evaluation scheme based on LAWA criteria (cf. 3.1.3), salt pollution is only indicated in the case of greatly depleted communities of organisms. With the aid of the "halobic system", however, it is possible to determine the biological impact of salt concentrations in inland waters with greater accuracy. Halobes are indicator organisms capable of providing information of certain salinity ranges for inland waters. Diatoms have proven to be particularly well suited for indication of contamination of this type (93, 94); various animal species are additionally monitored.
The halobic system can only be used for assessment of the degree of salinity of inland waters, however; it is not appropriate for diagnosing the salinity of thalassogenic waters, i. e. those that are influenced by marine water (95). This is due to the fact that marine and coastal brackish water is subject to completely different hydrographic and population-related conditions than saline inland waters.
On the basis of the halobic system (93), ZIEMANN (94) has elaborated a scheme for ecological classification of inland waters according to the biological impact of their salt concentrations. Fresh waters are characterized above all by a predominance of calcium bicarbonate ( Ca(HCO3)2). At low calcium bicarbonate concentrations, the pH level additionally influences the composition of the biological community. With increasing salinity, the alkali/calcium ratio then grows in importance. In biological terms, it is especially the alkali ions and the increased osmotic pressure which play a role. In addition, the effects of other specificions can be important.
HUSTED (93) distinguishes the following categories in his halobic system:
1. Polyhalobes (ph):
Salt concentration 30 or higher (euryhaline species also occur at below 30 0/00)
2. Mesohalobes (mh):
- Euryhaline mesohalobes: salt concentration of approx. 0.2 - 30 0/00
- Alpha mesohalobes: species typical of "lower" brackish water, minimum NaCl concentration approx. 10 0/00
- Beta mesohalobes: species typical of "upper" brackish water, salt concentration approx. 0.2-10 0/00
3. Oligohalobes:
- Halophilic species (hp) < 0.2 0/00
- Indifferent species
4. Halophobic (haloxenic) species (hx)
Thus, polyhalobes and mesohalobes are indicators for increased salt concentrations, while oligohalobes are characteristic of fresh waters. Among these, the development of halophilic species is stimulated by increased salt concentrations. By contrast, halophobic species are typical of extremely salt-poor waters, e. g. acidic moorland waters.
Going a step further, ZIEMANN (94) analyzed the occurrence of certain indicator species in water with different salinities, thus laying the groundwork for an ecological classification of inland waters on the basis of the biological impact of their salt concentrations. This is illustrated in Table 3.
A given body of water is classified by calculating its "halobic index" (H) with the following formula:
Where:
hH = sum of the frequencies of the halophilic
and halobiontic species (hhp + hmh + hph)
hX = sum of the frequencies of the haloxenic
species
h = total frequency
The following halobiotopes are distinguished on the basis of the halobic index:
H =< 30:
infrahalobic
H = -30 to -10:
gamma oligohalobic
H = -10 to +10:
beta oligohalobic
H = +10 to +30:
alpha oligohalobic
H = +30 to +50:
beta mesohalobic
H = +50 to +75:
alpha mesohalobic
H = >+75:
polyhalobic
3.1.5 Macrophytes as indicators of the ecochemical composition of fresh waters
The high indicator value of higher plants, so-called macrophytes, for evaluating the water quality of the littoral zones of standing and flowing waters has been demonstrated by numerous studies (90). In addition to a large number of swamp and water plants, water mosses and algae of the family Characeae also possess this attribute. These indicator species provide information on the chemistry of the water and soil. Since a fair amount of time is required for a macrophyte community to develop, analysis of it reflects a condition which has remained relatively stable over a lengthy period of time. To some extent, even short-term changes in water chemistry can be detected. for example by changes in the visible appearance of plant individuals. Similarly to water quality estimation with the aid of the saprobic system, evaluation of the ecochemical composition of waters with macrophytes also involves examination of biocoenotic systems, in this case floral communities.
Table 3: Classification of inland waters according to the biological impact of salinity (based on 94, modified and expanded).
Class
Subclass
Water characteristics
Halobic index
Fresh waters
Infrahalobic
Extremely low salt concentration, halophobic species predominate
Gamma oligohalobic
Calcium-poor waters, oligohalobic species predominant,
halophiles diminishing in number
Oligohalobic
Beta oligohalobic
Typical freshwater bodies, strictly oligohalobic diatom community
Alpha oligohalobic
Fresh water with slightly raised alkali/calcium ratio, oligohalobic species
with frequent blooms of halophiles
Saline waters
Mesohalobic
Beta mesohalobic
Moderately sahne, intense growth of halophiles, halobionts and
euryhaline oligohalobic species, incipient injury to fresh water species
Alpha mesohalobic
Strongly saline, halobiontic species predominate, freshwater species
greatly diminished
Polyhalobic
Polyhalobic
Extremely saline, very few species grow well
Water chemistry is primarily determined by the geological conditions at the site and within the catchment area. It allows a specific form of water vegetation to develop. This can then be modified in a characteristic way by changed trophic conditions as a result of influx of anorganic or organic waste.
On the basis of observations of correlations between frequently occurring species and plant communities on the one hand and various degrees of water pollution on the other, with the aid of the so-called "coincidence method" it has been possible to calibrate most Central European species of water plants and the most important groups of species for indication of the impact of certain environmental factors. In all, over 20 water chemistry parameters have been related to the most important plant species. The characteristic values have been organized into a 5-level system. Level l denotes the lowest degree of contamination, level 5 the highest.
For evaluation of water chemistry with the aid of indicator species, qualitative and quantitative data must be collected on all of the macrophyte species occurring at a site. The floristic-sociological structure can then be used to calculate the value corresponding to the most important ecological site factors. The actual calculation of the average factor number of a macrophyte community is performed using the standard formula for determining the arithmetic mean:
Where:
x = average factor number
n = number of macrophyte species considered, i.e.
number of individual values measured
xi = individual factor numbers ( 1, 2,..., n)
A good summary of this method is given in (90). It is similar to that used by ELLENBERG (96) in the field of terrestrial ecology.
A number of different water plants utilize anorganic carbon compounds in different ways, and are therefore good indicators of the pH level and the carbon dioxide complex, among other factors. Important cations and anions are also indicated, e. g. Na+, K+, Ca++, Mg++, total Fe, Cl-, SO4-- , and SiO2, as well as trophic levels like those of NH4+, NO3-, PO4---, O2. and dissolved organic matter.
As an example for diverging indicator values, i.e. factor numbers, the parameter ranges indicated by two species, namely Nitella flexilis and Salvinia natans are listed in Table 4.
3.1.6 "Coupling analysis"
BUCK (74, 75) developed his "coupling analysis" on the basis of the mathematical postulates of set theory. If only a limited num ber of species are found, coupling analysis is more accurate than the saprobic index. Less labor is also involved. BUCK is of the opinion that coupling analysis gives a more reliable indication of contamination with organic substances, since there is not necessarily a one-to-one correspondence between organic matter and the oxygen content of the water. This applies particularly when assessing strongly turbulent waters with intensive oxygen influx due to physical phenomena. The reason is that many saprobionts react more sensitively to the oxygen content of the surrounding water than to the organic matter carried by it. In the case of such turbulent waters, therefore, a misleadingly positive assessment of water quality results. When calculating the amount of organic waste which can be safely absorbed by a river, this can lead to mistakes with
catastrophic consequences for downstream river sections with less turbulence. "Coupling analysis" has one major drawback, however: its use presupposes that thorough analyses be performed beforehand of the floral and faunal composition of a large number of study sites (64). That is why, in the Federal Republic of Germany, this system is presently only in use in Baden-Wuerttemberg. An example is the cartographic work on "Water Quality in Baden-Wuerttemberg" (Gutezastand der Gewdsser in Baden-Wurttemberg) (5). ILLIES and SCHMITZ (64) therefore correctly state: "For fundamental, e.g. biogeographical, reasons it is impossible to expect that, unless it is modified, it will be possible to apply the coupling analysis system developed by BUCK outside of Baden-Wuerttemberg in other parts of Europe or even everywhere within the Federal Republic of Germany."
Table 4: Factor numbers (F) and quantities (Q) of selected ecochemical parameters of two aquatic plant species with differing environmental requirements (compiled on the basis of 90). All quantity figures except pH in mg/l. * mg/l of consumed permanganate.
Parameter
Nitelia pexilis
Salvinia natans
F
Q
F
Q
pH
CO2
HCO3
NH4
Na+
K+
Ca++
Mg++
Total Fe
Cl-
NO3
PO4--
O2
Dissolved organic matter
3.1.7 The "species deficit" method
One method which is based exclusively on the number of species of macroorganisms present, but can also be extended to include the number of species of microorganisms, is referred to as the "species deficit" (Artenfehlhetrag) technique (97). This method is derived from THIENEMANN's "basic biocoenotic law" (98): "The more varying the conditions of life are in a place, the greater are the numbers of species in the community present at the locality. The further conditions of life in the locality concerned are distant from the conditions that are optimal for a majority of species, the poorer in species becomes the biocoenosis, the more characteristic, and the more numerous each species" (quoted in English in 51 ).
KOTHÉ assumes that the number of species declines under the influence of both organic and toxic waste. All of the occurring macrofauna and macrophytes are taken into account. Difficulties are associated with the postulation of a binding figure for the "normal" or standard number of species of a given biocoenosis (ideally under unpolluted conditions). This is because in small streams the physiographic conditions and thus the biocoenoses change with increasing rapidity as one approaches the headwaters. It is much easier to determine the species deficit in longitudinal studies of large rivers with uniform physiographic conditions over long distances. In practice, the standard figure for number of species is taken at the beginning, i.e. upstream, of the river section under study. If surveys are conducted at different sites using the same methods, the species deficit (SD) can be calculated on the basis of the number of species at the reference sampling site (S0) and the number of
species at any locality (Sx) downstream of S0. The result is expressed as a percentage. SD = 0 means that there is no loss of species, while SD = 100 % corresponds to complete obliteration. The formula used for calculation is as follows:
3.1.8 Biological-ecological water analysis (of flowing waters) using the DEV method (87)
Samples are taken and analyzed as described in section 3.1.3. A list of species is prepared containing information on their frequency in terms of the above-mentioned 7 frequency levels, if relevant also in the form of absolute frequency and/or quantity values per unit area (number of individuals per m², for plankton number of individuals per ml). A practical example is illustrated in Tables 5 and 6.
SCHWOERBEL (27) gives a survey in table form of the time requirements, depletability, completeness and accuracy of various biological water analysis techniques (Table 7).
3.1.9 Depiction of results
For specialists, simply listing the saprobic indices of individual sections of flowing waters as measured at sampling sites is readily understandable. But for conveying information to persons who are not as familiar with the subject matter, graphic depictions are quite useful. Various approaches have been developed for this.
Table 5: Practical example of: Compilation of biological/ecological study findings in tabular form; here: population table with classification of organisms by the saprobic system in compliance with Paragraph 8a (from 87).
Investigation of the .....river
Investigated section: from .........to mouth
Date of inspection: July 21, 19....
Population table
Sampling site number
River kilometer (from source)
Day and time samples
were taken
Weather on day samples
Sunny
Sunny
Sunny
Sunny
Sunny/ overcast
Ovvercast
were taken
Dry
Dry
Dry
Dry
Dry
DDry
Saprobity level
Water temperature in °C
Site designation
... river
... river
... river
Tributary
... river
... river
above
below
Headwaters at
at ...
300 m below
dam or lock
(approx.
(town)
discharge of
500 m above mouth)
industrial waste
Indicator organisms
Spongila fragilis
bmms
Pelmatohydra oligactis
bmms
Planoria torvo
emms-bms
Tubificidae gen. spec.
pss-ems
Clossosiphonia complanata
bmms-os
Helobdella stagnalis
emms-bms
Haemopis sanguisuga
bmms
Herpabdella octoculata
aams-bms
Plumatella repens
bbms-os
Paludicella articulata
bmms-os
Gammarus pulex
bbms-os
Asellus aquaticus
amms-bms
Potamanthus luteus-L.
bmms-os
Cloëon sp. Larvae
bbms-os
Agrion sp. larvae
bmms-os
Sigara striata
Haliplus spec.-Imago
Leptoceridae-gen. spec.-L.
bmms-os
Chironomidae larvae
(undetermined)
Eristalis sp. larvae
ps
Radix ovia
aams-bms
Planorbis corneus
bmms
Ancylus f laviatilis
amms-bms
Bythinia tentaculata
amms-bms
Viviparus viviparus
amms-bms
Pisidium spec.
Sphaerium corneum
amms-bms
Frequency levels: 1 = Isolated findings; 2 = Low occurence; 3 = Low to medium occurrence; 4 = Medium occurrence; 5 = Medium to high occurrence;
6 = High occurrence; 7 = Massive occurrence
Table 6: Practical example for: Compilation of biological-ecological study findings in tabular form; here: evaluation of biological-ecological study findings in compliance with Paragraph 8b and c (from 87).
Investigation of the .................river
Investigated section: from ............to mouth
Date of inspection: July 21, 19...
Sampling site number
Site designation
... river
... river
... river
Tributary
... river
... river
above
below
Headwaters at dam or lock
at ...
300 m below
(approx. 500 m above mouth)
(town)
discharge of industrial waste
Water quality class (saprobity level)
Biological water quality class
II
III
III-II
I
II
No change in saprobic level, but biocoenoticc depletion caused by toxic industrial wastewater
I = Not
II = Moderately
III = Heavily Polluted
IV = Grossly
Biological characteristicligures for population table
å os
1 I.3
å bms
å ams
å ps
å ps + ems + bms + os
Biological relevant organic pollution in %
(å ((ps+ams)/å(ps+ams+bms+os)) 100
Saprobic index
(4å ps+3å ams+2å bms+1å os)/ å (ps+ams+bms+os)
Species deficit in °70(S1 = standard no. of species: 25)
((S1-Sx)/S1)·100 (cf. M 7)
Table 7: Assessment of methods for biological water evaluation (from 27)
Method
Time requirements
Depictability
Completeness
Accuracy
KOTHE
Very low
Very good
Low
Very low
KNOPP
Low
Very good
Moderate
Moderate
PANTLE u.
Moderate
Very good
Good
Good
BUCK
ZELINKA &
Very great
Good
Very good
Best
MARVAN
Figure 9: Section of the water quality map of the Federal Republic of Germany (changed, from 6). The original map is printed in seven different colours corresponding to the seven classes of water quality. For water quality classes see Tab. 1.
For the water quality map of the Federal Republic of Germany (6), the declared aim has been to make use of as few parameters as possible in order to present information on the quality of bodies of water in a readily understandable way that is adequate for general evaluation purposes. The cartographic approach used is based on LIEBMANN's system (20), who assigned different colors and hatching types to the various quality levels (KOLKWITZ and MARSSON = saprobic levels) as follows: IV (ps) = red, III (ams) = yellow, II (bms) = green, I (os) = blue. In contrast to LIEBMANN, who used colored hatching in alternating colors to designate intermediate levels, e. g. yellow/green for III/II, the LAWA uses intermediate hues: IV/III (ps/ams) = orange, III/II (ams/bms) = light green, II/I (bms/os) = light blue. For general purposes, the system illustrated in Figure 9 is well-suited and easy to understand.
The depiction techniques used in (87) are more informative and easy to read. Results obtained using the procedures developed by PANTLE and BUCK (54) (cf. 3.1.3) are depicted in the first and fourth quadrants of a 2-axis coordinate system. The x axis corresponds to the kilometers, and the calculated sums åps, åams, åbms and åos, corresponding to the various kilometer positions, are entered on the y axis as follows:
åbms as a positive y value above the x axis
åos as a positive y value added on top of åbms
åams as a negative y value below the x axis
åps as a negative y value added below åams
By linking the corresponding points and filling in the bands with different colors or types of hatching (see above), a vivid representation of the population figures for the 4 saprobic levels is obtained. Since the total y values at a given sampling site are also a measure of the total population density at that locality, they also denote eutrophication, depletion or depopulation (cf. Figure l 0). The biological impact of organic contamination is calculated using KNOPP's method (92) (cf. 3.1.3). The corresponding saprobic indices and/or pollution levels as indicated in the example can also be added beneath the graphic depiction using the method proposed by PANTLE and BUCK.
Finally, the species deficit calculated in KOTHÉ's method (97) can also be entered in the same graphic representation (see below). Figure 10 shows an example of this type of combined representation taken from DEV (87).
3.1.10 Special applications of biological water analysis for surveys of water pollution in the Federal Republic of Germany
Studies of bodies of water are naturally not merely aimed at identifying their current condition and/or any positive or negative changes which this may undergo; they also serve to forecast additional sources of contamination, reduction in contamination levels, e.g. after construction of purification plants to improve water quality, and the potential impact of plant hydraulic engineering measures. In the Federal Republic of Germany, over a period of years a model for computer assisted water quality simulation has been developed on the basis of physical, chemical and biological analyses (99-104). This is intended to make available an instrument to planners with which they can better assess the likely impact of planned measures on water quality. Water quality simulation can make a more or less comprehensive contribution to system, data and impact analysis. The most important field of application is regarded as being that of impact analysis. The following parameters can be
simulated: CBODs, nitrogen cycle, reactive phosphorus, algal biomass, zooplankton/fish, dissolved oxygen, substances with a preservative effect, radioactive substances, coliform bacteria, temperature. The most important interconnections are shown in Figure 11 (based on 104). More detailed information is provided by the same source.
3.1.11 The R-P-C system and BIP
Finally, two other simple methods of biological water analysis deserve mention, although these yield only a limited amount of information. The WHO included these methods in its International Standards of Drinking Water ( 105).
In Chapter I I briefly sketched the interconnections among the three major groups of organisms (producers, consumers and decomposers) based on their biological functions. GABRIEL ( 106) has developed a simple water evaluation concept based on these interconnections. In the most strongly polluted zone the decomposers or reducers (R) predominate, in the next zone the number of consumers (C), which feed on the decomposers, increases, and finally, with increasing self-purification (i.e. mineralization) the autotrophic producers (P) gain the upper hand. GABRIEL ( 106) uses these three values to calculate an index as follows:
I (Index) = 2 · P / (R + C)
The "biological index of pollution" is even easier to calculate (107). Here, the author only takes into account the relative numbers of chlorophyllous (A) and achlorophyllous organisms (B) to define this index:
BIP = 100 · B / (A + B)
3.1.12 Evaluation of standing waters
For years there has been a great deal of controversial discussion on the issue of whether the saprobic system can also be applied to evaluation of standing waters (cf. 65, 66, 70, 82, 83, 108-110). In the following, this discussion will be briefly summarized.
To begin with, here are a few definitions of basic concepts: oligotrophic is used to refer to waters with low nutrient availability and thus low production. They are, literally, "scantly nourishing". Consequently, in an oligotrophic body of water the number of organisms is relatively low. Eutrophic is applied to fresh-water bodies which are rich in plant nutrients and therefore have a high rate of organic production. They are literally "highly nourishing". In eutrophic waters the number of organisms is thus relatively high. The term saprobity has to do with a water body's content of decomposable organic matter and the consequences which its breakdown has, while -trophy or trophic refers to the nutrient status of a water body and its implications. KOLKWITZ (36) however lists indicator organisms as:
1. Polysaprobes in standing and flowing waters containing readily decomposable domestic sewage.
2. Mesosaprobes in well-drained fish ponds, etc.
3. Oligosaprobes (such as in Lake Geneva, etc.)
LIEBMANN (20) also cites typical biocoenoses of indicator organisms, e. g. "in standing and slowly flowing waters" of the alpha and beta mesosaprobic and oligosaprobic zones. While KOLKWITZ (36) goes on to make a comparison of saprobic and trophic levels, LIEBMANN rejects this approach; for him, the concepts of "oligosaprobic" and "oligotrophic" are virtually identical, but he is unable to correlate the concept of "eutrophic" with "any saprobic level at all". The "Prague Convention" (84) (cf. section 3.1.2) documented the situation. ODUM (80) and CASPERS and KARBE (83) provided a schematic representation in terms of interactions between primary production and respiration. By way of explanation, the reader is referred here to the scheme put forward by CASPERS and KARBE (83) (cf. Figure 3).
The Landerarbeitsgemeinschaft Wasser of the Federal Republic of Germany ( I 11 ) performed a classification of standing waters incorporating their trophic levels; this study was completed in 1980. SCHWOERBEL (27) believes that the resulting quality maps (e.g. of Lake Constance) are very instructive, and approves of the use of the colors yellow and red to indicate critical zones. Because of the entire complex of problems and the ongoing discussion of the applicability of the evaluated indicator species, particularly for flowing waters, as well as the controversy about the overall procedure, the most recent edition of the water quality map for the Federal Republic of Germany (6) no longer included standing waters. In the Federal Republic of Germany, a special working group was formed for the purpose of elaborating a new approach; it has not yet submitted the results of its work. If the procedure is applied in a thorough and discerning manner, taking additional factors into
account such as the form characteristics of the body of water, the geology of the catchment area, etc., however, values can be obtained that are suitable for tentative classification (cf. 112). At least for littoral zones, it is also feasible to use the method described in section 3.1.5 for monitoring of the ecochemical attributes of water bodies with the aid of macrophyte communities. For the purpose of providing a readily understandable survey of the nutrient situation of lakes, the LAWA (111) previously used a system of 4 trophic levels for classification of standing waters. This categorization of lakes according to trophic levels involves certain difficulties, however, since the interrelationships between nutrient influx and its impact on the oxygen metabolism of a water body are highly dependent on its morphology, in particular its depth. The way in which the trophic levels are now defined is based for the most part on information which has been collected on Bavarian
lakes. It still remains to be seen whether these definitions are appropriate for classification of lakes in other parts of the Federal Republic of Germany. The working group must resolve this question. For the time being, these definitions are still tentative.
According to this preliminary approach, standing waters are assigned to quality classes on the basis of their trophic levels, i.e. their nutrient status and its effects on oxygen content:
1. Oligotrophic lakes
Clear, nutrient-poor lakes with low plankton production that are characterized by oxygen levels of over 70% of saturation even at great depths at the end of the summer stagnation period.
2. Mesotrophic lakes
Lakes with low nutrient availability, moderate plankton production, and visibility depths of over 2 m whose lower layers are characterized by oxygen contents of between 30 and 70% of saturation at the end of the summer stagnation period.
3. Eutrophic lakes
Nutrient-rich lakes whose lower layers are poor in oxygen at the end of the stagnation period (0-30% of saturation); the water at the surface is at times oversaturated with oxygen. The visibility depths are usually less than 2 m, and heavy plankton growth is typical.
4. Polytrophic lakes
Lakes with a very large supply of plant-available nutrients; the lower layers are depleted of oxygen in the summer, with production of hydrogen sulfide part of the time; the surface water is greatly oversaturated with oxygen part of the time; very low visibility depths; overproduction of phytoplankton.
In the chemical metabolism of standing waters, free-living plankton play a dominant role. In order to assess the trophic level of a body of water, biological and chemical studies are performed on vertical profiles, as well as analyses of the sedentary organisms populating the littoral zone and the lake floor. Vertical profiles are surveyed at the end of the summer stagnation period, since the greatest degree of oxygen depletion can be expected above the lake bottom at this time. In order to obtain more detailed information on a lake's oxygen metabolism, additional studies distributed over the entire year are necessary.
The trophic levels of lakes, namely oligotrophic, mesotrophic, eutrophic and polytrophic, are depicted using the colors blue, light blue, green, and yellow, respectively. Because of the different attributes considered for evaluation purposes, complete correlation of the water quality of lakes with that of flowing waters of the same color is not possible.
Further detailed discussion based on long experience is given in (242). A new comparatively simple method of defining the trophic state of stagnant waters will be published in the near future (243). And recently SCHMIDT (244) has made an attempt to classify tropical lakes and reservoirs of Brazil.
It should also be pointed out that additional biological factors must be taken into account for evaluation of lakes, for instance productivity (measured using the radiocarbon method).
3.1.13 Drinking water
The methods described above are not sufficient for assessing the quality of drinking water. Here, additional chemical, medical and hygienic analyses are required. On the one hand, pathogens must be studied, such as certain bacteria, viruses, protozoa, worm species, etc. On the other hand, organic and/or anorganic toxins can be dissolved in the water. These can be of natural origin, such as certain substances secreted by algae, or anorganic contaminants leached out of the rock substrate, e.g. fluorides (India), chlorides, etc. Human activities can aggravate this natural contamination. New pollutants are discharged into the water as well, for instance organic matter that decomposes very slowly or not at all, like pesticides, or anorganic substances, such as heavy metals. These can find their way into the water in sewage or via the atmosphere. Even nitrates, which are important plant nutrients, are anthropogenic contaminants when they occur in high concentrations. They can get
into bodies of water via domestic or industrial sewage, or be washed out of fertilized farmland. In addition to preliminary assessment by means of biocoenotic studies, here two possibilities are available for biological monitoring, making use of certain test procedures and organisms. For example, suitable fish tests exist in which fish are made to swim in water that has been processed for drinking. If they exhibit unusual behavior, this is an indication that toxic substances are present in the water, although without revealing which toxins are involved. "Electric" fish can be used for this, as well as other tests (19). Certain electric fish species (18) can often be used to indicate even very small concentrations of toxic substances. However, instead of the species recommended in the literature it would be better to use fish that emit uniform electrical signals, such as the species of the genus Eigenmannia (113). Any changes could then be automatically detected and evaluated
more easily.
3.1.14 Application of biological water evaluation methods in developing countries (questions, problems, possibilities)
In general it can be stated that the methods used for the water quality map of the Federal Republic of Germany (6), as well as most of the other approaches described here, could also be applied in developing countries. A number of preconditions must first be fulfilled, however, and some aspects of the overall concept would have to be sacrificed, at least for the time being.
In the major works which have been published on biological water quality analysis it is stressed again and again that entire biocoenoses, not individual indicator organisms, are important for evaluation. Exclusively physical and/or chemical analyses, even if they include bacteriological studies, are not sufficient to yield meaningful assessment of a water body (20, 66). BICK et al. (114) have pointed out possibilities for determining saprobity levels, for example in India, and presented a preliminary list of indicator species in general use in (Germany which also widely occur on the Indian subcontinent. On the whole, however, very little has been published on attempts to apply biological water quality analysis in developing countries. And most of these few studies have only limited relevance, due to the small number of species used and their lack of thoroughness. An example of this is the study carried out by NANDAN and PATEL (115), which includes neither a complete
biocoenotic analysis nor calculation of the saprobic index or the like on the basis of a standardized procedure. Moreover, lists of indicator organisms contained in the literature are not always used in accordance with the instructions given for them. By contrast, the study by RAI (116), conducted in the area around Delhi, India, is quite thorough.
This brief criticism leads us to the first problem. In the developing countries, as well as elsewhere, there is a lack of trained personnel for the collection, identification and evaluation of indicator organisms. There is agreement among both critics and advocates of biological water analysis that well-trained staff is needed in order to obtain meaningful information using the above-mentioned systems. There is an urgent need for Europeans experienced in the use of such analytical methods to be sent to developing countries to carry out studies on-site and train local staff, and for the latter to receive further training in Europe. It would definitely be more meaningful for this work to be carried out directly in the developing countries concerned. The reasons for this are explained further below.
The second problem is the geographical distribution of "our" indicator species. Even in Europe, which is relatively poor in species as a result of its geological development, including the impact of the ice ages, not all species occur everywhere that are, for example, contained in the DVKW list (83). This is illustrated by the following comparison.
Of the 25 different faunal zones in Europe, Rivulogammarus fossarum (s = 1.3; g = 4) only occurs in 14, Agapetus fuscipes (s =1.0; g = 5) and Clossosorna boltoni (s = 1.1; g = 5) in 11, and Rhitrogena semicolorata (s = 1.0; g = 5) only in 12 zones (77). This problem thus exists within Europe, and the difficulties grow as one moves further away from the "core region of biological water quality evaluation". It will therefore be essential to perform regional studies and calibration of macrofauna and macroflora species.
Does this mean that the optimism expressed at the beginning of this chapter is not justified? When applying the saprobic system, it is essential to initially concentrate on cosmopolitan species. These can be found above all among the protista. It is no accident that BICK et al. (114) began by studying such organisms. And comparisons with other publications (117-143) show that a large number of unicellular animal and plant species are "cosmopolitans". With the number of relevant studies, the number of known protista that occur throughout the world will also grow, in the same way that the number of known plant and animal species is "high" in the surroundings of biological research institutes, falling off as one moves further away.
Other species can then be "calibrated" on the basis of these cosmopolitan indicator species and the results of comparative physical and chemical measurements of a few important parameters. More or less complete lists exist of the indicator species used in Central and Eastern Europe, e.g. in (63), (67), (69), (90), (91) and (144). The calibrations referred to above must be repeated in Europe at regular intervals. The necessity for this is illustrated by the green algae, the saprobic index for which has increased by about 0.3 0.5 levels during the course of the last 30 years (145).
Evaluation of water quality on the basis of unicellular organisms alone represents in itself a limitation to subsets of the overall population of a given ecosystem, and information obtained from a single protistological biological analysis only has validity for a limited period of time. But there are good reasons for the increased utilization of single celled organisms for monitoring purposes. Many authors have devoted attention to this aspect (22, 23, 43, 146-149). LIEBMANN (150) gives the following explanation: "The sensitivity with which an organism reacts to the chemical composition of the water increases proportionally to its degree of organizational simplicity and smallness, i.e. if it has less volume and more cell surface, and if its surface is relatively unprotected from chemical influences acting upon it from the surrounding medium." These prerequisites are best met by the protozoa.
Since the volume of water carried by flowing waters can vary considerably, especially in the warmer regions of the earth, it is definitely necessary to carry out multiple biological analysis of the same aquatic system so that seasonal fluctuations can be taken into account. For evaluation of standing waters, the same difficulties exist that are currently interfering with the search for a general solution in the Federal Republic of Germany, in addition to other problems. The thermal stratification of deeper waters in the tropics typically remains constant on a long term basis. Complete circulation with turnover or exchanges of water between the top and bottom layers can thus rarely, if at all, be observed in a great many lakes. On the other hand, bodies of water exist which are characterized by daily alteration of a stagnation phase with stable stratification and a turnover phase. Examples of this phenomenon can be found in Java (151, 152), India ( 153), South America ( 154),
and Africa (155, 156). Examples of nutrient-poor water bodies which appear to be eutrophic because of certain environmental influences are also known in Europe (Lake Shkodër, 157). Additional studies are needed here, e.g. to supplement the LAWA program, in order to permit approximate evaluation of the condition of such lakes.
The lack of knowledge about indicator species in developing countries is due in large measure to the fact that there is very little suitable literature on classification containing saprobiological or trophobiological data. A few promising beginnings have been made here, among others by BICK (68), who has published a classification key for frequently occurring, predominantly ubiquitous ciliates, complete with saprobiological data.
<section>3.2 Evaluation of water quality with the aid of biomonitors</section>
3.2.1 General aspects
3.2.2 Utilization of biomonitors in brackish and marine water
3.2.3 Utilization of biomonitors in fresh-water bodies
So-called biomonitors or monitor species can also be used to yield qualitative and quantitative information on contaminants. BICK (179) distinguishes between two types of monitor species, namely on the one hand reactive monitors (158, 159) which provide information on the type and concentration of a given water pollutant, and on the other hand cumulative monitors, i.e. species that store and sometimes concentrate organic pollutants, heavy metals, and the like in their bodies (cf. also 15, 17). In the following, attention will focus on the latter type.
3.2.1 General aspects
The observed decline in populations of certain species of birds and mammals at the end of food chains or food webs cannot be completely explained by changes in their habitats or direct interventions. Attempts to identify the real causes have revealed the presence of toxic substances in the form of organic compounds such as DDT (cf. 2) or anorganic substances, like heavy metals. Severe poisoning of human beings has also occurred along with the characteristic symptoms, e.g. mercury and cadmium poisoning in Japan caused by eating marine animals (the Minamata and Itai-ltai diseases). A few years ago, the discovery that maternal milk exhibits concentrations of organochlorines 30 times those found in cow's milk made the headlines in the Federal Republic of Germany.
Residue analyses were increasingly performed, but at the same time efforts to develop an "early warning system" were intensified. In a number of different countries systems involving biomonitors were developed and tested. One of the focuses was on the search for suitable organisms, since migratory hawks - to take an example - are of no use for monitoring the pollution of fresh-water bodies and seas (160). They have little to find there in the way of prey. Neither are predatory birds, some of which derive their sustenance primarily from fish, suited for monitoring a given body of water or portions thereof, since as a rule they have a much larger radius of activity. Such species can be used for evaluation of pollution phenomena within larger areas, however, e.g. the silver lake eagle (Haliaetus vocifer) in Africa.
What requirements are made of a biomonitor? For marine environments, the requirements which biomonitors must fulfill have been repeatedly summarized (15, 161-165). These also apply to fresh-water bodies (166):
The organism should:
1. Be able to accumulate pollutants to as great an extent as possible (167) whilst itself being largely tolerant.
2. Be sedentary or at least exhibit a high degree of site loyalty.
3. Be representative of the collection site and be permanently available in sufficient numbers.
4. Be sufficiently long-lived in order to offer adequate variety in terms of size and age.
5. Possess sufficiently large organs that can be easily removed and provide enough material for studies.
6. Be easy to collect and preserve.
7. Tolerate brackish water.
8. Show a straightforward correlation between its pollutant content and the level in the surrounding medium.
9. Exhibit this correlation at all sites and under all external conditions.
10. Occur throughout the world, or at least have close relatives that satisfy requirements 1 -9
Not a single organism has yet fulfilled all of the points of this checklist. In other words, compromises are essential. For marine environments, so far only relatively few groups of organisms have been examined in the search for suitable species, and the situation is no better for freshwater systems. Aquatic plants can assimilate and sometimes store pollutants occurring in their environment, and animals can also ingest toxic substances along with their food, possibly enriching them and thus reflecting the pollution of their environment. The pollutants which cause concern here are not only anorganic and organic substances that enter the water as a result of anthropogenic influences, but also viruses, bacteria (168) and natural toxins. Quantification of pollutants by means of biomonitors can provide usable information on the suitability of organisms as food, as well as on the occurrence of ecotoxicologically relevant pollutant concentrations in organisms. Without reliable
correlations between pollutant concentrations in organisms on the one hand and the environment on the other, the contamination of a given body of water can only be qualitatively described.
3.2.2 Utilization of biomonitors in brackish and marine water
A large body of literature already exists on studies of pollution with the aid of biomonitors (cf. 240). In the following I will concentrate on those dealing with a specific animal species, namely the common mussel Mytilus edulis, as well as closely related species such as Mytilus galloprovincialis, M. californianus, and M. viridis. These mussels need a relatively large number of the conditions listed above, and are therefore used as monitor species in many parts of the world, especially along the coasts of the United States, within the context of the "Mussel Watch Concept" (169).
Depending on the kind of information that it is wished to obtain from such studies, the investigation program must be more or less extensive. For trend analyses over a period of many years that take into account seasonal differences and other factors the following rules should be observed:
1. Various mussel sizes should be studied to permit correlation of data with them; this can then possibly serve as the basis for agreement on a standard size.
2. Mussels should be collected at several characteristic times during the course of a year. The animals are then kept alive for two days to allow them to empty their digestive tract.
3. Parallel to collection of the mussels, abiotic factors are measured at the collection sites (salinity, temperature, depth at which animals are collected, sediment type and particle size distribution, turbidity, food availability).
4. Comparative analyses should be performed of biochemical parameters such as protein, lipid and carbohydrate contents.
5. In addition to entire animals, individual organs should be studied that are not involved in the reproductive or food reserve systems, such as kidneys, byssus glands, gills and possibly the mesenteric gland.
For identification of heavily polluted areas, the program can be limited to points I and 3, for example. In many early studies, the abovementioned program was not carried out. As a result, the results could frequently not be compared with one another. Why was this?
As stated above, Mytilus species are relatively well-suited as biomonitors for pollutants, including heavy metals, organic compounds and radionuclides. Mussels are relatively tolerant of pollutants. They are sessile organisms that form large beds in which individuals of different ages and sizes occur together. The individual organs can be easily extirpated. They primarily inhabit the tidal zone. As a result, they are easy to collect in sufficient quantities. Moreover, they are euryhaline, i.e. they tolerate a large salinity range. Mussels use their gills both for respiration and for filtering the water to extract nourishment from it. They thus possess two paths by means of which pollutants can enter their bodies:
1. The gill is an organ with a large surface area and very thin walls of tissue separating the water from the blood, and a high blood circulation rate. Consequently, pollutants can pass into a mussel's blood by diffusion relatively quickly, within just a few hours. Heavy metals, for example, accumulate in the lymph and their concentration can reach more than ten times that of the external medium ( 170).
2. By means of filter feeding, mussels collect fine particulate matter and pass it to their gastrointestinal tract. Here, pollutants can be passed to the bloodstream by means of digestion, and later enriched in certain organs. Biomagnification can occur here (167).
For many metals, it has been demonstrated that their assimilation rate from the water into the mussel body proceeds in a linear relationship to their concentrations in the external medium (171). The rate at which they are absorbed is dependent on the form in which they occur, e.g. in the case of metals on the ionic radius and on whether or not the ions are hydrated. The extent to which enrichment ultimately occurs also varies for different pollutants. At this point attention should be drawn to the fact that pollutant accumulation only takes place if the substance in question is available in a form that can be utilized by the organism.
In general, pollutant accumulation can be described and calculated with the aid of the following formula ( 172)
ca = A · (1 - e-lta)
where A = (hypothetical) concentration, l = coefficient of accumulation, ta = onset of accumulation. Formulas have also been published for calculating the biological halflives of accumulated pollutants (172-174). For the most part, however, they only apply to models involving a single contaminant type. Moreover, it is assumed that the contaminant is not subject to any breakdown and does not form any compounds in the host's body which could impose restraints on its capacity for remobilization.
Toxins exist which are quickly assimilated and concentrated but then released again, for example perchloroethylene. Conversely, many substances are characterized by very slow assimilation and elimination rates, e.g. heavy metals. In the case of lead, for instance, it is estimated that when the concentration in the surrounding medium changes more than one year is needed for the internal concentration to reach a new equilibrium (171). The integrating and smoothing effect of monitor species is based on kinetic properties of this sort (170). There is thus no indication of short-term changes.
Enrichment is also largely governed by the type and chemical structure of the toxin, as well as by other abiotic and inherent biotic factors influencing the biomonitor, as is illustrated by the following:
Lead and zinc uptake is not influenced by temperature (161). Cadmium uptake is reduced at low temperatures. Anorganic mercury and methyl mercury are absorbed more quickly at higher temperatures, but are also eliminated faster (175). SCHULZE-BALDES (170) offers the following explanation: temperature exerts a different influence on metals than on physiological functions of an indicator organism. The diffusion processes, e.g. via the gills into the bloodstream and vice versa, proceed independently of temperature. By contrast, active uptake and metabolism are affected by changes in temperature.
Salinity also has an impact on pollutant uptake, etc. (170, 176-179). The intensity of biomagnification, i. e. pollutant uptake via food ingestion, can also greatly depend on the degree to which an animal's food is contaminated, as well as on food availability (180).
Apparently, the size, weight and age of monitor organisms also have a major influence on contaminant concentrations; seasonal variations in weight, for example, must therefore be taken into account (181-184). The usual practice of listing concentrations per gram of live or dry weight without any additional information can lead to misinterpretations, as is illustrated by the fact that young mussels exhibit high metal concentrations which then decrease with advancing age; in very old mussels, the concentrations rise again. The varying metabolic processes and rates in mussels of different ages are probably responsible for this. On the other hand, the percentages of overall weight accounted for by the individual organs also shift. Gonads are relatively poor in metals. As they mature and grow in size, therefore, the concentration of pollutants per gram of body weight diminishes (171). BOYDEN (185) has therefore proposed, in order to get around this weight dependency, that metal
concentrations be converted to refer to a "standard" animal with a shell length of 50 mm and 1 g of live weight. Other factors have also interfered with the reliability of data as well; as already explained, not every metal provokes the same reaction, and different monitor organisms also respond differently.
The examples discussed so far make it quite clear why comprehensive study programs are necessary in order to obtain details and comparable data: the results can depend not only on the monitor species used, but also on the type and possibly the chemical structure of the pollutant or pollutants and on various abiotic and biotic environmental parameters.
I would now like to mention a few interesting applications of biomonitors. Direct chemical analysis is often insufficient to detect contaminants present in the water in very low concentrations. After being enriched in a biomonitor, the reliability of such analysis is greater, especially when the concentration rate is high. KRUGER (166) therefore regards fish as being suitable biomonitors. The explanation given is that fish possess a long-term collection function, so that in spite of excretion and metabolization even years later they faithfully reflect the pollution situation within a defined area. As an example, he cites studies of fish in the North Atlantic that, in contrast to those taken from near the mouths of the larger German rivers, did not exhibit "any significant pollutant concentrations" (166).
In Spain, the "mussel watch concept" has been applied to analyzing pollutant concentrations in mussels and the chemical attributes of these substances (186). The observed patterns of steranes and pentacyclic triterpenes differed greatly from the waste products emitted by a nearby oil platform. It was therefore deduced that these substances could not be derived from domestic oil production. The PCB concentration was quite high, reflecting the continued use of these substances in Spain. In addition, increased concentrations of organic chlorine compounds were measured, such as HCB, endrin and b-chlordane, as well as extremely high concentrations of metabolites of DDT (o,p-DDD).
Figure 12: Decreasing lead concentration levels in common mussels (Mytilus edulis) in the Weser estuary (from 192).
In Japan (187), cobalt-60 contamination from nuclear power plants was detected with the aid of mussels used as monitor organisms, and in California it has been possible to identify deep water flowing into certain coastal zones as being the source of plutonium (Pu-238, Pu-239 and Pu-240) concentration in mussels ( 188). Plants can also be used for pollution analysis. In Limfjord (Denmark) heavy metal accumulations were studied with eel grass (Zostera marina), and a clear correlation between bioaccumulation rates and the distance from a pollutant source (and thus the corresponding pollutant concentrations in the environment as well) was established (189). The results achieved were subsequently also confirmed by studies of Mytilus edulis (190). Similar findings have been made in southern Australia (191). Rooted aquatic plants that remain fixed at the same location for long periods of time also faithful! reflect pollution levels (cf. 3.1 .5).
Figures 12 and 13 show two informative examples in cartographic form related to lead pollution.
Biomonitors are not only employed in Europe and the United States; this method has also already been used in a number of threshold countries, including Yugoslavia and Turkey. In addition to Myrilus edulis and closely related species, other biomonitors are used, some of them plants and some of them animal species. Pollutant enrichment directly from the water and via food ingestion has been investigated. Biomagnification studies have been conducted with sediment feeders like Macoma baltica, detritus feeders such as Eudistylia vancouveri, grazers like Patella coerulea and Littorina spp., ciliates and fish. The investigated pollutants have included organic compounds, heavy metals and radioisotopes ( 194-232).
3.2.3 Utilization of biomonitors in fresh-water bodies
Monitor species can also be found for freshwater bodies that reflect pollutant levels. Fresh-water monitoring species must fulfill the same requirements as were listed above for marine organisms, since parameters also play an important role here as well (233). In Europe the suitable mussel species include Dreissena polymorpha which has spread beyond its original habitat and now occurs in most of the European faunal zones. Sphaerium corneum also fulfills all of the requirements, with the added advantage of occurring naturally almost everywhere in Europe. A few fish species have also been shown to be suitable ( 166), including fatty fish such as eels (Anguilla anguilla) and lean fish like bream (Abramis brama) both of which have been used for pollutant monitoring in northern Germany. Here, it is advantageous to focus on certain organs, for example, reliable information on mercury accumulation can be obtained by analyzing muscle and liver tissue, for cadmium by analyzing the
kidney and (to a lesser extent) the liver, and for organochlorines by analyzing muscle tissue. For studies of heavy metal pollution in fresh-water bodies, fish are apparently where muscle tissue is concerned - not always optimally suited as monitors (234), since they exhibit lower concentrations of toxins compared with lower animals. Contamination of the muscle tissue of fish is only significant in heavily polluted waters.
In the water, uptake of heavy metals together with food, i.e. biomagnification, apparently plays a less important role (234). Contaminant absorption by ingestion of food, especially in the case of highly toxic substances such as methyl mercury, can nevertheless occasionally take on major importance (172). At least in slightly to moderately polluted waters, direct absorption from the water predominates. For lotic organisms, it has been possible to establish relative values for bioaccumulation rates of different heavy metals: Cu >> Hg > Pb > Cd. Studies conducted thus far have revealed that periphyton, in other words microorganisms, are best suited for diagnosis of pollution levels. However, "the results should not be interpreted to mean that when no biological amplification by the organisms of food chains occurs in fresh waters the pollution of our biosphere and our inland waters with environmental toxins is less dangerous than previously thought, and that the dangers posed
by them have been exaggerated in the past. The individual absorption capacities and bioaccumulation rates are apparently more than sufficient to yield the observed high pollutant accumulations in the terrestrial terminal links of aquatic food chains. On the contrary: studies of the sublethal effects below LD50 (= acutely toxic) concentrations have clearly shown that even the lowest pollutant concentrations in our environment can have little-appreciated or previously unknown consequences" (235). The abiotic and biotic parameters listed for sea water are also relevant for fresh-water bodies.
Underwater plants are cited as being preferable to lake-bottom fauna (zoobenthos), since they exhibit more prominent assimilation capabilities (234). On the basis of extensive data on the average intensity of bioconcentration of environmentally relevant metals, an evaluation approach has been applied which is suitable for detection of chronic pollution and delimitation of portions of water bodies that are contaminated with metals, as well as for follow-up monitoring of the affected zones. Figure 14 shows the relative value of various empirical indicators for studying heavy metal concentrations, in the form of a spiral; the value of the listed indicator organisms increases as one moves outwards from the center (234).
Thistakes us beck to LIEBMANN's(150) statement that an organism reacts more sensitively to the chemical composition of the surrounding water, the more simply it is organized and the smaller it is, i.e. the less volume and the more surface area it possesses, and the more unprotected its surfaces are against chemical influences from the surrounding medium.
<section>4. Water evaluation by remote sensing</section>
Certain biological phenomena that are directly or indirectly due to water pollution, and changes in them, can be studied in their entirety without detailed analysis of species and biocoenoses. As is illustrated by documentation of the continuing expansion of the Sahara by means of aerial and satellite photography, this approach can also be used for observation of water contamination in larger systems. Surveillance of marine waters has been carried out in Europe and North America to detect contamination with used oil let off by ships (236). The spread and movement of oil slicks caused by tanker accidents are also observed from the air and documented. "Less harmful" contamination of waters with readily decomposable organic substances or plant nutrients can also be observed and photographed from the air. Analysis of the photographic evidence can then reveal much about the intensity of contamination and, if the observations are repeated, any changes undergone by it. Such
analytical methods are suitable for both marine and large inland waters. The best spectral range for detecting differences in vegetation is in the near infrared (700-850 nary). Difficulties are encountered by this method, whether observations are made from the air space, when there is a high atmospheric moisture content, since the mentioned wavelengths are absorbed by water vapor, thus disguising differences between vegetation types and densities. This phenomenon increases in intensity with distance.
The multispectral scanning (MSS) method can be used for surveying both vegetation and water resources. From Landsat satellites, which were originally designated as Earth Resources Technology Satellites (ERTS), infrared photographs can be made in which each raster dot corresponds to an area of approx. 60 x 80 m. Photographs made in various different infrared bands are stored on tape, and can later be separately played back in 64 steps or bands between total reflection and total absorption. One channel is then used to, for example, clearly distinguish a lake from its surroundings and to depict its outline. The other channels can be used for classification of water quality, depending on color composition, ranging from oligotrophic (= low plant nutrient levels and phytoplankton population) to eutrophic (= high nutrient levels and dense phytoplankton population). An example is shown in Figure 17 in (237). Photographic techniques of this kind can also be used for identifying the
sources of water pollution (238, 241).
For studying and depicting the morphology of water bodies that are not excessively deep, e.g. estuaries and coastal waters, radar can be used. This also allows water levels with varying degrees of turbidity to be distinguished. Due to its high contrast, this method is also well-suited for surveying catchment areas and mapping the morphology of river basin, borders between saltwater and fresh-water areas in coastal zones, former river tributaries, etc. (239, 241).
<section>5. Summary: Use of bioindicators and biomonitors in developing countries</section>
For biological evaluation of water quality and the condition of water bodies, aquatic organisms offer a number of advantages over other approaches.
Bioindicators - as defined by ELLENBERG (14) - are as a rule used within a biocoenosis for detection and identification of contaminants and contamination levels. Evaluatory procedures based on the saprobic system of KOLKWITZ and MARSSON (22, 23) and later investigators are primarily used for classification of pollution with readily decomposable organic substances, such as those which occur in domestic sewage. Here the fact is taken advantage of that organisms place certain demands on abiotic and biotic attributes of their environment, and react to changes in them. The more stenobiontic an organism is, the narrower the range of environmental conditions which it tolerates, the higher is its value for indication of certain environmental factors and/or combinations thereof. In evaluatory methods based on the saprobic system, the starting point is not individual species, but entire biological communities or biocoenoses. There are only a few aquatic indicator species that point to
specific pollutants or pollutant concentrations. Indicators are known for hydrogen sulfide, iron, manganese and sodium chloride (19). During the course of their evolution, a few species have been able to adapt to some "natural" contaminants. For adaptation to anthropogenic pollutants, e.g. organochlorines, the available time has been too short compared with the geological times spans in which evolution has occurred. Nonetheless, anthropogenic contaminants like those mentioned or others that are released into the environment in greater quantities than before, like heavy metals, can also be detected with the aid of living plants and/or animals and, within certain limits, quantified. Use is made of the ability of certain organisms to assimilate and enrich toxins, which are then analyzed in the body of the concentrating organism. The species used for this are referred to as monitor species or biomonitors (15, 17).
Not all organisms are suited as bioindicators or biomonitors for biological water evaluation. They must satisfy certain conditions. For example, eurypotent species are not suited as indicator organisms, since they thrive in a broad range of variable environmental factors. In addition, animal species that undertake long-range migrations, of which only a few individuals occur in a given habitat, or which move back and forth among several habitats are as a rule less suited as indicators or monitors. Analyses of residues in fishes, especially predatory fish, or in fisheating mammals and birds can nevertheless provide information on the contamination of food chains that culminate in human beings.
Biological techniques for water evaluation, i.e. bioindicators and biomonitors, have provided certain prerequisites are met (cf. 3.1.3 and 2.1) - a number of advantages over physico-chemical analyses, for example. The latter only tell us about conditions at the time that samples were taken, while the former, depending on the generation time of the indicator organisms, reflect environmental conditions over a more or less lengthy period of time. The advantages of larger organisms include a longer generation time and thus more time in which to integrate environmental conditions. Conversely, the smaller and less well protected an organism is, the more susceptible it is to environmental pollution.
It is a good idea to corroborate and back up the results of biological evaluation by taking a certain number of samples for monitoring of physico-chemical parameters. As a rule, biocoenotic evaluations of water quality and the condition of water bodies do not require complex or expensive technology. With the aid of biomonitors, concentrations of pollutants can be analyzed in organisms that in the surrounding water itself occur in such low concentrations that they can no longer be detected by analytical means.
The following applications exist for bioindicators and biomonitors:
1. Evaluation of the pollution situation of flowing waters, principally as regards readily decomposable organic substances.
2. Within certain limits and taking into account their unique characteristics, evaluation of standing waters as well.
3. Assessment of saprobic and trophic levels.
4. Qualitative and quantitative evaluation of the contamination of habitats and food webs with substances that decompose slowly or not at all, primarily of anthropogenic origin.
5. Evaluation of the temporal and spatial trends of such contamination.
6. Identification of pollutant sources.
A certain amount of analytical work and technological inputs are unavoidable. In the case of biomonitors, it is absolutely essential. For physico-chemical and biological methods of evaluating water quality and/or water body condition, experienced staff is necessary. SLADECEK's statement (63) can thus be turned around: Only good work of trained people gives a good service for science and its practical application, generally spoken.
For direct application of bioindicators - and biomonitors as well - in developing countries, a number of initial problems will have to be solved if these wish or are expected to use these procedures on their own.
I have already mentioned the urgent need to train suitable personnel. I regard it to be more useful for training to be performed by experienced scientists and practitioners in the developing countries. The reason is that, apart from the personal difficulties which can be associated with undergoing training in the industrialized nations, learning under field conditions in the developing countries themselves has the advantage that the teachers are in general able, because of their greater experience, to react more quickly to new problem situations than trainees. This leads us to the next problem.
Only the "cosmopolitans" among the indicator species can be initially used on a feasible
basis for biocoenotic evaluations, and - at least in some cases - their suitability must nevertheless first be investigated. More highly developed indicator species must be sought in different regions and "calibrated". This also applies to biomonitors, since our fresh-water monitor species Dreissena polymorpha, for example, only occurs within a limited area.
The required expenditures for equipment and the training of experienced personnel in connection with the use of biomonitors are relatively high. The basic prerequisites for use of such techniques are not always met in developing countries. The industrialized nations are thus called upon to provide intensive aid here. Until this has been implemented, biomonitors could be utilized more efficiently by means of a division of labor: taking of samples according to plan in the developing country, followed by laboratory analysis in an industrialized nation.
Bioindicators and biomonitors are basically suited for evaluation of water quality and the situation of water bodies and changes of these in developing countries as well, in order to detect and/or prevent existing or expected contamination and the associated risks, above all for the human population, in good time.
<section>References</section>
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64 ILLIES, J. and SCHMITZ, W., 1980. "Die Verfahren der biologischen Beurtei1ung des Gütezustandes der Fließgewässer (Systematisch-kritische Ubersicht)." Studien zum Gewasserschutz No. 5. Karlsruhe: Landesanstalt fur Umweltschutz Baden-Württemberg.
65 ELSTER, H.-J., 1966. "Uber die limnologischen Grund1agen der bio1ogischen Gewässerbeurteilung in Mitteleuropa.,, Verh. Internat. Verein Limnol. 16:759-785.
66 ELSTER, H.-J., 1982. , Zur Definition der 'Gewasser-' bzw. ,Wassergüte, und über die limnologischen Grundlagen ihrer Beurteilung in Vergangenheit und Zukunft.,, In: AURAND, K. and LESCHER, R. (eds.): "Limnologische Beurteilungsgrundlagen der Wassergüte und aktuelle Fragen der Wasserwirtschaft und des Umweltschutzes - Kolkwitz-Symposium 1981 ."Schriftenreihe Verein Wasser-, Boden-, Lufthygiene 54: 21 -37.
67 BICK, H. and KUNZE, S., 1971. "Eine Zusammenstellung von autökologischen und saprobiologischen Befunden an Sußwasserciliaten." Int. Rev. ges. Hydrobiologie 56: 21 -37.
68 BICK, H., 1972. Ciliated Protozoa. An illustrated guide to the species used as biological indicators in freshwater biology. Geneva: WHO.
69 SLADECEK, V., 1976. Bestimmung des Saprobienindexes. Praha/Minist. Forst- und Wasserwirtschaft (in Czech.).
70 ELSTER, H.-J., 1962. "Seentypen, Fliegewässertypen und Saprobiensystem." Int. Rev. ges. Hydrobiol. 47: 211-1218.
71 DITTMAR, H., 1959. "Reicht das bisherige Saprobiensystem für die Gütebeurteilung eines Gewässers aus?" Forsch. u. Beratung, Reihe A, 8: 263-265.
72 SLADECEK, V., 1964. "Biologie der Brauchwasseralgen." Wiss. Z. Univ. Leipzig 13. 45-51.
73 LANDESAMT FUR WASSER UND ABFALL NORDRHEIN-WESTFALEN (ed.), 1982. Fließgewasser. Richtliniefür die Ermittlung der Gewassergüteklasse. Düsseldorf.
74 BUCK, H., 1976. "Determination of water quality by coupling analysis." In: WOODWISS, F.S. (ed.): Biological water assessment methods. Technical Seminar (Commission of the European Communities), Nottingham.
75 BUCK, H., 1986. "Vergleichende Gewassergütebeurteilung mit Hilfe der Kopplungsanalyse unter Verwendung statistischer Parameter.,, In: BAYERISCHE LANDESANSTALT FUR WASSERFORSCHUNG (ed.): "Bewertuna der Gewässerqualität und Gewässergüteanforderungen." Münchener Beitrage zur Abwasser-, Fischerei- und Flußbiologie,, Vol. 40: 117- 134.
76 KNOPP, H., 1968. "Stoffwechseldynamische Untersuchungsverfahren für die biologische Wasseranalyse." Int. Rev. ges. Hydrobiol. 53: 409-44l1
77 ILLIES, J., 1978. Limnofauna Europaea. 2nd Ed. Stuttgart: Fischer.
78 SCHLICHTING, H.E., 1969. "The importance of airborne algae and protozoa." J. Air. Poll. Contr. Assoc. 19: 946-951.
79 RATHMAYER, W., 1975. Zoologie heute. Stuttgart: Fischer.
80 ODUM. H.T., 1956. "Primary production in flowing waters." Limnol. Oceanogr. 1: 102-117.
81 ODUM, E.P.. 1959. Fundamentals of ecology. Philadelphia/London: Saunders.
82 CASPERS, H. and KARBE, L., 1966a. "Trophie und Saprobität als stoffwechseldynamischer Komplex. Gesichtspunkte für die Definition der Saprobitätsstufen." Arch . Hydrobiol. 61: 453-470.
83 CASPERS, H. and KARBE, L., 1967. "Vorschläge für eine saprobiologische Typisierung der Gewässer." Int. Rev. ges. Hydrobiol. 52: 145-162.
84 CASPERS, H. and KARBE, L., 1966b. "Proposals for a saprobiological classification of waters." WHO/EBL/66.80: 1-28. Geneva.
85 SLADECEK, V., 1969. "The indicator value or some free-moving ciliates." Arch. Protistenk. 111 : 276-278.
86 TUMPLING, W.v., 1968. "Suggested classification of water quality based on biological characteristics." Fourth Int. Conf Water Poll. Research, Prague 1, 16: 1-8.
87 FACHGRUPPE WASSERCHEMIE IN DER GESELLSCHAFT DEUTSCHER CHEMIKER (ed.), 1971. Deutsche Einheitsverfahren. Methoden der biologisch-okologischen Gewasseruntersuchung. Gruppe M: Fließende Gewasser. Weinheim: Verlag Chemie.
88 SLADECKOVA, A., 1962. "Limnological investigation methods for the periphyton ("Aufwuchs") community." Bot. Rev. 28: 286-350.
89 BRETTHAUER, R. and TREUERSCH, M. (in press). Neuentwickelte Expositionsgestelle fur Periphytonuntersuchungen.
90 BREITIG, G. and TUMPLING, W.v., 1982. Ausgewahlte Methoden der Wasseruntersuchung, Vol. 2. Jena: VEB Fischer.
91 DEUTSCHER VERBAND FUR WASSERWIRTSCHAFT UND KULTURBAU (DVKW), 1980. Verschlusselung biologisc her Taxa. Hamburg: Parey.
92 KNOPP, H., 1955. "Grundsatzliches zur Frage biologischer Vorfluteruntersuchungen, erlautert an einem Gutelangsschnitt des Mains." Arch. Hydrobiol. 22: 363-368.
93 HOSTED, F., 1957. "Die Diatomeenflora des Flußsystems der Weser im Gebiet der Hansestadt Bremen." Abh. naturuw. Ver. Bremen 34: 181-440.
94 ZIEMANN, H.,. 1971. "Die Wirkung des Salzgehaltes auf die Diatomeenflora als Grundlage fur eine biologische Analyse und Klassifikation der Binnengewasser.' Limnologica (Berlin) 8: 505-525.
95 CASPERS, H., 1959. "Vorschlage einer Brackwassemomenklatur ('The Venice System')." Int. Rev. yes. Hydrobiol. 44: 313-315.
96 ELLENBERG, H., sen., 1979. "Zeigerwerte der Gefaßpflanzen Mitteleuropas." 2nd Ed. Scripta geobotanica. Gottingen: Goltze.
97 KOTHE, P., 1962. "Der 'Artenfehlbetrag', ein einfaches Gutekriterium und seine Anwendung bei biologischen Vorfluteruntersuchungen." Dt. Gewasserkundl. Mitt. 6: 60-65.
98 THIENEMANN, A., 1920. "Die Grundlagen der Biozonotik und Monard's faunistische Prinzipien." Festschrift Zschokke. Basel.
99 STEHFEST, H., 1973. Modelltheoretische Untersuchungen zur Selbstreinigung von Fließgewassern. Karlsruhe: Gesellschaft fur Kernforschung.
100 BUNDESMINISTERIUM FUR FORSCHUNG UND TECHNOLOGIE (ed.), 1977. Biologischer Sauerstoffumsatz im Neckar. Bonn: Federal Ministry for Research and Technology.
101 HOFFMANN, W.M., 1977. Prognostisches Modell Neckar. Biologischer Sauerstoffumsatz im Neckar. Bonn: Federal Ministry for Research and Technology.
102 BOES, M.; CEMBROWIESZ, R.G.; HAHN, H.H.; RUF, J.; SCHREINER, H. and WERNER, R., 1977. Prognostisches Modell Neckar. Mathematische Modelle zur Simulation und Optimierung in der Wassergutewirtschaft. Bonn: Federal Ministry for Research and Technology.
103 BACKHAUS, D.; BAUER, L.; BESCH, W.; HERKORN, U. and PINTER, 1., 1977. Prognostisches Modell Neckar. Untersuchungsergebnisse zur Gewassergute. Bonn: Federal Ministry for Research and Technology.
104 MULLER, ST. and DUSCHL, M., 1985. "Die Gewassergutesimulation als Planungsinstrument, dargestellt am Beispiel der wasserwirtschaftlichen Rahmenuntersuchung Donau und Main." Bayer. Landesamt fur Umweltschutz, Schriftenreihe No. 65. Oldenburg, Munich.
105 WORLD HEALTH ORGANIZATION (ed.), 1958. International Standards of Drinking Water. Geneva.
106 GABRIEL, J.,1946. "Principy biologicheho hodnoceni vody." Cas. Lek. Ces. 85: 1425-1431.
107 HORASAWA, I., 1956. "A preliminary report on the biological index of water pollution." Zoo/. Mag. (Tokyo) 54: 1.
108 CASPERS, H. and SCHULZ, H., 1960. "Studier zur Wertung der Saprobiensysteme. Erfahrungen an einem Stadtkanal Hamburgs." Int. Rev. yes. Hydrobiol. 45: 535-565.
109 CASPERS, H. and SCHULZ, H., 1962. "Weitere Unterlagen zur Prufung des Saprobiensystems." Int. Rev. ges. Hydrobiol. 47: 100-117.
110 SLADECEK, V. (ed.), 1977. "Symposium on Saprobiology." Arch. Hydrobiol., Suppl., Ergebn. Limnol. 9: 1-245.
111 LANDERARBEITSGEMEINSCHAFT WASSER (LAWA), 1980. Die Gewassergutekarte der Bundesrepublik Deutschland. Esslingen: Bechtle-Druck.
112 SLADECKOVA, A. and SLADECEK, V., 1963. "Periphyton as indicator of the reservoir water quality. I. True periphyton." Sci. Pap. Inst. Chem. Techn., Praha, Technol. Water 7: 507-561.
113 KRAMER, B., 19X7. Personal communication, University of Regensburg.
114 BICK, H.; KRISHNAMOORTHI. K.P. and LAKSHMINARAYANA, J.S.S., 1967. "Preliminaiy findings concerning the potentialities of the European saprobity system for monitoring water quality under tropical conditions in India.,, WHO/EP/67.6: 1 -51 .
115 NANDAN, S.N. and PATEL, R.J., 1984. "Saprobity systems for the assessment of river water quality by algal community.', Indian Bat. Rep. 3: 1 29-132.
116 RAI, H., 1962. 'Hydrobiology of River Yumana at Okhla (Delhi. India)." Sci. Pap. Inst. Chem. Techn., Prague, Technol. Water 6: 77-98.
(Entries 117 - 143)
DISTRIBUTION OF EUROPEAN UNICELLULAR SPECIES IN THE TROPICS (an alphabetical listing of relevant literature):
117 ACLETO, C., 1966. "Algae de ague dulce de las cascades de Barranco. "Publ. Mus. Hist. Nat. Javier Prado (Lima), ser. B, 21 : 1 -65.
118 ACLETO, C., 1910. "Algae de valle de Camana." Rev. Progr. Oceanografica y Pesceria (Univ. de Villaria, Lima) 1 : 7-22.
119 BEEBE, W., 1925. ,'Studies of a tropical jungle; one quarter of a square mile of jungle at Kartabo, British Guyana.(VI,Fauna, l.Protozoa)." Zoologica (New York) 6: 1-193.
120 BICUDO, C.E.M. and BICUDO, R.M.T., 1970. Algas de aguas continentais brasileiras. Universidade de Sao Paulo.
121 BORROR, A.C., 1977. "Ciliophora.,, In: HURLBERT, S.H. (ed.): Biota acuatica de Sudamerica austral. San Diego State Univ., San Diego, California, pp. 55-56.
122 BOVEE, E.C., 1957. "Protozoa of Amazonian and Andean waters of Colombia, South America.,,J. Protozool. 4: 63-66.
123 COMPERE, P., 1980. "Argues de l'Air (Niger).,, Bull. Jard. bot. nat. Belg. 51 : 3-40.
124 COMPERE, P., 1984. ,'Some algae from the Red Sea Hills in north-eastem Sudan." Hydrabiologia 1 10: 61-77.
125 ELSTER, H.J. and VOLLENWEIDER, R., 1961. "Beiträge zur Limnologie Ägyptens." Arch. Hydrobiol. 57: 241343 .
126 GREEN, J.; EL MOGHRABY, A.J. and ALI, O.M.M., 1984. "A faunistic reconnaissance of Lakes Kundi and Keilak, Western Sudan."Hydrobiologia I 10: 33-44.
127 GRIFFITH, C.. 1977. "Zoomastigina." In: HURLBERT, S.H. (ed.): Biota acuarica de Sudamerica austral. San Diego State Univ., San Diego, California, pp. 44-47.
128 HECKY, R.E.; KLING, H.J. and RUDD, J.W., 1978. "Studies on the planktonic ecology of Lake Tanganyika." Can. Fish. Mar. Serv,. Tech. Rep. 816.
129 HECKY, R.E. and KLING, H.J., 1981. "The phytoplankton and protozooplankton of the euphobic zone of Lake Tanganyika: Species composition, biomass, chlorophyll content, and spatio-temporal distribution." Limnol. Oceanogr. 26: 548-564.
130 ILTIS, A., 1980. "Les argues." In: DURAND, J.R. and LEVEQUE. C. (eds.): Flore et faune aquatiques de l'Afrique sahelo-soudanienne. Vol. l: 9-61. Paris: Office Rech. Sci. Tech. Outre-Mer.
131 LAKSHMINARAYANA, J.S.S., 1 965. "Studies on the phytoplankton of the River Ganges, Veranasi, India." Hydrobiologia 25: 119-137. 138-164.
132 LEWIS, W.M., l978. "A compositional, phytogeographical, and elementary structural analysis of the phytoplankton in a tropical lake: Lake Lanao, Philippines." J. Ecol. 66: 849-880.
133 MOSS, B., 1979. "Algae in Lake Chilwa and the waters of its catchment area.,' In: KALK, M.; McLACHLAN, A.J. and HOWARD-WILLIAMS, L. (eds.): Lake Chilwa, Studies of changes in a tropical ecosystem. The Hague: Junk.
134 PANKOW, H., 1979. "Algae from Sudan." Willdenovia 8: 485-491.
135 PAYNE, A.I. , 1986. The ecology of tropical al lakes and rivers. New York: John Wiley & Sons.
136 SINADA, F. and ABDEL KARIM, A.G., 1984. "A quantitative study of the phytoplankton in the Blue and White Niles at Khartoum.,, Hydrobiologia 110: 45-46.
137 STARMACH, K., 1975. "A1gae in the Gebel Marra Mts. in West Sudan." Acta Hydrobiol. 17: 211-221.
138 THOMASSON, K., 1971. "Amazonian algae." Mem. Inst. Roy. Sci. Nat. Belgique, ser. 2, 86: 1-57.
139 UHERKOVICH, G., 1981. "Algen aus einigen Gewässern Amazoniens." Amazoniana 7: 191-219.
140 UHERKOVICH, G., 1984. "Phytoplankton." In: SIOLI, H. (ed.): The Amazon. The Hague: Junk.
141 YACUBSON, S., 1969. "Algae de ambientes acuaticos continentales, nuevas pare Venezuela (Cynophyta, Chlorophyta).,, Bot. Centro Invest. Biol. Univ. Zulia 3: 1-87.
142 ZAFAR, A.R., 1984. "Seasonality of phytoplankton in the South Indian lakes." Verh. Internat. Verein. Limnol. 22: 11-73.
143 ZUTSHI, D.P. and WANGANEO, A., 1984. "The phytoplankton and primary productivity of a high altitude subtropica1 lake." Verh. Internat. Verein. Limnol. 22: 1168-1172.
(End of list)
144 MAUCH, E., 1976. Leitformen der Saprobitat für die biologische Gewasseranalyse. Frankfurt: Courier Forschungsinstitut Senckenberg 21 .
145 SLADECEK, V., 1982. "Kenntnisstand und aktuelle Probleme bei der Beurteilung der Wassergüte mittels Bioindikatoren." Decheniana, Suppl. 26: 99-104.
146 LAUTERBORN, R., 1914-17. Die sapropelische Lebewelt. Ein Beitrag zur Biologie des Faulschlammes natürlicher Gewasser. Verh. Naturhist. Med. Verein. Heidelberg 13.
147 WETZEL, A., 1952/53. Aktuelle Aufgaben der biologischen Wasseranalyse. Z. Karl-Marx-Univ. Leipzig 7/8.
148 PATRIK, R.; HOHN, M.H. and WALLACE, I.H., 1954. A new method for determining the pattern of the diatom flora. Notulae Natural Acad. Sci. Phila. No. 259.
149 BICK, H., 1957. "Beiträge zur Okologie einiger Ciliaten des Saprobiensystems.,, Vom Wasser 24: 224-246.
150 LIEBMANN, H., 1947. Die Notwendigkeit der Revision des Saprobiensystems und deren Bedeutung für die Wasserbeurteilung. Gesundheitsingenieur 68.
151 RUTTNER, F., 1930. "Hydrographische und hydrochemische Beobachtungen auf Java, Sumatra und Bali.', Arch. Hydrobiol., Suppl. 8: 197-454.
152 VAAS, K.F. and SACHLAN, M., 1955. "Limnological studies on diurnal fluctuations in shallow ponds in Indonesia.,, Verh. Internat. Verein. Limnol. 12: 309-319.
153 PRUTHI, H.S., 1933. "Studies on the bionomics of fresh-waters in India. I. Seasonal changes in the physical and chemical conditions of the tank in the Indian Museum compound.,, Int. Revs yes. Hydrobiol. 28: 46-47.
154 POWELL, TH.; KIRKICH, M.H.; NEALE, P.J. and RICHARDSON, P.J., 1984. "The diurnal cycle of stratification in Lake Titicaca: Eddy diffusion.,, Verh. Internat. Verein Limnol. 22: 1237-1243.
155 WORTHINGTON, E.B.. 1930. "Observations on the temperature, hydrogen-ion concentration, and other physical conditions of-the Victoria and Albert Nyanzas." Int. Rev. ges. Hydrobiol. 24: 328-357.
156 TAILING, J.F., 1957. "Diurna1 changes of stratification and photosynthesis in some tropical African waters.,, Proc. Royal Soc.. B, 147: 57-83.
157 NEDELKOVIC, R., 1959. Skadarsko jezero. Biol. Inst. Beograd.
158 ARNDT, U. and SCHWEIZER. B., 1987. Bioindikatoren und ihr Einsatz zur Uberwachung in tropischen und subtropischen Landern. Here: Contr. No. 4.
159 STEUBING, L.; BIERMANN, J. and DEBUS, R., 1987. Bioindikatoren für Luftschadstoffe im asiatischen Raum. Here: Contr. No. 5.
160 BIBELRIETHER, H., BIRNBACHER, D.; BUCHWALD, K.; ORCHOWY, G. and PREISlNG, E., 1984. "Schutzgebiete und Schutzobjekte.,, In: BICK, H.; HANSMEYER, K.H.; OLSCHOWY, G. and SCHMOOCK, P. (eds.): Angewandte Okologie. Mensch und Umwelt. Vol. 2. Stuttgart: Fischer, pp. 282-312.
161 PHILLIPS, D.J.H., 1976a. "The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead, and copper. 1. Effects of environmental variables on uptake of metals." Mar. Biol. 38: 59-70.
162 PHILLIPS, D.J.H., 1976b. "The common musseI Mytilus edulis as an indicator of pollution by zinc, cadmium, lead, and copper. II. Relationship of metals in mussel to those discharged by industry.', Mar. Biol. 38: 71 -80.
163 PHILLIPS, D.J.H., 1977a. "The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environments." Environ. Pollut. I 3: 281 -317.
164 CUNNINGHAM, P.A., 1979. "The use of bivalve molluscs in heavy metal pollution research." In: VERNBERG, W.B.; CALABRESE, A.; THURBERG, F.P. and VERNBERG, F.J. (eds.): Marine pollution: Functional responges. New York: Academic Press, pp. 183-221.
165 NATIONAL ACADEMY OF SCIENCE, 1980. The international mussel watch. Washington D.C.: Office of Publications, Nat. Acad. Sci.
166 KRUEGER, K.E., 1985. "Fish as bioindicator for pollution of the environment with harmful substances." Arch. Lebensmittelhyg. 36: 130- 131 .
167 ELSTER, H.-J., 1987a. "Definitionen. 7-8." In: LILLELUND, K.; DE HAAR, U.; ELSTER, H.-J.; KARBE, L., SCHWOERBEL, J. and SIMONIS, W. (eds.): Bioakkamulation in Nahrungsketten. Zur Problematik der Akkumulation von Umweltchemikalien in aquatischen Svstemen Ergebnisse aus dem Schwerpunktprogramm "Nahrungskettenprobleme". Bonn: Deutsche Forschungsgemeinschaft (DFG).
168 AL-MOSSAWI, M.J., KADRI, M.: SALEM, A.A. and CHUGH, T.D., 1983. "The use of clams as bioindicator of fecal pollution in seawater." Water Air Soil Pollut. 20: 257-264.
169 GOLDBERG, E.D.: BOWEN, V.T., FARRINGTON, J.W.; HARVEY, G.: MARTIN, J.H.; PARKER, P.L.; RISEBROUGH, R.W.; ROBERTSON, W.; SCHNEIDER, E. and GAMBLE, E., 1978. "The mussel watch." Environ. Conserv. 5: 101-125.
170 SCHULZE-BALDES, M., 19X2. "Tiere als Monitoren für Schwermetalle im Meer. Ein Uberblick." Decheniana, Suppl. 26: 43-54.
17 1 SCHULZE-BALDES, M., 1974. "Lead uptake from seawater and food, and lead loss in the common mussel Mytilus edulis." Mar. Biol. 25 : 117- 193.
172 KARBE, L., 1987. "Kinetik der Akkumulation und Dekontamination von Schwermetallen." In: LILLELUND, K.; DE HAAR, U.; ELSTER, H.-J.; KARBE, L.; SCHWOERBEL, J. and SIMONIS, W. (eds.): Bioakkumulation in Nahnungsketten. Zun. Prohlematik der Akkumulation von Umweltchemicalien in aquatischen Systemen. Ergebnrisse aus dem Schwerpunktprogramm ,,Nahrungskettenprobleme." Bonn: Deutsche Forschungsgemeinschaft (DFG), pp. 75-88.
173 MORIARTY, E., 1975. "Exposure and residues.,, In: Organochlorine Insecticides: Persistent Organic. Pollutants. London: Academic Press, pp. 29-72.
174 ERNST, W., 1982. "Tiere als Monitororganismen fur organische Schadstoffe." Decheniana, Suppl. 26: 55-66.
175 FOWLER, S.W.; HEYRAUD, M. and LA ROSA, J., 1978. "Factors affecting methyl and inorganic mercury dynamics in mussel and shrimp.', Mon.. Biol. 46: 267-276.
176 PHILLIPS, D.J.H., l977b. "Effects of salinity on the net uptake of zinc by the common mussel Mytilus edulis." Man.. Biol. 41: 79-88.
177 PHILLIPS, D.J.H., 1977c. "The common mussel Mytilus edulis as an indicator of trace metals in Scandinavian waters. 1. Zinc and cadmium." Mar. Biol. 43: 283-291 .
178 PHILLIPS, D.J.H., 1978. "The common mussel Mytilus edulis as an indicator of trace metals in Scandinavian waters. II. Lead, iron, and manganese." Mar. Biol. 46: 147- l 56.
179 JAKIM, E.; MORRISON, C. and STEDE, R., 1977. "Effects of environmental factors on radiocadmium uptake by four species of marine bivalves." Mar. Biol. 40: 303-308.
180 KARBE, L.; BIAS. R. and BORCHARDT, T., 1987. "Aufnahmekinetik und Anreicherung von Blei und Cadmium in Muscheln und Fischen." In: LILLELUND, K.: DE HAAR, U.; ELSTER, H.-J.; KARBE, L.; SCHWOERBEL, J. and SIMONIS, W. (eds.): Bioakkumulation in Nahrungsketten. Zur Problematik der Akkumulation von Umweltchemikulien in aquatischen Systemen. Ergebnisse aus dem Schwerpunktprogramm "Nahrungskettenprnbleme". Bonn: Deutsche Forschungsgemeinschaft (DFG), pp. 219-225.
181 BRYAN, G.W., 1973. "The occurrences and seasonal variation of trace metals in the scallops Pecten maximus (L.) and Clamys opercularis (L.)." J. mar. trio. Ass. U.K. 53: 145-166.
182 COSSA, D.; BOURGET, E.: POULIOT, D.; PIUZE, J. and CHANUT, J.P., 1980. "Geographica1 and seasonal variation in the relationship between trace metal content and bodyweight in Mytilus edulis." Mar. Biol. 58: 7-14.
183 FOWLER, S.W. and OREGIONI. B., 1976. "Trace metals in mussels from N.W. Mediterranean." Mar. Pollut. Bull. 7: 26-29.
184 FRAZIER, J.M., 1975. "The dynamics of metals in the American oyster Crassostrea virginica. I. Seasonal effects."Chesapeak.eSci. 16: 162-171.
185 BOYDEN, C.R., 1977."Effects of size upon meta1 content of shell fish." J. mar. biol. Ass. U.K. 57: 675-714.
186 RISEBROUGH, R.W.; DE LAPPE, B.W.; WALKER, W.I.I.; SIMONEIT, B.R.T.; GRIMALT, J.; ALBAIGES, J.; REGUEIRO, G.J.A.; NOLLA, B.A. and FERNANDEZ, M.M., 1983. "Application of the mussel watch concept in studies of the distribution of hydrocarbons in the coastal zone of the Ebro delta, Spain." Mar. Pollut. Bull. 14: 181-187.
187 MOMOSHIMA, N.; SHIKI, A.; TAKASHIMA, V.; MAKI, T.; KORIYAMA, M.; SHIMOZONE, S.; INAMURA, H. and NAKAMATA, K., 1985. ,'Radioactive and stable cobalt concentrations in mussel in Kyushu Island, Japan.,, Radioisotopes 34: 257-261.
188 GOLDBERG, E.D.: KOIDE, M.; HODGE, V.; FLEGAL, A.R. and MARTIN, J., 1983. " mussel watch 1977-1978. Result on trace metals and radionuclides." Estuarian Coastal Shelf Sci. 16: 69-94.
189 BRIX, H.; LYNGBY, J.E. and SCHIERUP, H.H., 1983. "Eelgrass Zostera marina as an indicator organism of trace metals in the Limfjord Denmark. Mar. Environ. Res. 8: 165-182.
190 RIISGARD, H.U., 1984. "Mercury pollution in the waters around Harboore-Tange and Limfjord Denmark." Mar. Pollut. Bull. 15: 129-133.
191 WARD, T.W.: CORRELL, R.L. and ANDERSON, R.S., 1986. "Distribution of cadmium, lead, and zinc among the marine sediments, sea grasses, and fauna, and the selection of sentinal accumulators near a lead smelter in South Australia." Aust. J. Man.. Freshwater Res. 37: 567-586.
192 SCHULZE-BALDES, M., 1973. "Die Miesmuschel Mytilus edulis als Indikator fur die Bleikonzentration im Westästuar und in der Deutschen Bucht." Mar. Biol. 2 1 : 98- 1 02.
193 POHAM, J.D.; JOHNSON, D.C. and D'AURIA, J.M., 1980. "Mussel (Mytilus edulis) as 'point source' indicators of trace metal pollution. ,' Mar. Pollut. Bull. 11 : 261 -263.
(Entries 194-232)
AQUATIC ORGANISMS AS BIOMONITORS FOR DETECTION OF POLLUTANTS, IN PARTICULAR HEAVY METALS (an alphahetical listing of relevant literature)
194 AGADI, V.V.; BOSHLE, N.B. and UNTAWALE, A.G., 1978. "Metal concentration in some seaweeds of Goa ( India)." Botanica Marina 21 : 247-250.
195 ARGAWAL, H.C.; MITTAL, P.K.; MENON, K.B. and PILLAI, M.K.K., 1986. "DDT residues in the river Jumana in Delhi, India." Water Soil Air Pollut. 28: 89- 104.
196 AL-DABABS, M.A.M.; HUBBARD, F.H. and McMANUS, J., 1984. "The shell of Mytilus as an indicator of zonal variations of wafer qualify within an estuary."Esruarine Coastal Shelf Sc.i. 18: 263-270.
197 AMIARD-TRIQUET, C.; BERTHET, B.; METAYER, C. and AMIARD, J.C., 1986. "Contribution to the exotoxicological study of cadmium, copper, and zinc in the mussel Mytilus edulis. II. Experimental Study." Mar. Biol. 92: 7-14.
198 BADAWY, M.I. and EL-DIB, M.A., 1984. "Residues of organochlorine pesticides in fish from the Egyptian delta lakes." Environ. Int. 10: 3-8.
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214 KOEHLER, A.; HARMS, U. and LUCKAS, B., 1986. "Accumulation of organochlorines and mercury in flounder. An approach to pollution assessment." Helgol. Meeresunters. 40. 431-440.
215 KUIPER, J., 1986. "Monitoring fate and effects of oil in the marine environment." Environ. Monit. Assess. 7. 221-232.
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218 MIKAC, N. and PICER, M., 1985. "Mercury distribution in a polluted marine area. Concentrations of methyl mercury in the sediments and some marine organisms." Sci. total Environ. 43: 27-40.
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<section>The Use of Bioindicators for Environmental Monitoring in Tropical and Subtropical Countries</section>
by Uwe Arndt and Birgit Schweizer
<section>1. Introduction</section>
In the industrial countries of the earth, during the last 15 years the importance attached to having a healthy environment has steadily grown. In the Federal Republic of Germany it is currently one of the three most-discussed topics, on a par with means of reducing unemployment and topped only by issues related to maintaining world peace (SCHUTZE, 1982). Although this public attention is not synonymous with concrete measures to protect the environment, it is nevertheless clear that broad sectors of the population have become sensitive to this matter, even resulting in changes in existing political parties and the emergence of new ones in our country. Political decisions have been made in favor of environmental protection, and in spite of the fact that many people believe these measure are inadequate, it is nevertheless true that they have placed greater priority on ecological goals than on economic needs. Apparently, the time was ripe for a reconciliation of economy with
ecology.
The situation is significantly different in the developing countries, which are still struggling to become industrialized. The ongoing shift of industrial production facilities from Europe and the United States to countries of the Third World are confronting these with a new complex of problems: that of environmental pollution. With a view to alleviating their serious economic and social problems, however, many Third World countries portray their lax or completely absent anti-pollution legislation and regulations as an advantage, hoping to attract foreign industry. As a result, multinational chemical companies establish subsidiaries in the Third World in order to get around the stringent checks and controls in many industrial countries (GLOBAL 2000, 1980). Not enough environmental awareness of the right kind has been able to develop, and cannot be realistically expected to develop as long as excessively fast rates of population growth are forcing developing countries to
practice destructive exploitation of natural resources (PECCEI, 1981). Experience has shown, however, that unless appropriate laws are passed and enforced, the densely settled metropolitan areas preferred by heavy industry will inevitably be subjected to alarmingly high concentrations of pollutants. The outlook is worsened even further by the fact that the industrial countries have always exported goods to tropical and subtropical countries exclusively with an aim to increasing their own economic gain, and have consequently failed to provide the required infrastructure and know-how for dealing with the resulting environmental problems. In the light of this fact, it becomes understandable why the developing countries are repeating the same mistakes which we have already made with the environment. The threat to the ecology posed by anthropogenic activities is much more serious in tropical and subtropical regions, however, since, for example, the vegetation reacts much more
unfavorably to atmospheric pollution than in Central Europe. The claim is occasionally made that the geographical and meteorological conditions in tropical regions exclude any possibility of atmospheric pollution reaching a harmful level (PETERSEN, 1966; NG'ANG'A, 1980). But studies of air quality in the vicinity of large South American cities (SANHUEZA et al., 1982) have documented that even when wind conditions are predominantly favorable, a high rate of atmospheric pollution is attained as soon as the emission rates exceed the ability of the atmosphere to disperse the pollutants.
Any concept aimed at helping to remedy the situation must establish priorities and begin with collection, review and evaluation of existing publications. The present study is devoted to this purpose. It concentrates on biological monitoring methods suited for demonstrating the effects of toxins, in particular environmental pollutants, on the plants of terrestrial ecosystems. In Chapter 2, a number of key concepts are defined and a general survey of the possibilities and limitations of biological monitoring is given (cf. ARNDT, 1983). This is followed by presentation of a selection of approaches which have been successfully applied in Central Europe, including a discussion of their technical details and aspects related to their practical application. Then a survey is given of the known relevant studies which have been conducted in the tropics and subtropics, and the usefulness of their results for routine environmental monitoring discussed. The study concludes with
recommendations for continued action.
<section>2. Definitions and basic principles of biological monitoring</section>
One of the most fundamental attributes of living organisms, including human beings, animals and plants, is their ability to respond to external stimuli, i.e. these stimuli activate processes which normally help organisms to survive (MERIUS, 1955). Such a stimulus can, for example, be present in the form of pollutants in the environment, and provoke corresponding responses in living organisms. This peculiarity of living organisms can be utilized as a criterion or indicator for determining the presence of pollutants in the environment (SCHONBECK et al., 1970). When organisms are used as bioindicators for environmental monitoring purposes, however, they take on the role of instruments (RAVERA, 1975). In other words, only those biological responses need be evaluated that are caused by substances in the environment, with pollutant accumulations in excess of normal levels also being defined as effects in this sense (VDI-Richtlinie L 2329, 1983).
Bioindicators can thus be defined as organisms or communities of organisms that respond to environmental pollution by changing their vital functions or by accumulating toxins (ARNDT et al., 1987). In contrast to SCHUBERT (1985), this definition purposefully excludes indication of natural site conditions while at the same time improving on an earlier definition formulated by ARNDT et al. (1982).
The many proposals and new developments in the field of biological monitoring have also given rise to numerous designations for the methods and approaches which have developed in connection with different lines of pursuit and practical applications. The scheme illustrated in Figure I is discussed below.
In keeping with the definition cited above, two basic kinds of biological indicators exist: response indicators and accumulative indicators. Both types occur with all three possible kinds of utilization of indicator organisms.
Pointer organisms are defined here as biological indicators or communities of indicators that can provide information on conditions in an ecosystem (cf. Fig. 1). In the simplest of cases they can provide data on a certain pH value or on heavy metal concentrations in the soil. Certain plant species respond to changes in the environment, such as the appearance of pollutants, by dying out or multiplying. In other words, the size and species composition of plant and animal communities change. Quite frequently, mapping and observation of vegetation is better suited than monitoring of fauna, since plants have environmental requirements that are easier to assess, remain in one place and are more numerous (RAT VON SACHVERSTANDIGEN FUR UMWELTFRAGEN, 1978). It is generally impossible to quantify data obtained from pointer organisms or to draw reliable conclusions on pollutant levels. In order to identify changes in ecosystems, long-term and repeated collection of data from pointer
organisms is necessary. Such long-term studies lead to the compilation of comprehensive environmental inventories like those proposed by MULLER (1978), which can yield information on the extent of anthropogenic influences.
Test organisms are used primarily in toxicological laboratory tests and for water analysis. They are generally highly standardized and are often used chiefly to detect immediate risks for human beings. Accordingly, animals are often also used for this purpose (BESCH, 1977). Although the results of such tests cannot always be directly transferred to actual ecosystems (cf. Fig. 1), during recent years they have played an increasingly important role in connection with testing of environmental chemicals, for example pesticides, and environmental toxicology (SCHAFER, 1983). Test organisms such as algae, bacteria and higher animals generally yield quantifiable data (RIPPEN, 1984). Test organisms are also used for monitoring and control of air pollution. This means that polluted air samples and/or pollutants must be brought to the laboratory and their phytotoxicity tested there. The cress test developed by GARBER (1974) is used more frequently. In this test, the rate of germination
and/or the growth of sprouts and roots are studied under the influence of pollutants. A proposal which involves studying the effect on algae of particulates which settle out of the air must also be assigned to this category (ARNDT, 1974).
Monitor organisms, finally, include all those living organisms which are used for qualitative and quantitative monitoring of pollutant levels in the environment and their repercussions on the ecology. Response and accumulative indicators can be more clearly distinguished here than is the case with pointer or test organisms; both kinds can either already be present in an ecosystem (passive monitoring) or be introduced to it in standardized form (active monitoring). In both cases, the observed injury and/or chemical analyses performed permit more or less accurate conclusions to be drawn on the quantitative levels of specific pollutants, once appropriate benchmarks have been established.
The terminology used here for different types of indicators must necessarily remain somewhat vague in certain borderline applications. It is for this reason that Fig. I shows overlap zones between the pointer organisms and organisms used for passive monitoring on the one hand, and between test organisms and those used for active monitoring on the other hand. No clear distinctions are possible in either of these areas, and the extent to which pointer organisms for acid soil environments (ELLENBERG, 1982) lists a large number of such organisms for dry, moderately moist and wet soils) can be simultaneously used for passive monitoring of air pollution depends largely on the knowledge and objectives of the investigators.
Where monitoring of air pollution is concerned, the monitor organisms play the most important role of all biological indicators. They provide data on various different biological levels, depending on which attributes are suited for use as criteria in each individual case (STEUBING, 1982). The ways in which an organism responds to exposure to a pollutant can be observed or measured in biochemical or physiological terms (JAGER, 1982). If it is assumed that the appearance of visible injury to a plant must be preceded by metabolic changes, then this fact can be taken advantage of for early detection. Unfortunately, however, the existing techniques for doing this - developed for medical applications - are for the most part extremely complicated and have not yet been sufficiently adapted for use on plants.
Another proposed approach which is also quite involved and thus of only limited practical usefulness for air quality monitoring, is to utilize changes in subcellular structures as criteria. This approach calls for use of electron microscopy and the services of an appropriately trained specialist, so that although it has indeed permitted effects caused by pollution to be demonstrated, it cannot be regarded as a practical and easy-to-use instrument. The advantages and disadvantages of this and similar proposals are discussed by GODZIK (1982).
Optical methods such as those used for measuring the thicknesses of annual rings in trees are simpler to perform. To a certain extent, they can be used for reconstruction of events that represent long periods of past history. For instance, measurements of the annual rings of oak trees in the vicinity of an isolated pollutant source have been successfully used to reconstruct the history of pollution in that area without any other data being available on pollution levels (ARNDT and WEHRLE, 1982). Biological monitoring with annual ring thicknesses is also being used within the scope of studies of forest dieback in Europe (ECKSTEIN et al., 1983). Comparisons of healthy and diseased trees have shown not only that there has been a general decline in annual ring thicknesses, but also that there has been a high percentage of complete absence of annual rings in diseased trees (ATHARI and KRAMER, 1983). Measurements of annual diameter growth can also be used to determine the
effectiveness of forest fertilization (ARNDT and WEHRLE, 1982). It should be noted, however, that these studies only permit conclusions to be drawn on the causes of injury if the data on climate and tree age can be supplemented by data on pollution levels. Due to the relatively uniform site conditions in the tropics and subtropics, studies of growth zones in tree trunk cross sections are only feasible and meaningful there in special cases.
Biological monitoring approaches which are based on ecophysiological methods and make use of cellular and tissue-related criteria are also of interest for practical applications. This refers above all to measurement of plant respiration and other techniques that permit non-destructive assessment of the condition of plants. In spite of the fact that special equipment is also required in these cases, techniques exist that are acceptable in terms of cost and labor, especially considering that these parameters exhibit a high degree of sensitivity to environmental pollution (KELLER, 1978). Some of the metabolic processes frequently used for biological monitoring are summarized in Table I (WEIGEL and JAGER, 1985).
Quite a large number of plant species are now used for biological monitoring approaches in which visible symptoms of injury to certain organs and/or entire organisms serve as criteria. Most of the monitor plants routinely used today belong to this group. One reason for this is that they more or less meet various demands which are made of biological indicators:
1. They are easy to handle and care for.
2. They can be standardized.
3. The conditions under which they respond are well-known.
4. They are cost-effective.
5. The responses are easily evaluated.
6. The effects of pollution are obvious and quantifiable.
7. Genetic uniformity can be achieved.
8. The responses can be statistically evaluated.
It is not absolutely essential for a bioindicator to fulfill all of these conditions at the same time. Depending on the objectives, different attributes can gain and lose in importance, or additional requirements may be imposed for use within the scope of pollution response inventories.
The indication criteria dealt with so far have to do with biological aspects of individual organisms. They are thus of an auto-ecological nature, and the data they yield can be extrapolated to entire systems only within certain limits. The situation is different if passive monitoring is used, i.e. observation of naturally occurring plant species. Observation of entire phytocoenoses, i.e. investigation of the species makeup of plant communities and the changes which this undergoes under the influence of atmospheric pollution, opens up new possibilities for monitoring of the environment (KUTSCHERARITTER et al., 1982; SCHUBERT, 1982). In particular, the response of dominant species to pollutants provides a wealth of synecological information, since the injuries which they sustain then rapidly manifest themselves throughout the entire ecosystem (TRESHOW, 1968; ARNDT and WEHRLE, 1982).
Table 1: Physiological and biochemical response criteria for biomonitoring (WEIGEL and JAGER, 1985).
Procedure
Measured metabolic activity or parameter
Porometrics
- Transpiration
- Photosynthesis
Stomatal behavior
- Water budget
- Pollutant uptake
Gas exchange measurement
- Photosynthesis
- Respiration
Chlorophyll fluorescence
- Photosynthesis
- Condition of pigment system
Electron microscopy
- Surface structure
- Scanning electron microscope
- Ultrastructure
- Transmission electron microscope
Chemical analysis
- Pollutant content
- Pollutant uptake
- Nutrient content
- Nutrient leaching
Mass spectroscopy of sulfur isotopes
- Sulfur uptake and accumulation
Biochemical methods
- Enzyme activity
(e.g. peroxidase, super oxide dismutase, gluta mate dehydrogenase, catalase)
- Pool values of metabolites
(e.g. amino acids, amines, sugars, lipids, proteins)
- Pigment content
(e.g. chlorophyll a/b)
- Buffer capacity
- Membrane integrity
(e.g. malonidialdebyde, ethane)
Formation of volatile substances
(e.g. H2S, ethylene, ethane)
- Allocation of primary products of photosynthesis
- Special photosynthetic reactions
(e.g. ATP formation, electron transport, Cal vin cycle)
It must therefore be stressed that system-related biological monitoring has yet to be extensively applied. Especially in the form of active monitoring, in other words the calculated exposure of a model ecosystem, it has not progressed beyond the experimental stage. This must nevertheless be regarded as a promising field of endeavor, since in such plant communities competition among individuals plays a role in addition to the direct effects of environmental pollutants. This can serve to intensify responses - the observed signals are amplified, a fact which could be used to particularly great advantage for long-term monitoring of chronic low pollution in areas that are in a natural or nearnatural state (DE WIT, 1982).
The concept of monitor organisms as used here does indeed go far beyond the definition normally cited for bioindicators, and it is necessary to distinguish between two different approaches or functions. On the one hand, monitor organisms can provide information on the causes of injury, i.e. permitting the disease to be diagnosed, in this case the impact of environmental pollutants. On the other hand, they can also be used for spatial and temporal quantification of pollutant levels; in this case bioindicators are integrated into an impact-related measurement process, becoming monitor organisms in the true sense of the term.
For monitoring purposes, procedures must be standardized as far as possible. Unfortunately, practical fulfillment of this requirement is not keeping pace with the numerous proposals being made for biological monitoring. However, since standardization is a prerequisite for routine use, e.g. for compilation of pollution response inventories, during recent years various proposals have been published. In particular, the Commission on Air Quality Control of the Association of German Engineers (VDI) has been actively making major contributions to standardization (SPIEGELBERG, 1984).
The goal of such efforts is to attain essential comparability of results and to increase their accuracy by reducing error margins. This is accomplished by means of careful definitions of methods, issued in the form of guidelines. The most well-known example is probably the standardized grass culture. This is an accumulative indicator which has been used for years for active monitoring both locally and regionally. It was originally developed by SCHOLL (1971, 1972) and the State Institute for Environmental Protection of North-Rhine/Westphalia (Landesanstalt fur Immissionsschutz Nordrhein-Westfalen). The Commission on Air Quality Control of the VDI published the approach in 1978 in its guideline no. 3792, sheets I and 2. This guideline refers explicitly to "measurement of effective dosages", thus identifying its orientation as that of a monitoring approach (VDI, 1982, 1985). All aspects of the method are defined and described in detail, ranging from the quality of the seed,
cultivation and means of ensuring an independent water supply to exposure and analysis of results; during the last 15 years, this method has been successfully tested and applied under a wide variety of conditions.
Active monitoring with lichens is standardized to a similar extent. The principles involved were first formulated by BRODO (1961), but it was SCHONBECK (1968, 1969) who introduced this technique to Central Europe and developed it to its present state of sophistication.
Further examples could be cited, but those mentioned so far are sufficient to show that some of the approaches will require a number of technical improvements before they can be successfully applied. One of the major prerequisites for routine use of plants as bioindicators was the invention of a means to automatically ensure a supply of water to the exposed plants, since otherwise the labor involved in watering the plants during sunny weather would have made large-scale monitoring grids unfeasible. The first usable techniques to be developed for this were publicized at about the same time as the standardized grass culture procedure, and these two aspects must also be regarded as being intimately linked (SCHOLL, 1969; v. HAUT et al., 1972). Since that time, a number of improvements on the original technique have been made which reduce the likelihood of problems and permit easier handling (ARNDT, 1983).
The current state of the art is the use of a standardized "bioindicator fan". This involves simultaneous exposure of a number of different bioindicator species, such as tobacco (Nicotiana tabacum, var. BEL W 3), broad bean (Vicia faba, var. Herra), common bean (Phaseolus vulgaris, var. Pinto, Blue Lake, Hilds Maja, etc.), red clover (Trifolium pratense, var. Hege) etc., the different responses of which provide additional information. The varying sensitivities of common bean varieties to different pollutants and ozone concentrations permit more accurate conclusions to be drawn on pollution levels (SCHLUTER, 1984). The "indicator fan" is exposed in special frames (cf. Fig. 2) that are designed and placed in such a way as to ensure standardized shade, water supply, orientation and height above the ground. They are now in use at over 100 monitoring sites in the state of Baden-Wuerttemberg (ARNDT and SCHLUTER, 1985: ARNDT et al., 1985; LfU, 1984).
The technologically most sophisticated devices for exposure of bioindicators are likely the mobile chambers developed by VAN HAUT (1972). These can be used for concurrent observation, at a single monitoring site, of control plants receiving only filtered air and plants exposed to contaminated air; this is accomplished by keeping the plants under plexiglass hoods. This arrangement has the advantage of permitting direct comparison, but for cost reasons can only be used in special instances (cf. Fig. 3).
Biological monitoring (German: Bioindikation), is defined as the measurement of changes in organisms and/or ecosystems induced by environmental influences of anthropogenic origin (cf. SCHUBERT, 1984). It takes its orientation from a "normal state" established by benchmarking, and is performed in a spatially and temporally differentiated manner using monitor organisms. It is important to note that it does not involve quantitative determination of stress factors such as pollutants present in the atmosphere, but instead response-oriented monitoring procedures that should not be regarded as a substitute for methods involving direct measurement of pollution levels (ARNDT, 1983). The use of such systems is favored by attributes which only they possess:
- Indication of responses; this obviates having to deduce effects, on the basis of a constructed model, from data collected from a grid of pollution monitoring sites, an approach which is possible in principle but associated with a significant degree of uncertainty.
- More or less integral indication of the effects of a given pollution type, at least in the case of response indicators; in other words, the "cross-sensitivity" that can occur in connection with analytical measurement techniques no longer interferes with accuracy, instead simply contributing to the overall effect.
- All external influences affecting the nature of the response are unified, even if the bioindicator has varying degrees of sensitivity both to different types of air pollution and other parameters as well.
- Bioindicators can also permit detection of chronic pollution levels by, for example, enrichment of pollutants until a sufficiently large quantity for measurement has accumulated, or by showing reduced growth.
- Since the goal of air quality control is to contain the effects of pollution, and monitoring of this can take its orientation from response threshold values, for this purpose only bioindicators can provide useful data.
On the other hand, the wish to correlate specific responses with given pollutant types has proven to be virtually unattainable. To be sure, bioindicators exist which are particularly sensitive to certain types of atmospheric pollution, but it is not now nor will it likely ever be possible to definitively prove that these responses are exclusively tied to certain triggers. This statement does not hold for accumulative indicators, in the case of which concentrations of individual substances can be determined by chemical analysis.
There are two basic approaches to biological monitoring. One is aimed at identifying the environmental impact of known pollutant sources, and the other is usthis would also serve to describe the usefulness of given bioindicators. However, this should not be taken as a reason to forgo practical applications, on the contrary, enough basic data can be collected in the course of routine operations for assessment of the criteria listed above, although it should always be kept in mind that the use of bioindicators does not involve analytical test procedures, but instead effect-related, "biological measurement approaches".
In one case passive monitoring was successfully applied in the surroundings of a brickworks to simultaneously achieve three of the major goals of such methods (ARNDT et al., 1984). Firstly, use of a standardized technique for assessment of damage to a wine-growing area comprising about 100 ha revealed the spatial distribution of the effects, and secondly, it was possible to unambiguously identify the source (Fig. 4). Thirdly, another survey following installation of a filter at the source showed that the area had recovered from the damage. Numerous other publications have reported on studies of this type using both response and accumulative indicators (KUNZE, 1972; WALLIN, 1976; KELLER, 1980). The use of bioindicators along linear sources is used for studying the effects of pollution emanating from roads (KELLER, 1970; LAGERWERFF and SPECHT, 1970; KLOKE, 1974; LAAKSOVIRTA et al., 1976) or the paths followed by aircraft taking off and landing at airports (RUGE and BURKHARDT,
In order to collect evidence against environmental polluters or in order to test the environmental compatibility of technical facilities, bioindicators are frequently used within the scope of active monitoring. This can take the form of, for example, placing standardized organisms in a tract of land on which the establishment of industrial plants is planned. The plants can be exposed either in a checkerboard pattern or placed along lines radiating from a single point, but in most cases they are arranged irregularly, i.e. following the slope of the land, any buildings present, etc. In many cases, response or cumulative measurements are continued until a normal state has been identified (benchmarking) and the influence of the technical measures or industrial facilities can be determined. This can sometimes make it necessary to maintain a monitoring grid for several years. In this context, the standardized grass culture developed by SCHOLL proved itself in practice in
connection with the establishment of aluminum smelters in the Ruhr between 1965 and 1975 (SCHOLL. 1971). In 1974, LITTLE and MARTIN (1974) exposed Sphagnum moss in bags made of fine nylon fiber in the vicinity of a zinc and lead smelter near Bristol (United Kingdom). With the aid of this technologically simple method, they were able to identify zones with different levels of heavy metal pollution in the area around the plant, and the usefulness of this procedure was reconfirmed a year later at another location (RATCLIFFE,1975).
The objectives pursued by large-scale use of bioindicators are as a rule somewhat different from those in the above-mentioned cases. The aim here is to obtain information on the condition of ecosystems, and it is logical to concentrate on passive monitoring. Of course, when establishing test grids covering entire regions or countries difficulties can arise in connection with comparison of the data obtained from various sites, since their climatic and edaphic conditions can vary widely.
Nevertheless, the taking of adequately standardized samples permits collection of an amount of information much greater than that obtainable with any other approach. During the past 2() years, a large number of monitoring grids of this kind have been successfully established in densely settled metropolitan areas. In particular, the lichen mapping projects in Freiburg (KUNZE, 1974), along the lower course of the Main River (STEUBING et al., 1974) and in the Munster area (HEIDT, 1978), as well as other, similar programs conducted on a trial basis (including that of SCHUSCHKE et al., 1974) have contributed to the assessment of air quality. Nonetheless, the reliability of data obtained from lichen mapping may be jeopardized if site factors are not given sufficient consideration (MULLER et al., 1981).
For active monitoring, during recent years the ozone-sensitive tobacco variety Bel W 3 has been increasingly used. One drawback is that it often exhibits a weaker response in city centers than in outlying districts, a phenomenon which is attributed to the ozone "expending itself" by reacting with primary air pollutants such as NO, as well as meteorological factors in urban landscapes (STEUBING, 1982; ARNDT and SCHLUTER, 1985; ARNDT et al., 1985; RUDOLPH, 1977; FLOOR and POSTHUMUS, 1977; HORSMAN, 1981; ARNDT et al., 1983).
Large-scale application of biological monitoring procedures has also made it possible to obtain an overview of the condition of forest ecosystems in the Federal Republic of Germany. For example, the State Institute for Ecology, Landscape Development and Forestry Planning of North-Rhine/Westphalia (Landesanstalt fur Okologie, Landschaftsentwicklung und Forstplanung Nordrhein-Westfalen) developed a highly standardized procedure for surveying the ecological situation of forests with respect to pollution (KNABE, 1981) based primarily on assessment and analysis of spruce trees and their needles. SCHROTER (1983) was able to develop an assessment procedure for Baden-Wuerttemberg based on pine and spruce trees, which has now been in use for over 5 years. Finally, all of the experience gained in connection with forest damage in the various parts of the Federal Republic of Germany (SCHOPFER and HRADETZKY, 1984a+b) have been collected in the form of uniform national guidelines, which
were then used for implementation of a corresponding inventory by all forestry operations in the Federal Republic of Germany (excluding West Berlin) in 1983. This inventory probably represents the most extensive application of a biological monitoring approach to date (BML, 1985).
The systematic use of bioindicators can be used as the basis for pollution re.sponse in`,entories. This involves the collection of data on injuries caused by air pollutants to organisms and materials across space and through time. Pollution response inventories are now one of the standard measures employed by the Lùnder of the Federal Republic of Germany for identification and assessment of polluted areas. Credit goes to the Land of North-Rhine/Westphalia and its State Institute for Pollution Control (Landesanstalt fur Immissionsschutz) in Essen for having introduced such surveys to air pollution control practice (PRINZ, 1974; DREYHAUPT et al., 1979). These activities provide additional information not contained in the frequently already existing source and pollution inventories, and are therefore not a substitute for these but instead a valuable supplement, providing the justification required by the Federal Pollution Control Law (Bundesimmissionsschutzgesetz) of 1984 for
implementation of concrete measures. This fact has probably also been responsible for the establishment of further such regional and statewide monitoring grids outside of North-Rhine/Westphalia (ARNDT et al., 1982; LfU, 1984; RIJKSINSTITUT, 1978; RUDOLPH, 1979).
In the Federal Republic of Germany, Article 47 of the Federal Pollution Control Law has a major bearing on the performance of pollution response inventories; this law outlines the determination of environmental damage caused by pollution following delineation of contaminated areas. In this way, important data for the necessary air pollution control plans are obtained.
The overall size of a biological monitoring grid and the density of the monitoring sites must respond to the demands placed on the expected results. If it is wished to clarify a local matter, such as identification and localization of a pollutant source, then a denser grid must be used than for monitoring programs spanning entire regions. Quite frequently, economic considerations play a role, but these must not be allowed to endanger the usefulness of the data. Various grid densities have been used for monitoring of polluted areas in North-Rhine/Westphalia, varying between 16 x 16 km and I x I km (PRINZ and SCHOLL, 1975, 1978). The statewide surveys carried out in Bavaria used a spacing of 16 x 16 km, and it has been proposed that this grid be directly extended to cover the neighboring state of Baden-Wuerttemberg as well (ARNDT et al., 1982; RUDOLPH, 1979).
If suitable monitoring procedures are combined, to a certain extent it is possible to use correlative comparisons of the various results to deduce the causes of the observed damage. This can be facilitated by a threestep approach.
In the first step, an accumulative bioindicator is used to identify the amount of individual pollutants absorbed. The second step involves use of response indicators in an active monitoring approach that demonstrate an integral effect. Finally, the naturally occurring plants in the vicinity of measuring sites are studied (passive monitoring). If the various results are then correlated with one another, it often emerges that the data yielded by different kinds of indicators reinforce one another. For example, there is a relatively close correspondence between the response of fluoride-sensitive gladiolus species and the effect which fluoride has on grass cultures, and appropriate statistical methods can be used to demonstrate a correlation with pollutant concentrations as well. In general, the results are depicted in the form of bar diagrams superimposed on maps, with connecting lines drawn between the measured levels without any measurement data to support these intermediate
values. The advantage of this approach is that overall patterns are easier to view (Fig.7).
For practical reasons, comparative methods involving computation of correlations and regression analyses for different biological monitoring systems can be combined in an effort to identify the causes and nature of air pollution and develop an impact-related air pollution control strategy. For this purpose, evaluation is carried out in the form of interpretation of an identification and documentation pattern on several levels:
1. If data are available from continuously measuring permanent stations or intermittent field measurements made with mobile equipment, then these are documented. The statistical parameters, such as mean annual values, etc. are compared with the corresponding pollution values of the German Technical Guidelines for Air Quality Control (TA Luft 1974) or the maximum permissible pollutant concentrations (MIK values) stipulated by VDI guideline no. 2310 (1986).
2. This pollution data can then be used to deduce the potential risk for plants posed by SO2 and NO2 as stipulated by VDI guideline no. 2310 sheets 2 and 5 (1986) and by ozone, the most important photochemical oxidant, based on the "proposal for maximum ozone concentrations for vegetation" advanced by GUDERIAN et al. ( 1983).
3. When interpreting the results, data from the various different approaches are first compared with one another. At the same time, the responses of the plants used as bioindicators are compared with direct measurements of air pollution in order to correlate pollution levels with effects and, if possible, to deduce dose/response relationships for the area under study.
Studies carried out with 20 bioindicator stations in the Stuttgart area to determine the environmental compatibility of a proposed industrial facility exhibited a high degree of correlation among the biological monitoring approaches used, for instance between the dry matter of standardized grass cultures, the fresh matter of radishes (r = 0.79+++) and the needle coats of spruce trees (r = -0.76+). A correlation between lead concentrations in grass cultures and benzo(a)pyrene concentrations in green cabbage (r = 0.83+++) indicated that both were derived from automobile exhaust. Finally, correlations were established between mortality rates measured with standardized exposure of lichens on the one hand and fluoride concentrations in elderberry leaves (r = 0.80++) and the results of lichen mapping (r = -0.76++) on the other hand.
These results show that additional knowledge can be gained from statistical analysis of parameters such as yields, enrichment and responses. If measurements of pollution levels and injury to plants are compared and correlated, even more can be found out. The causal relationships between pollution levels and effects depicted in Table 2 were revealed by the above-mentioned surveys.
Regression analysis can be applied to deduce dose/effect relationships for given areas. For instance, in the study area it was possible to correlate lichen mortality rates greater than 10% with the following pollutant concentrations, defined as arithmetic mean values: SO2 0.02 mg/m3; NO2 0.03 mg/m3; lead 0.05 mg/m3 · d; cadmium 0.7 mg/m3 d.
If it is wished to use plants as bioindicators on a routine basis and to utilize the data they yield for practical air pollution control measures, then similarly stringent standards must be applied to them as to physical and chemical analytical procedures. The following seven criteria are important (FRANKE, 1969; KAISER, 1973; STOCKER, 1977, 1981).
Table 2: Correlation coefficients between pollution types and their effects, based on studies in the Stuttgart area.
Pollution type
Response criterion
Correlation coefficient
Mean annual O3 concentration
Fresh weight of radishes
Leaf injury in tobacco plants
SO2 concentration
S content in grass cultures
Lichen mortality rate
Lichen mapping (occurrence)
Lead in deposited particulates
Lead in elderberry leaves
Mean annual NO2 concentration
Lichen mortality rate
Significance levels: +++, p = 0.1%; ++, p = 1%
1. Accuracy is defined as exact quantitative capture of actual symptoms of pollution injury. What is important is not necessarily high resolution of the "measurements", but rather the provision of precise information on the margins of error associated with this quantitative data capture. The degree of accuracy reflects the deviations between measured and actual values, in other words the system-related or methodological error inherent in a measurement or observation.
2. The precision of the data yielded by a measurement procedure is determined by the limits within which these can be regarded as reliable. These limits can be expressed either in measurement units or as a percentage, and they also take into account changing spatial, temporal and staff conditions (cf. FRANKE, 1969). The concept of precision is equivalent to that of replicability, which is expressed as a relative standard deviation.
3. The concept of specificity is often incorrectly applied. The specificity of an indicator is understood as being the response of an organism to a given pollutant. But it can also refer to a certain response of the organism which can be clearly differentiated from other changes. This requires that all changes caused by other air pollutants and stress factors be clearly distinguishable.
4. The sensitivity of a measuring instrument is defined by DIN 1319 as the ratio of the change in the value indicated by the instrument to the actual value of the variable being measured. Applied to bioindicators, this means that clearly distinguishable responses or response levels must be present in response to different pollution levels.
5. The validity range of biological monitoring results refers to their spatial and temporal transferability. In the case of plants, for example, it is limited to the extent that results are only applicable to the growing season. In the case of pointer organisms a given indication can only have validity if the organism used actually occurs or could potentially occur in the studied ecosystem.
6. Representation refers to the transferability of biological monitoring results obtained from one type of organism to other living organisms. So far only a limited number of bioindicator organisms are known that possess this desirable attribute. It is naturally necessary to carry out extensive comparative studies before statements can be made on representation.
7. The last criterion to be mentioned here for bioindicators is their importance. This must be regarded as being large if the organism plays an essential role for human beings (e.g. domestic animals) or for an ecosystem (dominant species), or if the indicator organism possesses a high degree of representation.
It should be stressed that the criteria listed above are still under discussion. It still remains for them to be formulated in exact physical and mathematical terms and thus for a precise description of the procedural parameters to be provided, although this would also serve to describe the usefulness of given bioindicators. However, this should not be taken as a reason to forgo practical applications, on the contrary, enough basic data can be collected in the course of routine operations for assessment of the criteria listed above, although it should always be kept in mind that the use of bioindicators does not involve analytical test procedures, but instead effect-related, "biological measurement approaches".
Table 3: Biomonitoring with aquatic plants (NOBEL et al., 1983).
Indicator type
Approach
Criterion
Example
Pointer organisms
Passive
Existence
Studies of vegetation and flora, mapping.
Response
Surveys of ecological site types and groups of species.
Assessment of injury to naturally occurring species.
Passive
Accumulation
Determination of concentrations in naturally occurring
species.
Monitor organisms
Accumulation
Transplanting. Determination of concentrations in
exposed individuals.
Active
Response
Transplanting. Assessment of injury to exposed indi
viduals.
Test organisms
Active
Response
Exposure experiments under laboratory or feld-like
(and accumulation)
conditions. Toxicity tests.
The nomenclature used here, the methods and their application to pollution response inventories all apply to the field of air pollution. They can also be easily applied to aquatic ecosystems, and - particularly during recent years - water-dwelling macrophytes have increasingly been used as bioindicators (KOHLER, 1982). These are used as pointer plants or even for passive monitoring. It is very positive that efforts are being made to use the same terminology for both aquatic and terrestrial bioindicators (NOBEL et al., 1983), cf. Table 3.
In the following chapters, a number of different biological monitoring procedures are described in accordance with the distinctions defined above; experimental approaches and methods which have already proven their usefulness in practice are both discussed.
<section>3. Bioindicators in tropical and subtropical countries</section>
In many instances, the use of bioindicators requires quite some technical equipment and a fair amount of specialized knowledge and experience. The latter qualities are still almost entirely lacking in the tropical and subtropical countries of the earth, so that very little is still known about the routine use of bioindicators there. Moreover, far too little is known about the responses of tropical and subtropical plants to pollutants. Such knowledge is an essential prerequisite for the use of response indicators, and the compilation of corresponding reference works is urgently needed. In the industrial countries there already exist such works that could serve as models; they represent invaluable practical guides (VAN HAUT and STRATMANN, 1970; JACOBSON and HILL, 1970; LACASSE and TRESHOW, 1976; MALHOTRA and BLAUEL, 1980).
In the following, a few selected publications are reported on which either provide direct information on biological monitoring in tropical and subtropical countries or deal with phenomena which could be utilized for this purpose. Attention is also paid to publications from the southern United States, since some of the procedures developed there could be transferred to the countries under discussion here.
<section>3.1 Pointer species and pointer communities</section>
As already mentioned, certain plant species respond to changes in their environment, such as the appearance of pollutants, by dying out or multiplying. In the vicinity of abandoned African copper mines it has been observed that in Cu-contaminated soils the natural forest savanna vegetation had been replaced by a sparse cover of metal-tolerant plant species (DREW and REILLY, 1972). Becium homblei can be regarded as an especially suited pointer organism, since within the study area near Lusaka, Zambia it occurs exclusively on soils with high copper concentrations. The results of analytical measurements showed a correlation between copper concentrations in the soil with the copper concentrations which had accumulated in the aerial parts of the plants. The same phenomenon was demonstrated with Phynchosia monophylla, also a flowering plant, although this species is less suited for use as a pointer organism since it is not widespread on copper-contaminated sites.
WOOD et al. (1976) studied changes in the natural vegetation in the surroundings of an abandoned copper smelter in the Sonoran Desert, Arizona. It emerged that the occurrence of certain wild annual plants (Plantago purshii, Cryptantha barbigera, Pectocarya recurvata, Bromus rubens, Erodium cicutarium, Eriasirum diffusum) was clearly correlated with the distance from the facility. Within a radius of 0.4 km these plant species had died out completely. The same applied to species of the genus Opuntia, with dead cactus skeletons providing evidence that they had previously grown within this zone. The species diversity, species density and coverage of all plant species occurring at the site were inversely proportional to the measured heavy metal concentrations in the soil.
WONG (1978) reports on studies of the natural vegetation in the area of an SO2 source in Hong Kong. Vegetation samples were taken along a transect, with changes in the species distribution at various distances from the source being recorded.
Table 4: Relative sensitivity of annual desert plants to O3 and SO2, based on studies performed in 1982 and 1983 on threshold concentrations and extent of injury at increasing concentrations of O3 and SO2 (from THOMPSON et al., 1984).
No.
Plant species
Sensitivitya
No.
Plant species
Sensitivitya
O3
SO2
O3
SO2
Baileya pleniradiata
III
II
Langloisia schott
II
II
Bromus rubens
II
II
Lepidium lasiocarpum
III
II
Camissonia californica
II
I
Lotus tomentellus
II
II
Camissonia claviformis
I
I
Lupinus concinnus
II
II
Camissonia hirtella
I
I
Malacothrix glabrata
I
II
Caulanthus cooperi
II
II
Mentzelia albicaulis
I
II
Chaenactis caphoclinia
II
II
Oenothera californicab
II
II
Chaenactis fremontti
II
II
Pectocarya heterocarpa
I
II
Chaenactis stevioides
II
II
Pectocarya platycarpa
I
II
Chorizanthe brevicornu
II
II
Perityle emoryi
III
II
Coreopsis bigelovii
II
II
Phacelia campanularia
II
II
Ctyptantha angustifolia
II
II
Phacelia crenulata
II
Cryptantha circumscissa
II
II
Plantago insularis
II
II
Cryptantha micrantha
II
II
Platystemon californica
II
II
Cryptantha nevadensis
I
I
Salvia columbariae
II
II
Cryptantha pterocarya
II
II
Schismus barbatus
II
Descurainia pinnata
II
II
Spaeralcea ambigua
III
II
Erastrum wilcoxii
II
II
Stephanomeria exigua
II
II
Erigonum pusillum
II
Streptanthella longirostris
II
II
Erodium cicutarium
II
II
Stylocline filaginea
II
II
Eschscholzia parishii
I
II
Thelypodium lasiophyllum
II
II
Eucrypta micrantha
II
II
Thysanocarpus curvipes
II
II
Festuca octoflora
III
III
Viguiera deltoideab
II
II
Gilia stellata
II
aSensitivity categories:
I threshold concentrations: approx. 0.1 ppm of O3 or 0.2 ppm of SO2 for 32-40 hours
II threshold concentrations at 0.2-0.3 ppm of O3 or 0.5-1.5 ppm of SO2
Ill little or no injury at 0.3 ppm of O3 or 1.5 ppm of SO2
bPerennial plants
<section>3.2 Response indicators</section>
THOMPSON et al. (1984) exposed various annual plant species from the Mojave Desert to ozone and sulfur dioxide in open-top chambers. The greatest sensitivity to both of these pollutants was exhibited by Camissonia claviformis and Camissonia hirtella, in which the leaf necroses typically caused by these two pollutants were observed at low concentrations. The results of this study are depicted in detail in Table 4.
Where the effects of combined exposure to SO2 and NO2 are concerned, various wild perennials from the Mojave Desert exhibited prominent differences (THOMPSON et al., 1980). While Larrea divaricata Cav., Chilopsis linearis Cav. and Ambrosia dumosa (Gray) Payne sustained extensive foliar injury, slowed growth and reduced dry weight, with combined exposure to both pollutants having an additive effect, Atriplex canescens (Pursh) Nutt. proved to be relatively resistant to these pollutants. All of the studied annual plant species showed a significantly greater sensitivity to SO2, with combined exposure having a potentiating effect. Extreme sensitivity was demonstrated by Erodium cicutarium (L.) L'Her and Plantago insularis, high sensitivity by phacelia crenulata Torr, and moderate sensitivity by Baileya pleniradiata. It must nevertheless be pointed out that these exposure trials were conducted with very high pollutant concentrations of up to 2 ppm of SO2 (5340 mg/m³) and I ppm of
NO2 ( 1910 mg/m³).
In addition to environmental pollution with photochemical oxidants and sulfur dioxide, pollution from fluoride emissions from brickworks and aluminum smelters is of major importance. PANDEY (1981) studied the effects of fluoride pollution on a tropical broad-leaved forest in the vicinity of an aluminum smelter in Mirzapur, India. The dominant tree species of this forest area include Shorea robusta, Terminalia tomentosa, Anogeissus latifolia, Acacia catechu, Buchanania lanzan and Diospyros melanoxylon. The understory is formed primarily by Holarrhena antidysenterica and Woodfordia fructicosa. Chlorotic and necrotic injury to foliar tissue were used as a basis for classifying the sensitivity of the ornamental and economically important plant species occurring at this site. The results are shown in Table 5. It emerged that the arboreous species were the first to be affected by pollution of the air with hydrogen fluoride, followed by shrubs and grasses, although it is unclear
whether these variations are due to differences in resistance or to differing degrees of exposure.
Reduced chlorophyll contents were found by PANDEY (1985) in the leaves of Terminalia tomentosa and Buchanania lanzan trees growing near a fluoride source. This pigment reduction, like foliar biomass, correlated negatively with the accumulated fluoride concentrations in the leaves.
LAL and AMBASHT (1981) observed a reduction in the overall chlorophyll contents of leaves of Diospyros melanoxylon - a broad-leaved tree species that plays an economically important role for production of aromatic Indian cigarettes - in the vicinity of a factory which emitted hydrogen fluoride. They also established that foliar biomass was 32% less and leaf size 27% less than the corresponding values for control trees in unpolluted areas.
The rapid development of fluoride-emitting industrial plants in Australia, in particular aluminum smelters and coal-fired electric generating plants, has led to growing interest in the responses of indigenous wild plants to this pollutant class. The varying resistances to fluoride of a large number of naturally occurring plant species were studied in extensive field and laboratory trials, and comprehensively reported on in depth by HORNING and MITCHELL (1982). It was shown that, as a rule, gymnosperms and monocotyledons are more susceptible, while significant differences in resistance levels occur within the dicotyl plant families.
Table 5: Relative sensitivities of various plant species to atmospheric pollution caused by emissions from aluminum factories (from PANDEY, 1981).
Sensitive
Less sensitive
Resistant
Aegele marmelor
Acacia catechu
Achyranthes aspera
Alternanthera moniera
Amaranthur spinorus
Ageratum sp.
Aneilema nudiflorum
Anogeissus latifolia
Albizzia lebbek
Apluda mutica
Boerhaavia diffusa
Alysicarpus monilifer
Aristida adscenscionis
Bothriochloa pertusa
Bonnaya brachiata
Bauhinia tomentosa
Bridelia retusa
Buchanania lanzan
Blepharis molluginifolia
Butea monosperma
Cassia tora
Boswellia serrata
Cassia obtusifolia
Cosmos sp.
Cassia fistula
Cassia pumila
Cynodon dactylon
Cassia occidentalis
Chrozophora rottleri
Dactylacetenium sp.
Celosia arghentea
Chrysophogeon fulvus
Desmodium triflorum
Chloceisn completa
Corchorus acutangulus
Dichanthium annulatum
Convolvulus pluricaulis
Dendrocalamus strictus
Diospyrus melanoxylon
Crotalaria medicagenia
Desmostachya bipinnata
Diospyrus tomentosa
Cymbopogon martini)
Digitaria sangunalis
Ecplipta alba
Emblica officinalis
Eragrostis alsinoides
Eragrostis tenella
Eriolaena hookeriana
Hardwickia binata
Euphorbia hirta
Evolvulus alsinoldes
Holarrhena antidysenterica
Heteropogon contorts
Flacourtia indica
Justicia diffusa
Lagerstroemia parviflora
Gardenia turgida
Oldenlandia corymbosa
Leonotis nepetaefolia
Grewia tiliaefolia
Pterospermum marsupium
Leucas aspera
Helicteres sp.
Ricinus communis
Malvastrum tricuspidatum
Lannea grandis
Sachharum munja
Sida acuta
Madhuca indica
Schrebera swietenioides
Solanum xanthocarpum
Miliusa tomentosa
Scoparia dulcis
Terminalia arjuna
Mimosa himalayana
Sehima nervosum
Terminalia tomentosa
Nyctanthes arbortristis
Shorea robusta
Tephrosia purpurea
Oplismonis vermanis
Tridex procumbens
Woodfordia fruticosa
Paspalidfum flavidum
Vendellia crustacea
Zizyphus glaberrima
Phaseolus mungo
Vernonica cinerea
Zizyphus nummularis
Phyllanthus emblica
Xanthium strumarium
Samalia malabarica
Schleichera oleosa
A further in-depth discussion of the effects of fluoride pollution on Australian plant species has been published by DOLEY (1986). In addition to a description of pollutant accumulation and effects on metabolic processes, the book also contains a large number of colored plates depicting the symptoms of injury caused by fluoride to a large number of species belonging to different plant families. The authors of the present study would also like to recommend the many plant tables included by DOLEY as representing an invaluable source of information.
The dominant tree species of southwestern Australia belonging to the genus Eucalyptus, many of which have major economic importance as sources of timber and firewood, have been shown to be highly sensitive to sulfur dioxide (MURRAY, 1984). In particular, Eucalyptus punctata exhibits foliar injury and accelerated leaf senescence even at low pollutant concentrations. However, no changes in the chlorophyll content of the leaves have been observed in response to SO2 pollution; nor were any visible signs of foliar injury observed in Eucalyptus crebra or Eucalyptus moluccarna. Increased sulfur concentrations were measured in the leaves of all three studied species as a result of SO2 pollution. The high sensitivity and wide distributibon of Eucalyptus species are arguments in favor of their use as response bioindicators for biological monitoring of pollution of the air with SO2.
A study carried out in Nagda, India showed that the mango tree (Mangifera indica L.), widespread in the tropics, is highly sensitive to air pollution situations in which SO2 plays a major part (PAWAR and DUBEY, 1983). Within a radius of 0.5 km of a point source, all of the trees belonging to this species exhibited extensive foliar necroses. Other signs of injury included sparse foliage, stunted growth, short lateral shoots, modified crown structure, failure to bear fruit, and low pigment contents. There was also a clear correspondence between the degree of injury and the pigment contents of the leaves on the one hand, and pollutant concentrations on the other.
In the vicinity of a petroleum refinery emitting SO2 and NO2 in India, mango trees and wheat plants (Triticum aestivum) exhibited conspicuous foliar injury in the form of irregularly arranged bifacial chloroses and necroses in the intercostal zone (PRASAD and RAO, 1985). Here and there injury to leaf apices was also observed, which spread down through the middle of the leaves in the form of brown spots. The teak trees growing in the same area (Tectona grandis) were characterized by prominent bifacial necroses in the intercostal zone. The percentage of injured leaf surface area and the sulfur concentrations in the leaves decreased inversely proportional to the distance from the source (cf. Fig. 8). Trees growing on the lee side of the refinery 1.5 km away were used as control plants.
The use of tobacco plants (Nicotiana tabacum) for biological monitoring of photochemical oxidants has been practiced for many years and is highly standardized. The particularly sensitive variety BEL-W-3 has been selected for use in most of the investigations. The foliar tissue sustains necrotic injury, the severity of which is in direct relation to the intensity of pollution. Tobacco is well-suited for use as a response indicator for active monitoring for a number of reasons, including the ease with which it can be raised and its high sensitivity to atmospheric pollutants. However, its ecological requirements where length of the day and temperature are concerned impose restrictions on the period of time during which it can be used in temperate zones, although this plant species is particularly well-suited as a bioindicator in warmer climatic zones. Relevant studies have been carried out in Australia (HORSMAN, 1981) and Israel (NAVEH and CHAIM, 1978).
The leaf disease which has been afflicting potato plants (Solanum tuberosum L.) during the last few years in the north of India was shown by BAMBAWALE (1986) to be linked with the occurrence of high ozone concentrations in the air. This disease is characterized by numerous light grey, irregularly rimmed spots that grow within a few days to form bifacial lesions. On the underside of the leaves the necrotic tissue appears shiny, and dull and brownish on the upper leaf surfaces. In studies conducted in the United States (HEGGESTAD, 1973) with the potato variety "Cherokee", which responds sensitively to ozone, the described characteristic symptoms first appeared on the oldest leaves of potato plants 40-50 days old, affecting more than a third of the leaf surface area. By contrast, the resistant variety "Teton" sustained injury to only 0.2% of overall leaf surface area. The tobacco variety BEL-W-3 was used in this open-air trial for monitoring of ozone pollution, and the tobacco
plants exposed concurrently with the potato plants - also developed the same foliar injury characteristically caused by ozone.
The effects of cement-kiln dust, SO2 and NH3 emissions on fungi growing on potato plants of the variety "Chandramukhi" were investigated by RAI and PATHAK (1981), also in India. While Mortierella subtilissima and Fusarium semitectum proved to be resistant to sulfur dioxide and NH3 pollution, but occurred only sparsely on sites with and without, respectively, cement-kiln dust pollution, reduced occurrence of Trichoderma spp. was registered in areas with ammonia and cement-kiln dust pollution.
Other subtropical agricultural crop plants also proved to be sensitive to photochemical oxidants.
THOMPSON et al. (1976) studied the sensitivity of two maize hybrids (Zea mays) to photochemical oxidants, primarily ozone. While both varieties - "Bonanza" and "Monarch Advance" - responded with reduced height and dry weight, the variety "Monarch Advance" additionally developed visible injury in the form of premature yellowing and senescence of the leaves.
Within the scope of the "National Crop Loss Assessment Network" carried out in the United States, a 2-year study was devoted to the effect of various ozone concentrations and varying water supply on cotton yields (Gossypium hirsutum L.) (TEMPLE et al., 1985). Half of the plants received an optimum supply of water in open-top chambers, while the other half was subjected to water stress. During the first hot and dry growing season the yields of the optimally watered cotton plants were as much as 45% less than control plants not exposed to ozone. In the case of the plants subjected to water stress, no response to ozone exposure was observed. By comparison, during the second year of the study both groups sustained yield reductions of as much as 65%, although this greater sensitivity of the cotton plants to ozone can be ascribed to the cooler and moister weather during the second year. Ozone exposure experiments carried out with the cotton variety "Stoneville 213", also in
open-top chambers, revealed that this variety reacts very sensitively to naturally occurring ozone concentrations, suffering yield reductions of 11% as compared with control plants grown in filtered air (HEAGLE et al., 1986). Simultaneous fumigation with realistic concentrations of SO2 had no effect on the sensitivity of the cotton plants to ozone pollution.
The grain sorghum variety of which is grown as animal fodder in low-precipitation areas of the United States (Sorghum vulgare Pers.) was exposed to ozone concentrations of between 16 and 129 ppb (KRESS and MILLER, 1985). Foliar injury occurred in the variety used, "DeKalb A28+", only at ozone concentrations in excess of 100 ppb. Depressed yields were shown to result from 7-hour exposure to O3 concentrations of 40 ppb or higher. Two other sorghum millet varieties with differing susceptibilities to hydrogen fluoride were studied by MacLEAN et al. (1984). The more sensitive of the two varieties, "Northrup King 222A", developed prominent symptoms of injury in the form of necroses of leaf tips, chlorotic spots in the intercostal zone of the leaves, and chlorotic and necrotic injury to the tissue along the borders of the leaves, the severity of all of these symptoms increasing with pollutant dosage (0.6-3.3 ~gF/m³); by contrast, only necroses of leaf tips and chlorotic bleaching
in the intercostal zone occurred in the more resistant variety, "DeKalb C44C". Other symptoms of HF-induced injury observed in the "Northrup King 222A variety" were reduced numbers of seeds, and a decline both in foliar mass and total dry mass.
NAKAMURA and OTA (1977) showed that the so-called "akagare disease" which has widely afflicted rice plants (Oryza sativa) in Japan since the late 1960s is caused by photochemical oxidants. Tests in open-top chambers showed that when rice plants grown in unfiltered ambient air were exposed to high ozone concentrations, after just one day the stems developed a large number
of small reddish-brown spots and chlorotic bleaching. The greatest susceptibility was exhibited by young plants with 4-10 leaves, while the leaves of older plants were characterized by loss of chlorophyll and yellowing. By comparison, no foliar lesions occurred in control plants grown in filtered air. The symptoms of pollution injury observed in plants grown under field conditions were identical with those observed in the fumigation experiment, and a high degree of correlation was also shown in the field study between oxidant concentrations and incidence of the akagare disease.
AGRAWAL et al. (1982) fumigated rice plants with ozone and sulfur dioxide. Rice plants fumigated with ozone concentrations of 80 ppb (160 g/m ) developed chlorotic patches that gradually turned brown on all of the leaf surfaces after 7 days. Plants exposed for three days to SO2 concentrations of 500 ppb ( 1,135 g/m³) were characterized by chlorotic streaks in the intercostal area. Combined exposure to 40 ppb (80 1lg/m³) of O3 and 250 ppb (667 1lg/m³) of SO2 induced the same symptoms of injury after just one day, particularly on the leaf tips. The greatest reductions in chlorophyll and carotenoids in leaves was also observed in rice plants which were exposed to a combination of both pollutants (cf. Fig. 9). Besides the visible injury to the plants, therefore, pigment contents could also be used as objectively measurable criteria for biological monitoring.
VALENZONA and MENDOZA (1976) investigated the influence of sulfur dioxide pollution on young rice plants in the Philippines. The first visible signs of injury appeared after 25 days of fumigation with 400 ppb (1,070 mg/m³) of SO2; the injury took the form of isolated brown spots 2-3 mm across following the leaf veins on the upper leaf surfaces. After 30 days of exposure the same symptoms were observed at the leaf edges and on the lower leaf surfaces. After 36 days of fumigation all of the foliar tissue had died. Parallel experiments resulted in significant reductions in growth and depressed grain yields, increasing in severity at higher SO2 concentrations.
In the vicinity of porcelain factories and brickworks in Taiwan that emitted fluorides into the atmosphere, SUN and SU (1985) observed conspicuous foliar injury to rice plants; this injury took the form of acute symptoms such as necrosis of the leaf tips
and chronic symptoms like yellowing and mottling of the foliar tissue. In fumigation experiments with hydrogen fluoride the studied plants exhibited the same symptoms as had been observed under field conditions. Depending on the extent of injury, the injured leaves contained fluoride concentrations up to 80 times as high as levels in healthy leaves.
Numerous studies have been conducted on the influence of atmospheric pollutants on soybean plants (Glycene max.).
The cotyledons and primary leaves responded very sensitively to ozone; 7-8 days after germination, the primary leaves exhibited the highest degree of injury in the form of necroses on the leaf surfaces. In an investigation conducted by HOWELL and KREMER (1972) with 5 different soybean varieties, the "Kent" variety proved to be very susceptible, while the "Cutler" variety was the most resistant. PRATT and KRUPA (1981) established a relationship between ozone concentrations and duration of exposure on the one hand and incidence of chlorotic spots on the primary leaves and trifoliate leaflets in 25-to-30-day-old plants of the "Hodgson" variety on the other hand. A high degree of correspondence between extent of injury and reductions in leaf chlorophyll was also demonstrated (cf. Fig. 10). This relationship can be used to objectify assessment of pollution injury and can serve as a criterion for biological monitoring. REICH et al. (1986) also carried out tests on the "Hodgson"
variety, and found that the reduction in leaf chlorophyll induced by ozone pollution was accompanied by a parallel decline in the net photosynthesis rate (Fig. I I ). The profile shown in Fig. I I shows the net photosynthesis rates for leaves of various ages at different ozone concentrations, giving an indication of when indicative measurements can be meaningfully performed.
TINGEY and BLUM (1973) found that a single l-hour exposure to 75 pphm ozone decreased the number and size of nodules on soybean plants. They also reported that ozone decreased the leghemoglobin content in plant roots, a red pigment related to hemoglobin which plays a role in the symbiotic fixation of nitrogen in the root nodules of legumes. The ozone-exposed soybean plants were also characterized by reduced growth. These results are of great interest for biological monitoring purposes, although their routine application would require considerable expertise.
After exposing soybean plants for 5 weeks in open-top chambers to ozone concentrations of 17-122 ppb (34-244 mg O3/m³), KOHUT et al. (1986) measured reductions in biomass that closely correlated with the pollutant concentrations used. The relative distribution of total biomass among leaves, shoots and pods was not affected. AMUNDSON et al. (1986) reported a linear reduction in growth at increasing ozone concentrations, as well as delayed flower development.
Combined exposure lo SO2 and O3 caused visible foliar injury to soybean plants, as well as a significantly greater reduction in leaf chlorophyll content as compared with exposure to ozone alone (PRATT et al., 1983). At exposure to a concentration of 400 ppb of SO2 acting alone, after 4 hours neither visible injury nor changes in the leaf chlorophyll content could be observed.
HEAGLE et al. (1974) found that, whereas low ozone concentrations merely caused foliar injury and increased shedding of leaves, at both higher concentrations of ozone acting alone and with combined exposure to SO2 and O3 these symptoms were accompanied by reduced growth and depressed yields.
The experiments performed by REICH and AMUNDSON (1984) provided no evidence of synergistic interactions between these two pollutants with regard to reductions in growth and yields in soybean plants. However, these fumigation experiments, which were performed with low pollutant concentrations, did demonstrate that soybean plants possess a significantly higher susceptibility to ozone injury than to injury induced by sulfur dioxide. The parameters employed were the numbers of seeds and pods (Fig. 12).
THOMPSON and TAYLOR (1969) undertook a study of the effects of the complex of atmospheric pollutants typical of the Los Angeles area, consisting mainly of photochemical oxidants and hydrogen fluoride, on growth and yield of several Citrus spp. widely grown in that area, focusing on lemon and orange trees. Whereas growth was in general not adversely affected, visible signs of injury occurred in the form of increased shedding of leaves, and, especially in the case of orange trees, a greater incidence of premature fruit fall (Fig. 13). Fruit yields were also reduced by up to 50%. It may well be feasible to standardize these criteria and apply them for passive monitoring purposes.
Grapevines (Vitis vinifera) can also be classified as being sensitive to photochemical oxidants in the atmosphere (THOMPSON et al., 1969). In addition to foliar lesions in the form of speckling, the studied variety, Vitis vinifera L. "Zinfandel", also exhibited reduced chlorophyll content, a decline in the weight of the grapes, and lower sugar content of the grape juice.
MURRAY (1984) exposed grape plants (Vitis vinifera L. "Shiraz") in open-top chambers to hydrogen fluoride. Depending on the pollutant concentration used, foliar necrosis occurred in varied order of appearance. Whereas the fluoride concentrations in the grapes increased, chlorophyll a levels in the leaves dropped. No effects were observed on the weight or number of grapes, i.e. on yield, or on the chlorophyll b content of the leaves. However, LEECE et al. (1982) reported that the symptoms of injury observed on the grape leaves in response to exposure to hydrogen fluoride can also be due to other factors such as lack of water, lack of potassium and salt stress. Visual diagnosis of fluoride-induced injury should therefore always be supplemented by chemical analysis of the leaves.
TAYLOR et al. (1958) fumigated avocado saplings (Persea americana) with synthetic smog consisting of a mixture of ozone and 1-n-Hexane and studied the effects on growth. Reductions in height growth, leaf width, leaf length and fresh and dry weight were observed. Brown discolorations occurred on the lower surfaces of young leaves, and necrotic lesions also occurred on the edges and tips of a scattering of leaves of varied age. Since the shrublike avocado tree is grown throughout the tropics today, further studies of its pollution susceptibility would be useful.
The effects of aqueous soil extracts on the germinative capacity of the seeds and growth of the roots of three vegetable species - Brassica chinensis, Brassica parachinensis and Daucus carota - were studied by WONG and LAU (1983) with the aid of soil samples taken from along streets and roads in Hong Kong with varying traffic densities. The highest heavy metal concentrations were measured in soil samples taken from a predominantly agricultural region with a relatively low traffic density; these extracts had the greatest inhibitory effects on root growth and on the germinative capacity of seeds. The authors of the cited study attribute the high pollutant concentrations in the soil of this area, which has a very low level of pollution from motor vehicle exhaust, to the use of fertilizers and pesticides containing heavy metals.
GUPTA and GHOUSE ( 1986) conducted studies of the effects of emissions from coal-fired generating plants on the epidermal structures of eggplants (So/unum me/angenu var. Pursa Purple Long). 20-day-old eggplant individuals were transplanted to two different sites. The plants exposed in the vicinity of a power plant complex in Kasimpur, India were characterized by a significant reduction in the size of epidermal cells and the density, total number and size of stomata as compared with the control plants that were exposed at a considerable distance from all pollutant sources. By contrast, trichome length and number were increased. The study results provide evidence of the sensitivity of eggplant leaves to pollutants discharged into the air by coal-fired generating plants; the adaptive epidermal alterations which occur could be used for monitoring of these pollutants.
Studies conducted by YUNUS et al. (1979) using electron microscopy to examine the epidermis of Ricinus communis L., a domesticated plant which is widespread in India and Pakistan and is frequently grown for industrial and medicinal uses, showed that individuals taken from the bank of a sewage canal were characterized by a significant increase both in the total number of stomata and the percentage of abnormal stomata, for instance having only one guard cell. Moreover, clearly visible changes in the surface structure were observed.
The injurious effect of cement-kiln dust on wheat (Triticum aestivum) was studied by SINGH and RAO (1980). They were able to establish a relationship between the distance of the growing site from the pollutant source on the one hand and leaf chlorophyll content and biomass production on the other hand. Visible injury such as cracking, surfacial peeling and wilting occurred only in plants grown in the immediate vicinity of a cement factory, within a radius of 500 m. Grain analyses carried out parallel to this revealed reductions in both quantity and quality. In fumigation experiments involving exposure of plants 40-100 days old to cement-kiln dust, linear relationships were established between pollutant dose and effects on transpiration rate, chlorophyll content and biomass production (SINGH and RAO, 1981).
MISHRA (1982) investigated the effects of fly ash and sulfur- dioxide on the weed Commelina bengalensis L, which occurs widely in northern India. Plant populations studied in the vicinity of a coal-fired generating plant exhibited significant reductions in biometric parameters such as shoot length, leaf surface area and size of fruits and flowers as compared to samples taken from an unpolluted region. Whereas the stomata! frequency was also reduced, increased trichome density and length were measured.
The effects of motor vehicle exhaust gases on the activities of certain enzymes in wild herbaceous plants were studied by SARKAR et al. (1986) in India. Samples were taken of five different species at varying distances from the National Highway 2, which connects Calcutta with Bombay. Visible symptoms of injury in the form of reduced growth, chloroses and dark discolorations were observed in all plants up to a distance of 25 m from the edge of the road (cf. Fig. 14). Moreover, in all studied plants a significant rise in peroxidase and catalase activity was determined, the magnitude of which could be directly correlated with the distance of the sampling sites from the road (Figs. 15 and 16).
EBEL et al. (1984) found that Phyllanthus fluitans BENTH (Euphorbiaceae) is suited for biological monitoring of 502 in humid tropical regions. Phyllanthus fluitans occurs in swamps and bodies of water in northern South America, and has a habit similar to that of Salvinia. The plants were exposed to various SO2 concentrations (by combined fumigation and sprinkling) for 8 hours in artificial light. At the end of this period, the leaves, originally middle green to reddish in color, had suffered a significant loss of pigment. At SO2 concentrations of 0.17 mg/m³ or less no visible signs of injury at all were observed. However, even at low SO2 concentrations changes were observed in the ratio of chlorophyll a to chlorophyll b, as well as reduced protein content and increased carbohydrate content.
Tillandsia aeranthus and Tillandsia recurvata (Bromeliaceae) collected in South Brazil and adapted to Central-European conditions were fumigated with an average SO2 concentration of 400 g/m³ in order to obtain ecotoxicological data for the development of a bioindicator procedure (ARNDT and STREHL, 1989). After 25 days, the experiments led in the case of Tillandsia aeranthus only to distinct visible injuries, such as the folding of leaf tips, chloroses, and tip- and striping necroses. Also, many changes could be observed within the plants by means of light- and electron-microscopy. Particularly striking were the formation of crystals in the cells and the total closure of the trichomes, which is related to the coverage of the stomata. Given the fumigation applied, the sulfur content of the plants was, however, rather low. The results show that a great deal of further investigation is required in order to develop a bioindicator for sulfur dioxide.
<section>3.3 Accumulative indicators</section>
In addition to the response indicators described above, a number of plants are suited for use as accumulative indicators for monitoring of air quality (cf. Chapter 2). In order to gain information on heavy metal pollution in tropical regions, SCHRIMPFF (1981) carried out studies in the densely populated Cauca Valley in Colombia, in which the city of Cali is located. The plants used as accumulative indicators were the epiphytic bromeliaceous species Tillandsia recurvata L. and Tillandsia usneoides L. (Spanish moss), both of which also occur in urban areas in this region. Epiphytes are particularly well-suited for monitoring of atmospheric pollutants, since they satisfy their nutritional requirements exclusively from airborne dust and precipitation, and accumulate pollutants, including heavy metals, in their tissues. Plant samples were collected at the nodes of both a widely spaced grid (10 km) and a closely spaced grid (2 km), and the concentrations of various heavy metals in
their tissues analyzed. On the basis of a comparison of the heavy metal values from the Cauca Valley with average values for the southern United States, it was possible to perform an initial assessment of heavy metal pollution in this tropical region: the lead levels can still be considered very low, while Cd and Zn are present in concentrations similar to those in the southern United States, and Cu and Ni have even reached significantly higher levels.
Other studies conducted in the vicinities of two large Colombian cities showed that Tillandsia recurvata L. can be used for monitoring not only of anorganic trace elements (cf. Fig. 17), but also atmospheric pollution with organic compounds such as pesticides and polycyclic aromatic hydrocarbons (cf. Fig. 18) (SCHRIMPFF, 1984). The"biofilter method" used has proven to be a timesaving and cost-effective way of obtaining initial reliable data on relative air pollution levels and the spatial distribution of heavy metal deposition, even in the developing countries.
In order to study whether long-range transport of atmospheric pollutant s is taking place to remote parts of the Amazonian rain forest in southwestern Venezuela, MONTAGNINI et al. (1984) collected various moss species and tree leaves with and without epiphytic mosses near the small settlement of San Carlos de Rio Negro, which is 900 km away from the Venezuelan centers of heavy industry and 3,000 km away from those of Brazil, and analyzed their heavy metal concentrations. They found significantly higher concentrations in the leaf samples with attached epiphytic moss than in those without epiphytes, indicating the possibility of heavy metal pollution in the atmosphere as a result of long-range transport, even though it is minimal (cf. Figs. 19 and 20). No differences were observed between the generally low heavy metal concentrations in moss samples taken from live trees and dead tree stumps. Compared with regions far from industrial centers in the temperate latitudes, the
heavy metal concentrations measured in this study were characterized by significantly lower levels. They had approximately the same magnitude as those measured in lichens in Panama, and were noticeably lower than those in mosses in rural parts of Nigeria.
In Nigeria, ONIANWA and EGUNYOMI (1983) studied the heavy metal concentrations in 17 different moss species in the urban zone of Ibadan and in several rural areas. Whereas it was not possible to correlate the lead concentrations in samples taken from within the urban area with traffic densities, all of them were much higher than those in samples from the botanical garden of the university. Significantly lower lead concentrations were measured in moss samples from rural areas. The situation was similar with zinc, but in the cases of the other studied metals (Cu, Cd, Ni, Mn, Mg, Fe) no differences were found between rural and urban areas.
Within the scope of another study in Nigeria, ONIANWA et al. ( I 986a) collected various acrocarpous and pleurocarpous mosses in forested areas and at the edges of settled areas within a radius of 120 km around the city of Ibadan, which is the capital of the Westem State and has a population of over 1 million, and examined their heavy metal concentrations. The authors of the cited study compared the measured concentrations with study results from Central Europe and North America. The lowest lead concentrations were found in moss samples from very remote areas with very little road traffic, but on average were still far higher than the so called "background" concentrations measured in other parts of the world far from industrial centers. High lead concentrations were measured near densely populated areas, although these were less than values from comparable areas with high air pollution levels in Scandinavia and the Federal Republic of Germany. The same situation was
established with regard to zinc, cadmium and nickel concentrations. The high copper concentrations found in the moss samples from some parts of the study area were attributed by the investigators to the use on cocoa farms of fungicides and pesticides containing copper. Compared with iron and manganese concentrations measured in the industrial nations of Central Europe and North America, the mosses sampled in Nigeria were characterized by extremely high and greatly varying accumulation rates, for which reason they are not suited for monitoring of changes in the deposition rate of these metals.
The same investigators also studied the ability of three of the moss species used as accumulative indicators in the above-mentioned study to absorb and retain Pb, Cu and Cd ions (ONIANWA et al., 1986b). All three species - Rhacopilopsis trinitensis (C. Muell) Britt. et Dix., Stereophyllum virens Card. and Thudium gratum (C. Muell) were found to possess high absorption and retention capacities for these ions, and may therefore be regarded as suitable accumulative indicators for the corresponding metals.
In order to study the spatial distribution of heavy metal pollution caused by industrial facilities and automotive exhaust in Kampala, Uganda, NYANGABABO (1987) collected samples of the lichen Calyrneferes usambaricum at various sites within and outside of the urban zone and subjected them to analysis. Whereas no differences in calcium, magnesium and nickel concentrations were found between urban and rural areas, lead, cadmium and iron accumulations at urban and suburban sites could be correlated with motor vehicle traffic densities and the nearness of stationary pollutant point sources.
For the purpose of determining the influence of atmospheric pollutants on desert vegetation, GARTY (1985) measured the heavy metal concentrations in various different lichen species growing in the Negev desert in Israel. A high lead accumulation rate was found in the thallic tissue of samples of Squamarina crassa, which is eaten by grazing goats, taken from directly alongside a major desert highway. The lead concentrations measured in the lichens were considerably higher than those in the soil substrate on which they grew.
In the provincial capital of Benin City (located in the Nigerian rain forest zone), in which 75-80% of atmospheric pollution is caused by motor vehicle exhaust, ADEMOROTI (1986) took bark and fruit samples from individuals of five different economically important tree species (Delonix regia, Terminalia catapa, Casuarina equiselifolia, Mangifera indica and Citrus sinensis) growing along streets with varying motor vehicle traffic densities and measured their levels of various heavy metals. A clear relationship was found between the measured concentrations of lead and zinc and traffic densities at the sampling sites; in addition, a rough surface texture of the bark was correlated with a high rate of deposition of these metals (see Fig. 21). By contrast, no relationship could be established between traffic density and cadmium or copper accumulation in the bark of the trees. The measured lead concentrations were significantly less than those found by studies in Canada and Great
Britain. ADEMOROTI nevertheless calls attention to the fact that. especially because it is to be expected that traffic density will continue to increase in the near future and heavy metal enrichment in the studied tree species will therefore also be intensified, health hazards for the population can arise? since almonds, mangos and oranges play a major nutritional role locally and the leaves and bark of the trees are also widely used for treatment of malaria.
ELSOKKARY (1982) studied the Hg concentrations in various vegetable varieties in Alexandria. The Hg pollution in this area is principally caused by local industrial plants that use salt electrolysis for production of caustic soda and chlorine gas. The results showed that, in particular, growing of lettuce, radishes, parsley, cabbage and jute is inadvisable due to high mercury concentrations in the edible plant parts. Parallel soil analyses also showed a close correlation between mercury concentrations in plant tissue and in the soil at various distances from the industrial facilities.
Also in Egypt, SHAKOUR ALI and NASRALLA (1986) performed investigations that showed a clear relationship between lead and cadmium concentrations in various clover species that grow on roadsides on the one hand and motor vehicle traffic density and distance from the road on the other hand. Concentrations of as high as 40 mg Pb/g and 1.6 mg Cd/g were found in the samples, which were taken from alongside the highway linking Cairo and Alexandria and washed prior to analysis.
In the vicinity of an industrial complex containing chemical plants which mainly emitted SO2 and HF, GANESAN et al. (1978) studied pollutant concentrations in sorghum plants (Sorghum vu/gare). All of the samples taken from a farm close to the factories exhibited the foliar necroses characteristically caused by hydrogen fluoride pollution, and their leaves consistently had far higher fluoride contents than those of plants from a farming area 4 km distant.
WONG and TAM (1978) found high lead accumulations in two Brassica species grown next to roads in Hong Kong. The result of the study showed that in Brassica parachinensis and Brassica alboglabra there was a clear correlation between the lead concentrations in the soil and in the plants on the one hand and the distance of the sampling sites from the road on the other with a positive correlation between the concentrations in the individual plant parts and the lead concentrations in the soil. In both plant species the accumulations were greater in the leaves and roots than in the stalks (cf. Figs. 22 and 23).
Along five major roads connecting the city of Erbil, situated in a major dairy and meat production area in northern Iraq, with other parts of the country, HAQUE and HAMEED (1986) collected various wild plant species that account for most of the forage eaten by the livestock kept in this region and subsequently analyzed their lead concentrations. They found very high lead concentrations with maximum values of 23 mg/g of dry matter in all of the examined samples, with concentrations in plant material taken from locations 60 m away from the roads being higher than those in samples taken directly at the road edges, with variation governed by the prevailing wind directions.
In Puerto Rico, RODRIGUEZ-FLORES and RODRIGUEZ-CASTELLON (1982) took samples of the most widely occurring grass species, Cenchrus echinatus L., Sorghum halopense, Paspalum paniculatum L. and Stipa ichu, at various distances from the edges of heavily travelled roads and investigated their Pb and Cd contents. They found that the measured concentrations correlated closely with the motor vehicle traffic densities at the sampling sites. A correlation was also established between the lead concentrations in the grass plants and their distance from the roads at different wind directions (cf. Fig. 24).
The effects of automotive lead pollution on two weeds growing along the edges of the Bombay-Ahmedabad highway in India were studied by KRISHNAYYA and BEDI (1986). The parameters they examined were pollutant accumulation, pollen grain germination, pollen tube growth and germinative capacity of the seeds of Cassia tora L. and Cassia occidentalis L. individuals taken at varying distances from the road. Whereas the magnitude of lead accumulation in the plant tissue was inversely proportional to the distance from the road, there was a direct relationship between the percentage of pollen grain germination, pollen tube growth and germinative capacity of seeds on the one hand and both the measured lead concentrations in the plants and the distance of the sampling sites from the road on the other hand as compared with control plants from unpolluted areas.
Because of the wide distribution in many tropical and subtropical countries of the grass Panicum maximum, which is grown as animal fodder, this species can be regarded as suited for use as an accumulative indicator. WUSTEMANN (1983) found that the lead concentrations in plants growing in the vicinity of a lead recuperation facility in Guacara, Venezuela were found to permit reliable conclusions to be drawn on pollution of the environment with lead at varying distances from the facility (WUSTEMANN, 1983).
DE LACERDA (1982) designated the halopyhtic species Sesuvium portulacastrum as being a suitable indicator plant for heavy metal pollution of the environment. The advantages of Sesuvium for this purpose are its large biomass and wide distribution in the tropics. Relevant studies were carried out around the mouth of the Iraja River near Rio de Janeiro. The measured heavy metal concentrations (Cu, Cr, Zn, Mn and Ni) were of the same magnitude as levels measured in temperate regions.
Another halopyhtic plant species which grows along the shores of the Iraja River, Philoxeros vermicularis, contained chromium concentrations 10 times higher than those in plants growing in a control area (PFEIFFER et al., 1982). It was also shown that the aquatic plant Paspalum vaginatum developed chromium accumulations corresponding to the concentration in the surrounding medium.
All of the studies discussed so far deal with passive monitoring, but active monitoring approaches could also be applied. In Central Europe, transplanted lichens and other plants have already proven their usefulness as response bioindicators. Studies by GARTY and FUCHS ( 1982) in Israel showed that the lichen species Ramalina duriaei, which grows on the carob tree (Ceratonia siliqua), is also suited for use as an accumulative indicator for evaluation of air quality within the scope of active biological monitoring. The criterion which can be used is enrichment of various heavy metals (Cu, Cr, Cd, Pb, Zn, Ni) in transplanted specimens (cf. Figs. 25 and 26). In further studies of this lichen species concentrations of Ca, P, K, Br, Cl, S, Ti, Li and Sr were determined (FUCHS and GARTY, 1983). The decline in the chlorophyll a contents of pigment extracts from transplanted individuals was also measured. While increased concentrations of Br, Pb, Fe and Ti were associated with
decreased chlorophyll a contents, no significant relationship between pigment contents and other elements could be established (e.g. S, Ca, Cl, Sr, Zn, P).
A summary of the potential biological monitoring procedures reported on in this chapter is provided in Table 6.
Table 6: Survey of possible bioindicators for the tropics and subtropics.
Indicator
Country
Response criteria
Pollutants
Degree of usefulness
References
Wild annual
Zambia
Pointer organisms
Cu
DREW and
plants
REILLY,
Wild annual
Sonoran Desert
Cu
WOOD and
plants. Cacti
United States
NASH, 1976
Wild plants
Hong Kong
SO2
WONG, 1978
Wild plants
Mojave Desert
Response indicators
SO2/O3
THOMPSON
United States
(passive)
et al.,
Necroses
Wild plants
Mojave Desert
(passive)
SO2/NO2
THOMPSON
United States
Necroses
et at.,
Growth
Wild plants
Australia
(passive)
HF
HORNING
Necroses
and MIT
CHELL,
1982, DO
LEY 1986
Wild plants
India
(passive)
Automotive
SARKAR
Necroses
exhaust
et al., 1986
Growth
gases
Enzyme activity
Commelina
India
(passive)
SO2/fly ash
MISHRA,
bengalensi,
Growth
Ricinus
India
(passive)
Sewage
YUNUS et
communis
Epidermal injury
al., 1979
Phyllanthus
South America
(passive)
SO2
EBEL et al.,
fluitans
Necroses
Pigment content
Tillandsia
Brazil
(passive)
SO2
ARNDT and
aeranthos
Necroses
STREHL,
Tropical dry
India
(passive)
HF
PANDEY,
broad-leaved forest
Necroses
Terminalia
India
(passive)
HF
PANDEY,
tomentosa
Pigment content
Buchanania lanzan
Foliar biomass
Dyopsyros
India
(passive)
HF
LAL and
melanoxylon
Pigment content
AMBASHT,
Foliar biomass
Mangifera
India
(passive)
SO2
PAWAR and
indica
Necroses
DUBEY,
Growth
Pigment content
Mangifera indica
India
Necroses
SO2/NO2
PRASAD and
Tectona grandis
RAO, 1985
Eucalypts
Australia
(passive)
SO2
MURRAY,
Necroses
Pigment content
Nicotiana
Israel
(active)
O3
NAVEH and
tabacum
United States
Necroses
CHAIM,
HORSMAN,
Solanum
India
(passive)
O3
BAMBAWA
tuberosum
Necroses
LE, 1986
Indicator
Country
Response criteria
Pollutants
Degree of
References
usefulness
Zea mays
United States
(passive)
O3
THOMPSON
Necroses
et al.,
Growth
Gossypium
United States
(passive)
O3
TEMPLE et
hirsutum
Growth
al., 1985
Yields
HEAGLE et
al., 1986
Sorghum
United States
(passive)
O3
KRESS and
vulgare
Necroses
MILLER,
Yields
Necroses
HF
MacLEAN et
al., 1984
Oryza sativa
Japan
(passive)
O3
NAKAMURA
India
Necroses
and OTA,
Pigment content
AGRAWAL
et al., 1982
Philippines
Necroses
SO2
VALENZONA
and
MENDOZA,
Taiwan
Necroses
HF
SUN and
SU, 1985
Glycine max
United States
(passive)
O3
HOWELL and
Necroses
KREMER,
Pigment content
Photosynthesis rate
PRATT and
KRUPA, 1981
REICH et al.,
Growth
TINGEY and
BLUM, 1973
Biomass
KOHUT et
al., 1986
Necroses
SO2/O3
PRATT et al.,
Pigment content
Growth
HEAGLE et
Yields
al., 1974
REICH and
AMUNDSON,
Triticum
India
(passive)
Cement-kiln
SINGH and
aestivum
Necroses
dust
RAO, 1980,
Pigment content
Biomass
Citrus spp.
United States
(passive)
O3/HF
THOMPSON
Defoliation
and TAYLOR
Yields
Indicator
Country
Response criteria
Pollutants
Degree of
References
usefulness
Vitis
United States
(passive)
O3
THOMPSON,
vinifera
Necroses
et al.,
Pigment content
Yields
Australia
Necroses
HF
MURRAY,
Pigment content
Persea
United States
(passive)
Synth. smog
TAYLOR et
americana
Necroses
al., 1958
Growth
Solanum
India
(active)
SO2
GUPTA and
melangena
Epidermal injury
GHOUSE,
Brassica spp.
Hong Kong
(passive)
Automotive
WONG and
Root growth
exhaust
LAU, 1983
Germinative
gases
capacity of seeds
Wild plants
Iraq
Acumulative
Pb
HAQUE and
indicators
HAMEED,
(passive)
Wild plants
India
(passive)
Pb
KRISHNAY
YA and
BEDI, 1986
Wild plants
Puerto Rico
(passive)
Pb/Cd
RODRIGUEZ
FLORES and
RODRIGUEZ
CASTELLON,
Wild plants
Egypt
(passive)
Pb/Cd
SHAKOUR
ALI and
NASRALLA,
Sesuvium por-
Brazil
(passive)
Heavy
DeLACER
tulacastrum
metals
DA 1982
Philoxeros
Brazil
(passive)
Cu
PFEIFFER
vermicularis
et al., 1982
Paspalum
vaginatum
Tillandsia
Colombia
(passive)
Heavy
SCHRIMPFF
spp.
metals
Organic
compounds
Epiphytic
Venezuela
(passive)
Heavy
MONTAG
mosses
NINI et al.,
Indicator
Country
Response criteria
Pollutants
Degree of
References
usefulness
Mosses
Nigeria
(passive)
Heavy
ONIANWA
metals
and
EGUNYOMI,
ONIANWA
etal.,
1986a/b
Calyrneferes
Uganda
(passive)
Heavy
NYANGA
usambaricum
metals
BABO 1987
Squamarina
Negev Desert
(passive)
Pb
GARTY,
crassa
Israel
Ramalina
Israel
(active)
Heavy
GARTY and
duriaei
metals
FUCHS, 1982
Broad-leaved
Nigeria
(passive)
Heavy
ADEMORO
trees
Tl, 1986
Panicum
Venezuela
(passive)
Pb
WUSTE
maximum
MANN, 1983
Sorghum
India
(passive)
SO2/HF
GANESAN
vulgare
et al., 1978
Vegetables
Egypt
(passive)
Hg
ELSOKKA
RY, 1982
Brassica
Hong Kong
(passive)
Pb
WONG and
spp.
TAM, 1978
- not useful at the time
+ might be suitable for use in active monitoring after extensive development or adaptation
++ further development may be promising
+++ developed procedures, which need only be adapted
<section>4. Discussion and recommendations</section>
If the results summarized in Table 6 are considered in the light of knowledge gathered in the industrialized countries (Chapter 2), then the conclusion is unavoidable that possibilities exist today for application and further development of biological monitoring in tropical and subtropical countries as well. Nevertheless, a great deal remains to be done in the way of preliminary work before practical application can commence.
When making decisions on the methods which have the greatest likelihood of success in given instances, the principal criteria which must be examined are the ecological and sociological conditions in the countries where studies are being planned. This refers above all to site factors, but also has to do with the level of knowledge and expertise on the part of those who will be conducting the studies, laboratory capacities and the behavior of local populations. The last-mentioned aspect can have a crucial bearing on the success of some active monitoring procedures, since theft and destruction of test stations can occur out of ignorance. For instance, there is always a certain risk involved in setting out self-watering pot installations, although these are without a doubt indispensable during dry periods. Yet, it is precisely such active monitoring methods deployed in source-oriented grids that yield the most reliable data when collecting evidence against environmental
polluters or investigating the environmental compatibility of planned installations. Only such approaches can eliminate uncertainty caused by unknown soil and nutrient conditions and competition from other vegetation. By arranging the stations in a checkerboard pattern or in radiating lines it is sometimes even possible to partially overcome unfavorable topographic reliefs.
Table 6 lists only one plant species which could be used for active monitoring relatively unproblematically and without major preliminary studies. This is the tobacco variety BEL-W-3, which responds to photochemical oxidants, especially ozone, and as such can be classified as a response indicator. Since photochemical oxidants are secondary atmospheric pollutants, this plant can be used to perform a kind of background measurement. In addition, young eucalypts would be suitable for use as response indicators for SO2, although the heterophyllous nature of these trees would have to be taken into account. The same holds for various lichens, if it is possible to transplant them onto exposure installations and adapt them to different sites. One accumulative indicator which has already been successfully used for active monitoring is the lichen Ramalina duriaei. It would also be possible, following the example of the standardized grass culture, to test suitable species and varieties
native to tropical and subtropical countries. However, the required investigations, above all testing of tolerances, accumulation abilities, suitability for being cut back, etc., would be extensive and require a long period of time.
A number of organic and anorganic materials may also be suitable for active monitoring, since they react to pollution with physically measurable responses. Sheet steel, for example, exhibits an accelerated corrosion rate when exposed to SO2 or other acidic gases, manifesting itself in the form of increased weight. Trials and/or modifications of this approach would definitely be required in especially dry regions, since the formation of iron oxide depends on a certain minimum atmospheric humidity.
The expansion of natural rubber can be measured simply by taking readings with a millimeter scale, without the need for any laboratory tests. It is influenced by the concentration of ozone in the ambient air. Preliminary trials still remain to be performed on this method, however, so that it will not be ready for use until sometime during 1988.
Little interference from local populations need be feared in the case of passive monitoring. In this approach, either standardized methods are used for examining naturally occurring vegetation for pollution injury in situ, or else apparently undamaged plant organs are removed and their pollutant concentrations analyzed in the laboratory. The reliability of the data which can be obtained in this way increases with the number of points sampled around a source. Compared to active biological monitoring, therefore, this requires a more closely spaced grid in order to permit conclusions to be drawn on the atmospheric pollutants that are causing injury to the plants.
In general, with passive biological monitoring it is essential to take the vegetation at the site of study and surrounding region into account. The only alternatives are therefore to exclusively address such plant species that occur widely within a given biome, like certain domesticated plants, or else to perform assessments of each individual site on the basis of thorough familiarity with local conditions. The latter possibility will not be discussed any further here, since at this time only a handful of ecotoxicologists from the industrial nations are likely to possess the required knowledge.
Great care is required when undertaking routine use of wild plants as bioindicators within the scope of a passive monitoring program. Only a few studies have been performed on the effects of pollutants on such organisms, but they show that even varieties of one and the same species can respond very differently. Particularly where herbaceous plants are concerned, experience has shown that several different varieties can occur within an area spanning just a few hectares, thus potentially leading to completely wrong assessments. It should be mentioned in this connection, however, that "mosses" of the genus Tillandsia have been used quite successfully as accumulative indicators for passive monitoring (SCHRIMPFF, 1987, 1988).
Of the species listed in Table 6, it is particularly the eucalypts which react sensitively to SO2 that appear to hold promise for passive monitoring. The fact that during the last 20 years their silvicultural utilization has spread rapidly in the subtropics outside of Australia, where they originated, ensures that they would have a large validity range and importance (cf. Chapter 2). Their degree of representation for other tree species would have to be investigated. The low-growing citrus trees which have proven to be sensitive to photochemical smog in California may well also play a useful role. In addition, the mango tree has also expanded far beyond its native range, namely the Malay Archipelago, and is now cultivated nearly everywhere in the tropics. Because of its wide distribution it can also be regarded as a potential bioindicator species.
Various varieties of grape plants have repeatedly been observed to respond to fluoride pollution and ozone with visible symptoms. The degree of sensitivity is dependent on the variety, however, a fact which would make it necessary to conduct preliminary tests.
Finally, certain lichens could also be used as response indicators, although it must be taken into account that in hot, dry regions these plants are only metabolically active for a few hours each day. Here, too, preliminary studies would be a must.
Lichens can also be utilized as accumulative indicators within the scope of passive monitoring. However, an essential prerequisite for this type of approach is the availability of staff and equipment for effective laboratory analysis, an aspect which even in the industrial countries does not always attain the required standards. However, appropriately dried and prepared samples can be relatively easily transported and thus centrally processed in specialized laboratories. Besides lichens, Panicum maximum could also hold promise as an accumulative indicator, as studies at my own institute have shown (WUSTEMANN, 1982).
From what has been said above, a few conclusions can be drawn regarding future work aimed at use of plants as bioindicators in tropical and subtropical countries. Accordingly, the following steps must be carried out:
1. Review and evaluation of the studies which have already been carried out in tropical and subtropical countries on the effects of pollutants. Centrally coordinated compilation of documentation on various relevant fields at appropriate specialized institutes.
2. Compilation of an atlas containing plates illustrating the effects of pollution on selected agricultural and silvicultural plants from the tropics and subtropics as a basis for development of response indicators.
3. Development and/or adaptation of response indicators for tropical and subtropical conditions. Cooperation with institutions in industrial and threshold countries (South Africa, Brazil, Australia) of these regions.
4. Identification and development of accumulative indicator plants together with appropriate analytical techniques.
5. Preparatory studies and development work in specialized German laboratories within the scope of a feasibility study.
6. Implementation of a selected model biological monitoring project in a tropical or subtropical country.
On the whole, it can be ascertained that, although much remains to be learned, our present level of knowledge nevertheless represents a firm basis for continued work. If activities are appropriately coordinated by a national working group, it should be possible to concentrate on a few promising goals. In cooperation with institutes in the countries where these biological monitoring procedures could potentially be applied, preparations could then be carried out for field studies.
We would like to conclude by reiterating our conviction that biological monitoring is highly suited for use in the developing countries. This conviction is based above all on two factors. One is that, in general, biological monitoring is technologically less demanding than physical sampling and analysis of pollutants, a fact which responds well to the situation in these countries. The second, even more important, aspect has to do with the inherently different type of information provided by biological monitoring (cf. Chapter 2). If use of bioindicators and response-oriented monitoring approaches in the tropical and subtropical countries begins soon, it may well be possible to set a development in motion which is based on obtaining evidence of and preventing pollution injury, and which is not limited to implementation of cost-intensive pollution monitoring networks.
<section>5. Summary</section>
The present study begins by defining important concepts related to biological monitoring, and goes on to discuss the possibilities and limitations of this approach at all levels, including comprehensive response oriented pollution inventories. Focussing on biological monitoring of atmospheric pollution, a few relatively well-developed techniques from Central Europe are presented. Those chosen for discussion are relevant for the objectives of the study and, after being modified somewhat, could also be applied to other conditions elsewhere.
Based on a review of existing literature on relevant studies conducted in the tropics and subtropics, a number of biological monitoring procedures are then discussed which could be of importance for the developing countries of the tropics and subtropics. The responses of inanimate materials such as steel and rubber to pollution are also given attention.
On the whole, the conclusion is arrived at in the study that, on the basis of what is known today, it would definitely be of advantage to apply and develop biological monitoring in the world's tropical and subtropical countries. Recommendations are also presented on the steps which need to be taken.
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<section>Bioindicators for monitoring of atmospheric pollutants in Asian countries</section>
(A survey of the literature up to 1986)
by Lore Steubing, Jutta Biermann, Reinhard Debus
<section>1. Introduction</section>
In view of the growing problems caused by environmental pollution in both the industrialized and the developing countries, there is a justified interest in finding appropriate methods for monitoring the environment and detecting the level of atmospheric contamination.
Because of the inherent limitations imposed on the information yielded by individual measurements of physical and chemical parameters, as well as practical difficulties associated with performing them, it is worthwhile investigating whether- especially in developing countries - biological indicators could be used alternatively or additionally to monitor the environment in tropical and subtropical ecosystems.
The aim of this survey of the literature is to show where in Asia biological monitoring ("biomonitoring") has already been practiced, and which, if any, unique aspects or special problems have arisen or must be taken into account in future.
A survey is provided of the techniques of biological indication which have been applied in India, China and Hong Kong. In addition, work which has been done in South Korea, Thailand and Malaysia is also given consideration. Japanese studies are discussed only by way of illustration.
Considerable difficulties had to be overcome in order to obtain some of the publications surveyed here. We were provided with most of the articles from China and India with the assistance of scientific colleagues in the respective countries. It was possible to obtain part of the literature by way of libraries, especially the library of the University of Hanover.
Almost without exception, the Chinese publications are also written in Chinese. Only a few of the articles begin with a brief English abstract. In order to carry out a detailed study of the literature, however, it was necessary to have certain of the articles translated.
In connection with articles that appeared in the periodicals "Journal of Environmental Science" and "Journal of Ecology", the problem arose that, evidently, in each case two journals exist with the same name, and the Chinese ones were not available in the Federal Republic of Germany.
For the above reasons, the present survey - finished in 1986 - cannot lay claim to being exhaustive.
The basis for decisions on whether or not and in what way a given plant species is suitable for use as a biological indicator is provided by laboratory experiments in which the resistance or sensitivity of crop and meadow plants to selected environmental contaminants are investigated. For this reason, the presentation of practical examples is preceded by a survey of fumigation experiments and their results.
These publications on bioindicators have been organized on the basis of the different monitoring techniques and biological indication types which they deal with. In the case of a few selected examples, the results are presented in graphical and tabular form. Potential sources of error are pointed out.
Finally, all of the surveyed publications are listed in a bibliography, grouped by country.
<section>2. Applied biological monitoring techniques in Asia, with special consideration given-to the developing countries</section>
<section>2.1 Fumigation and dusting experiments as the basis for selection of biological indicators</section>
The surveyed publications from India describe fumigation experiments which were carried out on agricultural crop plants. The concentrations of pollutants used for fumigation were between 0.25 ppm and 2 ppm. The experiments were conducted for maximum durations of 3 months, between I and 8 hours per day. As far as can be gleaned from the articles, the experiments were conducted either in simple fumigation chambers or in the open. Recently, single experiments have also been conducted in open pots.
PRASAD & RAO (1980 and 1981) exposed Triticum aestivam (wheat) to SO2 and studied its calorific value, respiration rate, carbohydrate content and biomass. RAO (1980) worked with Medicago sativa (alfalfa). He also studied the effect of SO2 fumigation on biomass, as well as that on primary production, root and shoot lengths, and chlorophyll content. SINGH & RAO (1980 a and b) extended the above-mentioned measurements to Solanum melangena (eggplant) and Phaseolus aureus (bean), also determining citric acid content and the pH value of leaf extract, and assessing leaf damage. The work of AGRAWAL et al. (1982) focused on monitoring of pigment, assessment of leaf damage and a description of pollution induced symptoms. The object of their study was Oryza sativa (rice). VARSHNEY & VARSHNEY (1981) studied the effects of SO2 pollution on pollen germination and pollen tube growth in Cicer arietenum (chick-pea), Nasturtium indicum (watercress), Petunia alba (petunia) and Tradescantia
axillaris (tradescantia).
AGRAWAL (1985) performed SO2 and O3 fumigation experiments on Oryza sativa (rice), Panicum miliaceum (Indian millet), Cicer arietenum (chick-pea) and Vicia faba (broad bean). He chose the symptoms of leaf damage, transpiration rate, pigment and metabolite contents, as well as catalase and peroxidase enzyme activity and biomass production as parameters for assessing the potential of each of these plant species as biological indicators.
AWANG & ZAINUN (1985/Malaysia) exposed plants to environmentally significant concentrations of gaseous SO2. They studied the effect of SO2 on transpiration, diffusion resistance, potassium loss of leaves, and chlorophyll content in Petunia sp. (petunia), Ixora javanica (evergreen shrub) and Cinnamon iners (cinnamon tree); these are ornamental plants that grow in the parks of Kuala Lumpur.
In a study by JIANG MEI-ZHEN (1983/China), the effects of SO2 on ornamental plants of varying sensitivity were investigated. Potted Petunia hybrida (petunia), Pelargonium hortorum (geranium), Begonia semperflorens (begonia), Dianthus barbatus (carnation), Euphorbia pulcherrima (spurge), Tulipa gesneriana (tulip) and Hyacinthus orientalis (hyacinth) plants were exposed to the air of different parts of Hang Zhou with varying intensities of SO2 pollution. An oil refinery was named as the source of the pollutants. The plants were grown from cuttings or seed, either in a greenhouse or directly in the open. The exposed pots were watered once a day. No additional information on the fumigation conditions is supplied. After 24 and 48 hours the damage to the leaves was assessed and the plant species assigned to one of three groups depending on the degree of damage suffered:
1. Very sensitive; 50% of the leaf surface area is damaged after 24 hours, and the flowers droop.
2. Sensitive; no obvious symptoms until fumigation has lasted 48 hours; 50% of the leaf surface area is damaged, the leaves wilt and turn yellow, but are not shed prematurely.
3. Non-sensitive; the leaves remain green, less than 10% of the leaf surface area is damaged.
CAO HONGFA and TAYLOR (1985/China) studied the growth and stomatal response of pinto bean plants following long-term fumigation with low SO2 concentrations. They were able to show that SO2 levels below the toxic threshold led to reduced growth, but that just one day after beginning fumigation the transpiration resistance reached the control value.
A large number of publications by Japanese researchers have appeared on fumigation experiments with SO2, O3, NO2 and ethylene:
Exposure to SO2
FUJINUMA & AIGA (1980) carried out SO2 fumigation trials with the aim of identifying sensitive rice varieties. The effects of SO2 on photosynthesis, transpiration and stomatal resistance in Helianthus annuus (sunflower) were described by FURUKAWA et al. (1980) and USHIJIMA & TAZAKI (1977). The latter also studied Pharbitis nil (morning glory), Zea mays (maize) and Sorghum vulgare (sorghum). Investigations were also carried out on Helianthus annuus (sunflower) by OMASA et al. (1980) and SHIMIZU et al. (1980). SHIMIZU et al. (1980) observed its growth behavior at different pollutant concentrations. FURUKAWA et al. (1980) listed the damage caused to the leaves of 25 herbaceous plant species following SO2 exposure, and measured the changes in transpiration rates. KATASE et al. (1983) provide data on the responses of three C4 and three C3 plants with respect to photosynthesis and transpiration. Their results throw light on the absorption of SO2 by the leaves. YAMAZOE & MAYUMI
(1977) report on the effects of SO2 pollution on the chlorophyll content of Nicotiana tabacum (tobacco).
Exposure to O3
A comprehensive study on the effects of ozone on the epidermis, chloroplasts, ribosomes and mitochondria in leaves of Pharbitis nil (morning glory) was conducted by NOUCHI et al. (1977). In a later study, NOUCHI and AOKI (1979) assessed leaf damage in Pharbitis nil induced by exposure to various O3 concentrations.
The response of Oryza sativa (rice) was studied by FUJINUMA & AIGA (1980), NAKAMURA & OTA (1975 and 1977) and YAMAZOE & MAYUMI (1977). The observed deleterious effects of fumigation were assessed, examined under the microscope, and correlated with the physiological parameters of photosynthesis and chlorophyll and protein content. YAMAZOE & MAYUMI (1977) also used Nicotiana tabacum (tobacco), Spinacia oleracea (spinach) and Zea mays (maize) for their fumigation experiments.
Exposure to NO2
YONEYAMA et al. (1980) describe the influence of NO2 on leaf surfaces and the drymatter weights of leaves, shoots and roots. They exposed Helianthus annuus (sunflower), Zea mays (maize), Phaseolus sp. (bean), Cucumis sativus (cucumber), Solanum Iycopersicum (tomato) and Beta vulgaris (beet) to NO2. YAMAZOE & MAYUMI (1977) determined the extent of leaf damage and the protein, nitrogen and sulfur contents in Zea mays (maize) after NO2 fumigation.
MATSUSHIMA (1977) exposed various tree species to NO2 and rated them in order of their sensitivity. In the case of zelkova, he also studied the effects of nitrogen dioxide on the microscopic structures of the cells.
Exposure to ethylene
After carrying out fumigation experiments, MATSUSHIMA (1977) rated a group of herbaceous plants according to their sensitivity to ethylene.
Exposure to dust
Another important aspect of pollution dealt with in these studies of biological indication is dusting of plants, especially with cement dust, which has been investigated most thoroughly by Indian researchers. SINGH & RAO (1978 and 1981) exposed wheat to cement dust in the laboratory. The dust treatments were performed in an open-top chamber in order to eliminate wind-induced drifting. Dust was applied at the rate of 7g/m³/d. Productivity, transpiration rates and chlorophyll contents were studied under the influence of the cement dust. The studies revealed a clear linear relationship between the amount of dust applied and the responses of the plants.
PERIASAMY & VIVEKANANDAN (1982/lndia) concerned themselves with the morphological and physiological effects of coal particle pollution on various angiosperms. They investigated the number of stomata, chlorophyll and carotenoid contents, and the transpiration activity of Calotropis giganta ("aak"), Leucas aspera (Labiatae), Tephrosia purpurea ("pila"), Croton sparsiflorus (Euphorbiaceae), Prosopis spicigera ("sami tree" or "sacred tree") and Boerhauvia diffusa ("peta-sudupala"). The specimens for the test were obtained from the immediate surroundings of a locomotive shed and from a control area which is not described in greater detail. The experiments showed that the responses of the selected plants to coal particle pollution varied greatly. While Calotropis, Leucas and Tephrosia suffered greater damage, the changes observed in Croton were minimal, and Prosopis and Boerhaavia were not affected at all.
<section>2.2 Active monitoring</section>
2.2.1 Cumulative bioindicators
2.2.2 Sensitive bioindicators
Active monitoring is the term used to refer to fumigation of uniform plant material in the field under largely standardized conditions. The plants for fumigation are raised in uncontaminated soil of standardized, uniform characteristics. They are subsequently placed in the field in pots or containers. The use of cloned individuals permits the number of specimens per site to be kept relatively low. Either cumulative or sensitive biological indicators can be used. The choice depends on which atmospheric pollutants are to be tested for.
Plant species used as bioindicators are characterized by high sensitivity to air pollutants or ability to accumulate contaminant(s). One of the major advantages of active monitoring is that physiology and ecology of the indicator plants are well known. Reactions to environmental stress are easier to evaluate with these exposed plants than the reactions of the local flora.
2.2.1 Cumulative bioindicators
Active monitoring with cumulative bioindicators was carried out with trees, herbs and grasses.
FANG CAI-GIN & DUAN JI-GUANG (1982/China) carried out trials with potted specimens of the Japanese pagoda tree (Sophora japonica), two other Sophora species, and one Populus (poplar) and one Pinus (pine) species in industrial areas of the city of Beijing with differing pollution levels. The Latin designations of the species used are not indicated in the Chinese text, for which reason it is not possible to accurately identify them here. Information provided on the conditions and duration of fumigation is also insufficient.
Afterwards the sulfur content of the dustfall on the leaves and of the leaves themselves was determined. Measurements of the SO2 concentrations in the air were not carried out.
Where high sulfur contents were measured in the leaves, the authors concluded that the trees in question had a high filtering capacity, and consequently that this served to reduce the sulfur levels in the air. This conclusion must be regarded critically, however.
Another study is from India (EIAS/1/19851986), and is concerned with lead pollution from automobile exhaust in New Delhi. Once a month, the SO2, NO2, dust and lead pollution of the air at traffic intersections with varying traffic densities were measured analytically. At six selected sites, Cynodon dactylon (devil grass), Alstonia scholaris (alstonia), Nerium indicum ("kaner" = a dense shrub) and Eugenia jambolana ("jamun" = a tree species) were exposed. The Cynodon dactylon plants failed within just a few days, however, due to nibbling by rodents. No information is provided on the fumigation conditions or on whether the water supply of the plants was standardized, which is an important aspect. On the basis of the lead contents measured in the soil and in the plants, as well as biomass, chlorophyll content and leaf surface area of the individual plant species at the different sites, a "lead pollution tolerance index" (LPTI) was calculated. It was not possible to establish
any correlation between traffic density and the lead content of the plants. It did emerge, however, that the tree Eugenia jambolana and the dense shrub Nerium indicum, due to their high accumulation capacity, are effective filters and suitable for planting along roadsides.
2.2.2 Sensitive bioindicators
DUN WAN-RU et al. ( I 985/China) were able, using a nucleolus test with Tradescantia cells, to demonstrate the lead pollution caused by a factory producing dry-cell batteries. The mutagenic effect of lead can be quickly and simply diagnosed by determining the nucleolus frequency.
Since only fragments of the original Chinese article are available, it is not possible to provide any further details on the method used.
YIAN LI-YING et al. (1985) carried out active monitoring with plants of varying sensitivity to sulfur dioxide in the immediate vicinity of a sulfur factory, and in an unpolluted control area. The plants used as indicators were Pittosporum tobira (hedge laurel), Rhododendron simsii (rhododendron), Nerium indicum ("kaner"), Michelia alba (Magnoliaceae) and Eucalyptus maculata (a eucalypt). After 45 days they observed visible signs of damage, analyzed the sulfur content of the leaves, and used electrophoresis to determine the number of peroxidase isoenzymes. They also used analytical means to measure the SO2 concentration in the air, and recorded weather and microclimatic factors.
Table 1: Sites selected for phytomonitoring of ambient air quality around a fertilizer factory in Bombay, using Ipomoea carnea.
Site No.
Site
Description in brief
I
Research center
Green area treated as control. South of factory.
II
Training institute
Southwest of factory; stacks not in wind direction.
III
Effluent treatment plant
North of stacks; not in wind direction.
IV
Ammonium nitrophosphate plant(ANP1 )
In the downwind direction on the eastern side and near the stack.
V
Ammonium nitrophosphate plant(ANP2 )
20 m south of site IV.
VI
Trainee hostel
In the downwind direction on the eastern side, about 500 m away from the stack.
VII
Collectors' colony
In the downwind direction on the eastern side and500 m east of site IV.
VIII
Highway gate No. 111
Fairly green area, to the north of the factory com plex.
It turned out that Rhododendron responded sensitively. Nerium and Pittosporum, by contrast, proved to be resistant to sulfur dioxide pollution, as evidenced by their external symptoms, the sulfur content of the leaves, and the numbers of isoenzymes.
VARSHNEY (1985/lndia) presents a pollen germination test as a suitable method of active monitoring with sensitive indicator plants. Numerous fumigation experiments showed that pollen grains are more sensitive to emissions than the assimilation organs. Within just a few hours, exposure to atmospheric contaminants results in a reduced pollen germination rate and diminished pollen tube growth.
CHAPHEKAR et al. (1985/lndia) carried out active monitoring in the area around a fertilizer factory in Bombay using the ruderal plant Ipomoea carnea. This plant species is readily available and can be easily propagated by means of cuttings; moreover, it responds sensitively to air pollution.
The authors gathered plant material at eight different polluted sites in the city (Table 1) and weighed the dry matter of the individual specimens (Figure 1).
Here, too, the authors express criticism of the lack of standardization. In additional studies they intend to optimize the procedure.
Very extensive active monitoring with a sensitive bioindicator was carried out by BORALKAR & MUKHERJEE (in press/India). The indicator plant used was Medicago sativa (alfalfa), which was exposed at five sites in New Delhi with varying levels of air pollution, under controlled conditions which are not described in detail. After 21 days, shoot length, oven-dry weight and soluble sulfate content were measured. All three parameters underwent distinct changes as a result of the air pollution. The extent to which they changed corresponded to the physically measured levels of atmospheric contamination (SO2, NO2, dust particles and sulfur deposition). The reduction in shoot growth and dry matter and the increase in sulfur content of the foliar material, all expressed as percentages, were used to derive an "Air Pollution Index" (API). The API is thus intended to be a measure of the level of air pollution. It is depicted graphically as a circle, the radius of which is proportional to
the API of Medicago sativa at that particular measuring site (Figure 2).
The authors of the study point out the difficulties associated with tending the measuring stations and with providing the exposed plants with a uniform supply of water. However, they exclude the possibility of the growth parameters being inhibited primarily by lack of water.
<section>2.3 Passive monitoring</section>
2.3.1 Cumulative bioindicators
2.3.2 Sensitive bioindicators
In this approach as well, the sensitive or accumulating properties of plants with respect to atmospheric pollutants are utilized. Deviations from the normal behavior of flora growing at a given site (wild, crop or forest plants) are observed and analyzed.
Repeated vegetation mappings can also be described as a kind of passive monitoring. Such measures include the making of maps and lists of species, and descriptions of distribution patterns. One special technique involves mapping the cryptogamic vegetation of an area; if the sensitivities of the individual species are known, a correlation can be established between the degree of atmospheric pollution and the distribution of moss and lichen species.
In the studied developing countries, passive monitoring techniques were used far more frequently than active monitoring procedures.
In the following, all of the relevant publications are grouped together according to bioindicator type and the principal sources of emissions, irrespective of country of origin. Greatest attention has clearly been focused on SO2 and F pollution by industry, as well as on lead and particulate contamination from automobile traffic.
2.3.1 Cumulative bioindicators
Industry
FANG CAI-GIN & DUAN JI-GUANG (1982/China) analyzed sulfur concentrations in the leaves of various tree species in industrial areas with varying pollution levels in the city of Beijing.
YIAN LI-YING & ZHU TIANJI (1983/China) also measured the sulfur content of the leaves of four different plant species at 18 sampling sites in the city of Guang Zhou, and subsequently divided the city up into four zones on the basis of a calculated sulfur content index (IPC):
I: IPC < 1.0
clean
II: IPC between 1.0 and 1.5
lightly polluted
III: IPC between 1.5 and 2.0
moderately polluted
IV: IPC > 2.0
heavily polluted
Similar studies were carried out by CHEN QINGNAN (1984/China) in the city of Tianjin, and SONG et al. (1988) in Shanghai.
MEENAKSHY and coworkers (1981/lndia) investigated fluoride accumulation in forage plants, in particular Cynodon dactylon (devil grass), in the vicinity of a phosphatic fertilizer factory. Over an extended period of time, fluoride levels in the ambient air and in the plants were periodically determined. The test sites were chosen in such a way that the plants growing there were subjected to different levels of pollutants at different times of the year, depending on the prevailing wind directions. The studies yielded a clear correlation between atmospheric fluoride contamination and the fluoride content of the plants (Figure 3).
CHENG DONG-JI et al. (1983/China) used three relatively insensitive tree species to assess the atmospheric burden in the city of Hang Zhou. Under standardized conditions, Ligustrum lucidum (privet), Cinnamomum comphora (camphor tree) and Platanus acerifolia (plane tree) were tested at a height of 5 m above the ground and in three different directions. In addition, the atmospheric fluoride content was determined by mounting alkaline collector traps in the selected trees, also at a height of 5 m above the ground, and measuring the amount of adsorbed fluoride after I month. The fluoride content of the plant tissue was measured with an ion-selective electrode following treatment with perchloric acid.
There was a strong correlation between the fluoride content of the leaves and that of the air. The authors were thus able to show that the pollutant content of the leaves could be used to monitor atmospheric quality with respect to fluoride pollution.
GAO DE & LIU HUANZHI (1985/China) and SHI GUANG (1986/China) used a similar approach to determine the fluoride content of the atmosphere and plants in the immediate vicinity of iron and steel works in Baoutou. The fluoride contents measured in the leaves had a clear positive correlation with atmospheric fluoride pollution. However, SHI GUANG's endeavors were primarily directed towards identifying tree species which are particularly tolerant of fluoride and therefore suited for planting in the city.
SUCKCHAROEN (1980/Thailand) measured the mercury content of various food plants in order to determine the extent of mercury contamination emanating from a caustic soda factory (TACSCO) (Table 2). In the course of his investigations he was able to observe a "chimney effect". For instance, he found less mercury in samples of Sporobolus virginicus taken from directly next to the factory than at a short distance from it. It is not apparent from the article at what distances from the factory the other plant samples were taken. Neither is any detailed information provided on the control area.
PARTHASARATHY et al. (1975/lndia) investigated the effect of dust emitted by a cement factory on the physical properties of the soil and spike production of maize plants. It emerged that the cement dust had a significant deleterious effect on the production of maize spikes. The authors attributed this to diminished photosynthesis by the maize plants as a result of dust accretion on the assimilation organs.
Automobile exhaust
WONG & TAM (1978/Hong Kong) used two different species of brassica (Brassica alboglabra and Brassica parachinensis) as cumulative bioindicators for detection of lead contamination caused by road traffic.
Table 2: Mercury content (on dry-weight basis) in the leaves of plants from the TACSCO area and from the control area.
Species
TACSCO area
Control area
Leucaena glauca (horse tamarind)
Coccinia indica (small gourd)
Psidium guayava (guava)
Solanum melongena(eggplant)
Morinda citrifolia(Indian mulberry, brimstone tree)
Sporobolus virginicus (grass) Distance from the factory
5m
10 m
20 m
45 m
At various distances from a major thoroughfare, soil and plants were sampled and atomic absorption spectroscopy used to determine their lead content. The plant samples were differentiated into leaves, shoots and roots that were unwashed, washed with distilled water, or cleaned with a detergent (Figure 4).
HO & TAI (1979/Hong Kong) demonstrated the importance of leaf surface characteristics for the propensity of plants to trap airborne pollutants. They also established the relationship between meteorological factors, in particular rainfall, and the degree of leaf surface contamination - Alocasia odora (Araceae) for example possesses smooth, ceraceous leaves, while those of Mikania guaca ("17-miles-a-minute") are covered with hairs (Figure 5).
Taking an approach similar to that of WONG & TAM, AGRAWAL et al. (1980 and 1981/India) determined lead contamination levels caused by automobile exhaust in Baroda. However, no precise information is supplied on the plant species used.
ZANG CHUN-XING et al. (1984/China) used the lead levels measured in poplars, willows and locust trees to divide the city of Shenyang into four zones (seriously polluted, polluted, lightly polluted, relatively clean).
BORALKAR et al. (in press/lndia) investigated the increase in atmospheric lead levels caused by automobile emissions in New Delhi during the IXth Asian Games, which lasted from November 19 to December 4, 1982.
During the months of October, November and December, they took samples of Nerium indicum ("kaner") and Eucalyptus rostrata (a eucalypt) at seven selected traffic intersections. At the beginning of the games in November a clear increase in the lead concentrations in the leaves was recorded (Figure 6; based on Nerium indicum samples). In December the values dropped off again drastically.
2.3.2 Sensitive bioindicators
Industry
In the surveyed articles, four principal methods are described for delimitation of the area affected by pollutants emitted by a given source.
Phytosociological studies in combination with soil analysis were carried out (WONG, 1978/Hong Kong), macroscopic evaluations of visible damage were performed, in part combined with quantitative analysis of pollutant levels (BORALKAR, 1980/lndia; CHAPHEKAR, 1972/lndia and DENG RUIWEN, 1985/China); and physiological parameters and decreases in yields were investigated (SINGH & RAO, 1980/lndia; LAL & AMBASHT, 1981/India and HE YANLING & JIA XIU-FENG, 1986/China). Most of these studies involved morphological and microscopical examination, with attention focusing on leaf surface characteristics and epidermal cell types.
Table 3: The results of soil analysis and the distribution of plant species along transects I and II.
Distance from the factory (m)
Transect I
pH
Soluble sulfate (ppm)
Ground coverage of plants (%)
Transect II
pH
Soluble sulfate (ppm)
Ground coverage of plants (%)
WONG (1978/Hong Kong) performed vegetation mappings along two transects with differing degrees of exposure to a pollution source (Figure 7). He collected data on how the distribution of plant species changed at varying distances from the SO[2] source (5-100 m) and at differing orientations with respect to the source. Parallel to this, WONG recorded the damage sustained by plante and carried out soil analyses (Table 3). In addition, he carried out a greenhouse experiment to determine the effect of soil collected from the site on growth of Solanum lycopersicum (tomato) and Phaseolus mungo (mung bean).
Macroscopically visible damage to vegetation caused by fluoride pollution was assessed by BORALKAR (1980/lndia) along a transect 500 m long and 3 m wide extending out from a glass factory. The degree of damage at each point was assigned to one of four categories:
"S" slight: less than 25% of the leaf surface area is damaged
"M" moderate: 26-50% of the leaf surface area is damaged
"H" heavy: 51-74% of the leaf surface area is damaged
"C" complete: 75% or more of the leaf surface area is damaged
He observed that the crowns of the surveyed mango and Ficus trees had not grown toward the glass factory. The fluoride content of the ambient air and the plants was not measured, however.
CHAPHEKAR (1972/India) proceeded in a similar way to delimit the contamination caused by a fertilizer factory.
Both were only able to draw the conclusion that the responses of the plants to fluoride contamination varied widely.
DENG RUI-WEN (1985/China) measured the fluoride levels in the air, the soil and plant samples (Prunus persica (peach), Prunus armeniaca (apricot), Triticum aestivum (wheat) and the bulbs of scallion and garlic) and evaluated leaf damage within a radius of 4,000 - 7,500 m from the contaminant source (an aluminum foundry), and on the basis of the results divided the area into four zones of differing pollution levels, thus defining the environmental impact of the source. There was a direct correlation between atmospheric fluoride levels and leaf damage and fluoride content of the plants.
Reductions in yield and physiological parameters, in particular chlorophyll content, were used by SINGH & RAO (1980/India), LAL & AMBASHT (1981/India) and HE YAN-LING & JIA XIU-FENG (1986/China) to evaluate various environmental burdens caused by industrial emissions.
SINGH & RAO determined the influence of cement dust on the chlorophyll content, biomass and grain quality of Triticum aestivum (wheat) (Figure 8). They were able to establish a positive correlation between growth of the plants and the distance from the source of contamination. LAL & AMBASHT measured the following reductions in chlorophyll, biomass and leaf sizes caused by fluoride pollution in Diospyrus melanoxylon (ebony tree of southern India), the leaves of which are used in India for manufacture of aromatic cigarets (Figure 9).
AHMAD and YUNUS (1985/lndia), in their publication "Leaf surface characteristics as indicators of air pollution", provide an extensive survey of studies conducted using light or scanning electron microscopes at the National Botanical Research Institute in Lucknow (India) on the effects of air pollution on leaf surface structures (JAFRI et al., 1979; KULSHRESHTHA et al., 1980; SRIVASTAVA et al., 1980 and 1982; YUNUS and AHMAD, 1980 and 1981; YUNUS et al., 1979 and 1982).
On the basis of the results of these studies, they recommend using the micromorphological leaf characteristics and their modifications as indicators of air pollution as listed in Table 4.
YUNUS et al. (1979) examined, among other tissues, the epidermis of Ricinus communis (castor-oil plant) populations in four different pollution areas and one control area. A scanning electron microscope was used to determine the frequency of stomata, epidermal cells and idioblasts, stomatal size, and the stomatal index (Is).
Table 4: Modifiable leaf surface traits and their responses to air pollution.
Trait
Indication
Epicuticular wax
Deposition, ornamentation (tubes, rods, granules and plates)
Cuticle
Thickness, configuration of striations, folds, leaching, etc.
Epidermal cells
Frequency; size; cell wall thickening; cell injury, necrotic lesions; particulates,
crystals
Stomata
Frequency; size; abnormal, degenerated/aborted stomata; size of openings
Trichomes
Frequency; size; degeneration or disorganization
Special features
Idioblasts (size, shape and frequency); cystoliths (size, shape and frequency)
IS = S x 100 / (E + S)
S = number of stomata
E = number of epidermal cells
The work with the electron microscope was done in England, however.
DEBNATH & NAYAR ( I 983/lndia) also studied the effect of gaseous emissions on the number and size of stomata in nine different tree species.
MISHRA (1982) observed morphological changes (in the shoot length, leaf surfaces and fruit sizes) and modifications of the epidermis (trichome length and density, stomatal frequency and size) in two Commelina hengalensis ("Diya-meneriya") populations in two areas in Kanpur with different levels of SO2 pollution (Figure 10).
BHIRAVAMURTHY et al. ( I 985/lndia) used different staining techniques for microscopic examination of changes in the epidermis of Cassia tora ("peti-tora" or "sennes") (an annual herbaceous mesophyte) and Pergularia daemia (Asclepiadaceae) (a perennial succulent) that had been exposed to emissions from a fertilizer factory. The leaf characteristics studied were:
- Specific weight per unit area (mg/cm2)
- Leaf thickness (mm)
- Thickness of epidermis (mm)
- Thickness of cuticle (mm)
- Stomatal frequency, stomatal index and stomatal size
- Frequency of epidermal cells
- Frequency of abnormal and dead cells
The authors characterized the chosen methods as being cost-effective, easy to perform, and yielding clear results, being effective for determining the extent of air pollution in large parts of a given area; however, they failed to take into account the importance of orographic, edaphic and climatic factors.
Automobile exhaust and particulate pollution in urban areas
For the purpose of assessing the degree of contamination in the city of Seoul, LEE et al. ( 1982/South Korea) performed a mapping of lichens within the urban zone. The area was divided up into a grid of squares measuring 4 x 4 km, and the incidence of lichens on trees was recorded. 10 to 20 trees with a bole diameter of > 20 cm were studied in each square. Since it was not possible to apply the IAP method and the ecological index Q for procedural reasons, the authors drew up their own 4-point rating scale:
0: No lichens present
1: Low frequency, individual lichen individuals very small
2: Frequency high, but individuals small
3: High frequency and large lichen thalli
10 lichen families with a total of 13 genera and 20 species were found in Seoul. Of the 80 surveyed squares, 10 had no lichens at all.
In 1979, automatic SO2 gas analyses were carried out at 14 sites in the city. The results are depicted in Figure 11. A comparison with the map of lichen zones showed that lichens with a normal threshold value of around 30 ppb of SO2 occurred in the study areas with a SO2 concentration of 100 ppb. The authors speculated that orographic factors had not been taken into account sufficiently when measuring the SO2 concentrations, and call attention to the fact that the lichens could be utilized for more reliable long-term monitoring of air pollution levels.
THROWER (1980) proceeded in a similar way in Hong Kong. By applying the method advanced by GILBERT (1974), but with a simplified rating scale, he was able to show that the distribution of tropical lichen species is clearly influenced by the presence of power plants and heavy industry. As in the temperate climatic zones, the vitality of lichens and the number of lichen species increased at greater distances from contaminant sources.
LI DENG-KE (1986/China) investigated the possibility of utilizing liverworts for monitoring the air quality in Shanghai. He mapped the number of liverwort species occurring in areas of the province with different air pollution levels. In all, 39 liverwort families were identified in the study area, with 87 genera and 154 species. In less heavily polluted zones up to 55% of these species were observed, while only 13 - 18% of them occurred in the city center and in industrial areas.
The author points out that it is not yet possible in China to carry out analytical measurements on the scale which would be necessary in order to monitor the quality of the air. Consequently, because of the low costs involved and the high sensitivity of the plants, liverwort mappings represent a suitable method of assessing air pollution.
BHATNAGAR et al. (1985/lndia) and VORA et al. (1986/India) carried out experiments in the urban district of Ahmedabad with the aim of identifying plant species which are sensitive and resistant to urban and industrial particulate contamination. While BHATNAGAR and coworkers investigated the chlorophyll content of the leaves of 9 different arboreous plants as a function of the intensity of particulate pollution, VORA et al. studied the same plant species in order to determine the effect of dustfall on soluble sugar content. For 4 of these plant species, Table 5 and Figure 12 illustrate the relationship between leaf surface characteristics and the ability of the plants to trap or filter out dust particles from the air.
Table 5: Filtering ability and sensitivity to particulate contamination of four different plant species.
Plant species
Leaf position Leaf surface
Filtering ability
Sensitivity
Aelianthus excelsa
horizontal
high
sensitive
(Simarubaceae)
hairy
Ficus religiosa (fig tree)
glabrous
low
sensitive
Cordia myxa (Boraginaceae)
horizontal
low
sensitive
Nyctanthus arbortristis ("night-flowering jasmine")
hairy
high
insensitive
<section>3. Summary in table form of the surveyed publications</section>
On the following pages, all of the surveyed publications are compiled in the form of a table, separately for each country.
The publications are organized according to the different monitoring approaches and bioindicator types used.
<section>3.1 India</section>
Active monitoring
Cumulative bioindicators:
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Cynodon dactylon
Lead;
Pb content in plants and
EIAS/1/1985-1986
Alstonia scholaris
Automobile
soil, biomass, leaf,
New Delhi
Nerium indicum
exhaust
surface,
Eugenia jambolana
chlorophyll content
Sensitive bioindicators:
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Medicago sativa
SO2, NO2 and
Biomass, length growth,
BORALKAR &
particulates
sulfur content
MUKHERJEE in press
New Delhi
Various species
General
Pollen bioassay,
VARSHNEY 1985
pollen germination,
pollen tube growth
Ipomaea carnea
Fertilizer factory
Biomass
CHAPHEKAR et al. 1985
Bombay
Passive monitoring Cumulative bioindicators:
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Zea mays
Cement dust;
Leaf surface, growth
PARTHASARATHY et al.
cement factory
height, size and number
of spikes,
water capacity,
thermal
conductivity and
pore size
distribution of the soil
Various
Lead;
Pb content in
AGRAWAL et al.
unspecified
Automobile
plants and soil
1980 a+b
species
exhaust
Baroda city
Nerium indicum
Lead;
Pb content of leaves
BORALKAR et al.
Eucalyptus
Automobile
New Delhi
rostrata
exhaust
Cynodon dactylon
Fluoride;
Fluoride content in
MEENAKSHY et al. 1981
Phosphate
air and plant
Bombay
fertilizer factory
samples
Sensitive bioindicators.
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
All site
Fertilizer
Assessment of
CHAPHEKAR 1972
vegetation
factory
macroscopically
visible damage
Fluoride;
BORALKAR in press
Glass industry
Karad, Maharashtra
Diospyrus
Fluoride;
Biomass, leaf surface,
LAL & AMBASHT,
aelanoxylon
Aluminum factory
chlorophyll content
Triticum aestivam
Cement dust;
Qualitative and
SINGH & RAO 1980
Cement factory
quantitative grain analysis,
biomass, chlorophyll
content
Calotropis procera
Particulates
Chlorophyll a, b
BHATNAGAR et al. 1985
Aelianthus excelsa
Dustfall
Ahmedabad
Nyctanthus
arbortristis
Ficus religiosa
F. bengalensis
F. drupacea
Polyalthia longifolia
Cordia myxa
Terminalia catappa
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Calotropis procera
Particulates
Sugar content
VORA et al. 1986
Aelianthus excelsa
Dustfall
Ahmedabad
Nyctanthus
arbortristis
Ficus religiosa
F. bengalensis
F. drupacea
Polyalthia longifolia
Cordia myxa
Terminalia catappa
Mangifera indica
General Industry
Microscopic studies
DEBNATH & NAYAR
Ficus bengalensis
Ficus religiosa
Psidium guayova
Syzygium jambos
Artocarpus
integrifolia
Minusops elengi
Alstonia scholaris
Polyalthia
longifolia
Commelina
SO2 and coal dust;
Morphologic and
MISHRA 1982
bengalensis
Coal-fired power plant
microscopic studies
Kanpur
Cassia tora
SO2, H2S,
Microscopic studies
BHIRAVAMURTHY et al.
Pergularia daemia
NO2;
of leaf epidermis
Fertilizer factory
Ricinus communis
H2S, CH4;
Scanning electron
YUNUS et al. 1979
Sewage canal
microscope studies
of epidermal traits
<section>3.2 China</section>
Active monitoring
Cumulative bioindicators:
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Various tree species,
SO2
Sulfur content of leaves,
FANG CAI-GIN & DUAN
incl.:
dust accretion
JI-GUANG 1982
Sophora japanica
Beijing
Sophora spp.
Pinus spp.
Sensitive bioindicators.
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Tradescantia sp.
Lead;
Nucleolus test,
DUN WAN-RU et al.
Industry
frequency of nucleoli
Petunia hybrida
SO2;
Assessment of leaf
JIANG MEI-ZHEN
Pelargonium
Oil refinery
damage
hortorum
Begonia
semperflorens
Dianthus barbatus
Euphorbia
pulcherrima
Tulipa gesneriana
Hyacinthus
orientalis
Pittosporum tobira
SO2;
Assessment,
YIAN LI-YING et al.
Rhododendron
Sulfur factory
sulfur content,
simsii
peroxidase and
Nerium indicum
isoenzyme contents
Michelia alba
(electrophoresis)
Eucalyptus
maculata
Passive monitoring
Cumulative bioindicators:
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Trees*
General
Infrared photography,
CHEN QINGNAN 1984a
sulfur, fluoride and
Tianjin
chloride contents,
pH values of bark
Populus spp.
Lead
Pb content of leaves
ZANG CHUN-XING et al.
Salix spp.
1984 Shenyang
Robinia spp.
Various tree
SO2
Sulfur content of leaves,
FANG CAI-GIN & DUAN
species, incl.:
dust accretion
JI-GUANG 1982
Sophora japanica
Beijing
Sophora spp.
Pinus spp.
Trees
SO2
Sulfur content of leaves
CHEN QINGNAN 1984b
Tianjin
Not specified
SO2
Sulfur content of leaves
YIAN LI-YING & ZHU
TIANJI 1983
Guang Zhou
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Platanus
Lead, Copper,
Heavy metal
SONG, YONGCHANG
acerifolia
chromium, Zinc
content of
GO, YONGJIE 1988,
bark and leaves
Shanghai
Herbaceous plants
Fluoride;
Fluoride content in air
GAO DE & LIU
Iron and steel
and plant samples
HUANZHI 1985
industry
Baoutou
Various tree species
SHI GUANG 1986
Ligustrum lucidum
Fluoride,
Fluoride content in
CHENG DONG-JI et al.
Cinnamomum
Steel, glass
air and plant samples
comphora
and thermos
Hang Zhou
Platanus
container
acerifolia
industry
No additional information is provided in the available articles
Sensitive bioindicators:
Plant species
Pollutant(s)
Methods and/=
Authors
and/or source
parameters
Study area
Liverworts
General
Mapping
LI DENG-KE 1986
Shanghai
Salix motsudana f.
HCl, SO2;
Carbohydrates
HE YANG-LING &
pendula
Electrolyte
JIA XIU-FENG 1986
Ulmus pumila
and steel factory
Acer negundo
Prunus persica
Fluoride;
Fluoride content in ah,
DENG RUI-WEN 1985
P. Armeniaca
Aluminum
soil and plant samples
Lanzhou
Allium ascalonicum
Allium sativum
<section>3.3 Hong Kong</section>
Passive monitoring
Cumulative bioindicators:
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Alocasia odora
Lead;
Pb content of plants
HO & TAI 1979
Mikania guaco
Automobile exhaust
Brassica
Lead;
Pb content in soil and
WONG & TAM 1978
alboglabra
Automobile exhaust
plant samples
B. parachinensis
Sensitive bioindicators:
Plant species
Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
All site vegetation
SO2; Sulfur factory
Mapping, assessment,
WONG 1978
soil parameters
Lichens
General Industry
Mapping
THROWER 1980
<section>3.4 Other countries</section>
Passive monitoring Cumulative bioindicators:
Plant species Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Site vegetation Mercury
Hg content of
plants
SUCKCHAROEN 1980
Thailand
Sensitive bioindicators:
Plant species Pollutant(s)
Methods and/or
Authors
and/or source
parameters
Study area
Lichens SO2
Mapping
LEE et al. 1982
South Korea
<section>4. Conclusions</section>
Active monitoring is clearly underrepresented in the surveyed countries. Only 22 - 26% of the publications from India and China deal with this approach to bioindication, and no studies at all on this aspect are available from Hong Kong, Thailand or South Korea. The problems involved are apparently associated with technical aspects of monitoring the established measurements stations and with the required standardization of procedures. In one study involving only 5 measurement sites, the authors (BORALKAR & MUKHERJEE, in press/lndia) pointed out the difficulties posed by management and supervision, and in particular the problems involved in providing a uniform water supply to the exposed plants. On the whole, insufficient information was supplied on fumigation conditions (FANG CAI-GIN & DUAN JIGUANG 1982/China, EIAS/1/1985-1986/lndia and CHAPHEKAR et al. 1985/India).
Equally little attention was paid to hydrocarbons and to photochemical oxidants. The latter class of pollutants comprises a special case in the sense that no component storage takes place. The extent of contamination can only be evaluated by using active monitoring to observe the incidence of typical symptoms.
A far larger number of publications deals with passive monitoring. This approach was used mainly to assess certain kinds of pollution within narrowly defined areas, serving to delimit and characterize the zone of influence of a contaminant source or to identify areas or urban zones with differing degrees of pollution. In some of the articles, information was given on the ability of individual plant species to filter out heavy metals, particulates or cement dust, and their potential significance for helping to prevent health hazards for humans discussed (FANG CAI-GIN & DUAN JI-GUANG, 1982/China; EIAS/1/1985-1986/lndia; BHATNAGAR et al. 1985/India; and VORA et al. 1986/lndia). The problem of bioconcentration of contaminants in the nutrient cycle was also dealt with (MEENAKSHY et al. 1981/lndia and SUCKCHAROEN 1980/Thailand).
The techniques and methods used correspond largely to those used in western industrialized nations. In a few cases, coauthors from western countries participated (YUNUS, AHMAD and GALE, 1979/lndia), the studies were conducted by foreign scientists in an Asian country (THROWER 1980/Hong Kong), or the inspiration for conducting the study in the first place was obtained by the author during a stay abroad (LEE et al. 1982/South Korea and SUCKCHAROEN 1980/Thailand). In some cases, the chemical analyses (SUCKCHAROEN 1980/Thailand) and electron-microscopic examinations (YUNUS et al. 1979/India) were carried out in Europe or North America.
The focus was on measurement of yields, assessment of macroscopically visible damage, morphological studies, light- or electron microscopic examinations, chemical analyses (of heavy metals, fluoride and sulfur content), and physiological measurements. In this context it should be noted that analysis of physiological parameters for assessment of the pollution situation can only be recommended if the stress factor "transport to the measuring station" can be eliminated. It is not apparent from the articles whether sufficient consideration was given to this aspect.
Only a few lichen, moss and liverwort mappings were carried out. However, THROWER (1980/Hong Kong) was able to show with his studies that the response of tropical lichen species to atmospheric pollution is similar to that of temperate varieties. Thus, lichen zones develop which reflect air pollution levels.
One attempt was made to utilize phytosociological mapping to obtain information on air pollution (WONG 1978/Hong Kong). It would be appropriate to continue this work by carrying out detailed research on plant successions, following the example of recent successful studies in western countries on continually observed study areas within the scope of endeavors to compile environmental impact inventories for certain pollutants.
The advantages of passive monitoring are that relatively little equipment is required and that the reactions of the bioindicators can be relatively dependably used to infer the condition of other organisms at the same site. A disadvantage of this method is that the sensitivity and ability to respond of a given plant individual is strongly dependent on its genetic disposition and on the conditions under which it has grown to maturity. For this reason, additional data is required on pollutant concentrations, the climate, soil parameters, etc., as well as information on the condition, chemical composition and reaction of the plants in order to permit interpretation of the results.
In many of the surveyed studies, an exceedingly one-dimensional approach was taken that failed to give adequate consideration to the complex functional processes of the organisms and their mutual interreactions. Two extreme examples of this are the studies by BORALKAR (1980/lndia) and CHAPHEKAR (1972/lndia). They merely assessed the leaf damage of all of the site vegetation along a transect and attributed the observed damage to pollutant emissions, without performing any chemical analyses on plant or soil samples. Climatic and soil parameters were ignored completely.
The importance of orographic and edaphic factors, climatic conditions and plant attributes - e.g. differing propensities of leaf surfaces to trap airborne particles- was only recognized and incorporated by WONG (1978/Hong Kong), HO & TAI (1979/Hong Kong) and MEENAKSHY et al. (1981/lndia).
The majority of the studies made only a first step towards fulfilling the conditions which must be met for successful analysis of air pollution over an entire area. In order to corroborate the results and facilitate their interpretation, it is essential for standardization of the test conditions to be optimized and for a comprehensive study to be made of meteorological and microclimatic factors.
Finally, on the basis of the results of numerous fumigation experiments and the Asian publications surveyed here, concrete proposals for phytomonitoring techniques can be made, in particular for active monitoring:
The reactions of Oryza sativa (rice) and Pharbitis nil (morning glory) to different pollution levels are sufficiently well known from a large number of fumigation and open-site experiments. In the studies by MATSUNAKA (1977/Japan), Pharbitis nil is utilized as a sensitive bioindicator in a passive monitoring approach. This species responds to high ozone burdens with chlorosis, necrosis and curling of its leaves. Extensive studies on the effect of O3 on its epidermis, chloroplasts, ribosomes and mitochondria (NOUCHI et al. 1977/Japan), and assessment of leaf damage following exposure to different ozone concentrations (NOUCHI & AOKI 1979/Japan), have provided additional data which permit evaluation of the potential of this plant species as a bioindicator.
A great deal is also known about the sensitivity and reactions of Oryza sativa to air pollution. FUJINUMA & AIGA (1980/Japan) established that the rice varieties Nihonbare and Kinmaze react sensitively to ozone and sulfur dioxide. Their sensitivity to NO2 is significantly lower. The effect of ozone on
Oryza sativa was also investigated by NAKAMURA & OTA (1975 and 1977/Japan). They described the macroscopic damage caused by fumigation. YAMAZOE & MAYUMI (1977/Japan) studied the effect of NO2, O3 and SO2 fumigation on rice leaves. Similar studies were performed by AGRAWAL et al. (1982/lndia). They studied chlorophyll and carotenoid contents, and assessed leaf damage after exposure to SO2.
On the basis of the results of the above-mentioned studies, it can be assumed that Pharbitis nil is suitable as a sensitive bioindicator for ozone and Oryza sativa for active monitoring of ozone and SO2. We recommend proceeding in accordance with VDI guideline 3792, sheet I (1978). This source contains both guidelines for fumigation and a description of a semiautomatic technique for supplying the plants with water.
In a large number of independently performed studies, Nerium indicum ("kaner") has demonstrated a high filtering capacity and low sensitivity to atmospheric contaminants (EIAS/1/1985- 1986/lndia; BORALKAR et al. in press; and YIAN LI-YING et al. 1985/China). Under standardized fumigation conditions, it could therefore be used as a cumulative indicator within the scope of an active monitoring approach.
<section>References</section>
INDIA
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CHINA
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DENG RUI-WEN, 1985. The effects of fluoride pollution by an Al smeltery on plants in Lan-Zhou. Acta Phytophysiologica et Geobatanica Sinica (2): 132-141.
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GAO DE and LIU HUANZHI, 1985. Influence of air fluoride pollution on herbages. Journal of Ecology (3): 5-9.
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HONG KONG
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JAPAN
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OMASA, K. et a]., 1980. Evaluation of air pollution injury to plants by image processing. In: SASA, M.: Studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Research report from the National Institute for Environmental Studies (11): 249-254.
SHIMIZU, H. et al., 1980. Effects of low concentrations of SO2 on the growth of sunflower. In: SASA, M.: Studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Research report from the National Institute for Environmental Studies (11): 9 - 17.
USHIJIMA, T. and T. TAZAKI, 1977. The influence of SO2 on the photosynthetic and transpiration rate in several higher plants. In: KASUGA, S. et a].: Proc. of IV Int. Clean Air Congress Tokyo: The Japanese Union of Air Pollution Prevention Associations: 84-87.
YAMAZOE, F. and H. MAYUMI, 1977. Vegetation injury from interaction of mixed air pollutants. In: KASUGA, S. et al.: Proc. of IV Int. Clean Air Congress Tokyo: The Japanese Union of Air Pollution Prevention Associations: 106-109.
YONEYAMA, T. et al., 1980. Absorption of atmospheric NO2 by plants and soils. V. Day and night NO2 fumigation effect on the plant growth and estimation of the amount of NO2 nitrogen absorbed by plants. In: SASA, M.: Studies on the effects of air pollutants on plants and mechanisms of phototoxicity. Research report from the National Institute for Environmental Studies (11): 31 -50.
KOREA
LEE, U.-H. ; C.W. PARK; S. K. LEE and U. H. HONG, 1982. Untersuchungen zur Bewertung der Umweltbelastung durch Flechten. Inst. f. Wissenschaft und Technik, Abt. Umwelt, Seoul, Sudkorea.
MALAYSIA
AWANG, M. and N. ZAINUN, 1985. Physiological responses of ornamental plants (Petunia spp., Ixora javanica and Cinnamon iners) to SO2 with special reference to Kuala Lumpur ambient air pollution. Symp. Biomonitoring State Environ.: 106-113.
THAILAND
SUCKCHAROEN, S., 1980. Mercury contamination of terrestrial vegetation near a caustic soda factory in Thailand. Bull. Environm. Contam. Toxicol. (24): 463-466.
GENERAL REFERENCES (see ARNDT)
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GILBERT, O.L., 1974. An air pollution survey by school children. Environ. Pollut. (6): 175-180.
STEUBING, L. and H.J. JAGER (eds.), 1982:Monitonng of air pollutions by plants. Junk Publ., The Hague.
VDI-Richtlinie 3792, Blatt 1: Verfahren der standardisierten Graskultur. VDI-Handbuch Reinhaltung der Luft, 1978.
<section>Chemical Substances and Compounds</section>
Aluminum
Al
Ammonia
NH3
Ammonium
NH4+
Antimony
Sb
Bromine
Br2
Cadmium
Cd
Calcium
Ca
Calcium fluoride
CaF2
Calcium sulfate
CaSO4
Carbon dioxide
CO2
Copper
Cu
Ethylene
C2H4
Fluorine
F2
Hydrochloric acid
HCl
Hydrogen fluoride
HF
Hydrogen sulfide
H2S
Iron
Fe
Lead
Pb
Magnesium
Mg
Manganese
Mn
Mercury
Hg
Methane
CH4
Methylmercury
HgCH3, Hg(CH3)2
Molybdates
M2 MoO4, MoO4--
Nickel
Ni
Nitrogen
N2
Nitrogen dioxide
NO2
Nitrogen oxides
NOX
Orthophosphate
PO4--, Me3PO4
Ozone
O3
Perchloric acid
HClO4; also known as Fraude's reagent
Perchlor Ethylene
C2Cl4
Phosphorus
P
Polychlorinated biphenyl
PCB.
- Normally a multitude of different PCB's, characterized by varying extent of chlorination: position and number of Cl-atoms connected to the C-atoms of the biphenyl may vary. These PCB's differ in quality and quantity of impact on living organisms. In many cases they are accompanied by other toxic substances such as dioxines.
Potassium
K
Radioactive isotope of cobalt
Co-60
Radioactive isotopes of plutonium
Pu-238 etc.
Sodium chloride
NaCl
Steranes
Cycloalkanes derived from a sterol. Any compound with one or more sulfur atoms in which the sulfur is connected directly to a carbon, metal or other non-oxygen atom; for example, sodium sulfide (Na2S)
Sulfide
S2-
Sulfur
S
Sulfur dioxide
SO2
Tin
Sn
Titanium
Ti
Tungsten
W
Zinc
Zn
<section>Glossary</section>
Acrocarpous
In some mosses of the subclass Eubrya, having the sporophyte at the end of the stem, thus exhibiting an erect habit.
Active monitoring
Cf. text by Ellenberg - Fig. 4.
Aerial
Relating to or occurring in the air or above the ground.
Alkaline collector traps
Artificial surfaces coated with an alkaline medium to absorb acidic atmospheric components.
Allochthonous nutrients
Nutrients that are transported from elsewhere into an ecosystem.
Allochthonous organic matter
Organic matter of external origin, such as fallen leaves in a brook.
Andesite
An extrusive, usually dark greyish, rock consisting essentially of plagioclase feldspar with dark ferromagnesian minerals and little or no quartz.
Angiosperms
The common name for members of the plant division Magnoliophyta.
Anion
A negatively charged atom or group of atoms, or a radical that moves towards the positive pole (anode) during electrolysis.
Aquatic system
Cf. text by Bretthauer.
Arthropods
Members of the large phylum of the Arthropoda, comprising invertebrate animals with jointed legs and a segmented body; e.g. insects, spiders and myriapods.
Assimilation
The incorporation or conversion of nutrients into protoplasm that in animals follows digestion and absorption, and in higher plants involves both photosynthesis and root absorption.
Assimilation organs
(Mainly) leaves.
Atomic absorption spectroscopy
AAS - physical method of determining heavy metal contents.
Autotrophic soil algae
Self-nourishing green algae living in soil (capable of synthesizing organic nutrients directly from simple inorganic substances).
Azonal soils
Soils that have developed under special conditions not typical of the surrounding area, mostly influenced by the action of wind and water (e.g. the soils of valley bottoms and sand dunes).
Background contamination
The natural heavy metal content in the stones and soils of an area that is being investigated to determine pollution of it with the same metals.
Bar diagram
Block diagram depicting data from measurements.
Binoculars
An optical instrument with two eyepieces.
Biochemical oxygen demand (BOD)
The quantity of oxygen that organisms need to mineralize degradable organic matter, especially in the breakdown of organic matter by microorganisms in a water body.
Biocoenosis
A community of biologically integrated and in terdependent plants and animals.
Biodegraded
Organic compounds that have been broken down by microorganisms.
Biological indication
Cf. text by Ellenberg.
Biomass
The amount of living matter (expressed per unit area or volume of habitat).
Biome
A complex biotic community covering a large geographic area and characterized by the distinctive life forms of important climax species.
Examples: tundra, taiga, tropical rain forest.
Biomonitoring
Cf. text by Ellenberg - Fig. 4.
Biota
All of the living organisms of a given region, including flora, fauna and microorganisms.
Biotope
A habitat that is uniform in its principal climatic, soil and biotic conditions (e.g. a sandy desert).
BOD
Biochemical oxygen demand (cf. above).
C/N ratio
The quantitative relation between carbon and nitrogen.
Calcination
The process of heating an organic material to a high temperature (but without fusing it) in order to drive out volatiles or affect it in some other way (e.g. oxidation or pulverization).
Canopy roughness
The unevenness or vertical geometric variations in the upper surface of a plant stand (e.g. a forest).
Carbon-14dating
A technique in which a radioactive isotope of carbon (carbon-14) is employed as a tracer in chemical and biochemical research. Because this isotope is present in all carbon-containing matter, it is useful for dating archaeological specimens, fossils, etc.
Carotenoid content
Cf. text by Arndt.
Carotenoids
Pigments that occur in plants and some animal tissues; they include carotene, xanthophylls and other fat-soluble pigments.
Catalase
An enzyme that occurs in plant and animal tissues; it decomposes hydrogen peroxide into water and oxygen.
Cations
A positively charged atom or group of atoms, or a radical that moves to the negative pole (cathode) during electrolysis.
Checkerboard pattern
A regular pattern of squares like that of a checkerboard.
Chironomids
Insects belonging to the family of slender, long winged, long-legged, small and very delicate nemotoceran Diptera, commonly called midges or true midges. They are scavengers, not blood suckers.
Chloroplasts
A type of cell plastic occurring in the green parts of plants; they contain chlorophyll pig ments and play a role in photosynthesis and protein synthesis.
Chlorosis
An abnormal condition in plants characterized by the absence of green pigments; it can becaused by lack of light or a deficiency of iron or magnesium. (Cf. text by Arndt).
Chlorotic injury
A disease condition of green plants, manifesting itself as yellowing of the green parts of a plant.
Cilicate
A single-celled animal with cilia on its surface.
Combined exposure
Exposure to different toxins in combination.
Compacted soils
Soils with few openings through which exchange of gases or percolation of water can take place.
Composite
A plant of the large Compositae family of dictyledonous plants with flower heads composed of dense clusters of small flowers surrounded by a ring of small leaves or bracts; the daisy, thistle, artichoke, chrysanthemum, etc. belong to this family.
Cumulative biological indicators
Cf. footnote to text by Ellenberg - p. 18, Fig. 4.
Coupling analysis
A special method for determining saprobity levels by using only a small number of very characteristic indicator species; only employed in Baden-Wuerttemberg (Federal Republic of Germany).
Cushion plants
Plants with globular or regularly rounded surfaces adapted to minimize water losses from transpiration, typical of high mountainous areas affected by frequent, strong winds.
Cumulative bioindicators
Cf. texts by Ellenberg and Steubing.
Cystolith
A concretion of calcium carbonate arising from the cell walls of modified epidermal cells in some flowering plants.
Defoliation
The loss of leaves in plants caused by a toxin or some other external effect.
Degradability
The decomposability of organic matter by the metabolic processes of animals or plants in the soil.
Diatoms
Unicellular algae; common name of the bacilla riophyta. Some are colonial, green or brownish in color (but all contain chlorophyll), with siliceous and often highly sculptured cell walls. They make up much of the producer level in marine and freshwater food chains, and they have contributed to the formation of oil reserves.
Dicotyls
Plants belonging to the plant class Dicotylae, all having two cotyledons, i.e. two leaves at the very early stage of life, as opposed to monocotyls.
Diffusion resistance
Stomatal resistance to exchange of gases and vapours.
Dioecious
Of plants, having the staminate and pistillate (male and female) flowers on separate individuals.
Disease vector
An animal, such as an insect, that transmits a disease-producing organism from one host to another.
Dissilimation
The disintegration of protoplasm, principally by oxidation.
Ecochemicalcomposition
The chemical composition of the surrounding environment.
Ecologicalvalence
The ranges of biological and abiotic factors within which an organism is able to live.
Ecosystem
A system made up of a community of plants, microorganisms and animals, along with their physical and chemical environment.
Ecotoxicologist
A specialist who works to determine the impacts of pollutants on the environment.
Ecotype
A biotype or a characteristic population of a species of organism resulting from natural selection in a given habitat.
Electrophoresis
An electrochemical process in which colloidal particles or macromolecules with a net electric charge migrate in a solution under the influence of an electric current; also known as cataphoresis.
Endemic
Confined to a given region and having originated there.
Enrichment horizons
Soil horizons in which salts such as lime, gypsum or clay accumulate.
Environmental impact inventory
A survey of the influence of polluting substances on the environment.
Environmental specimen
An animal or plant taken as a sample from an ecosystem for analysis. Within the scope of biological monitoring, the sample is designed so as to be representative of that ecosystem.
Epicuticular wax
The superficial layer of wax that covers leaves.
Epilothic
Of plants, growing on the surfaces of rocks and stones, e.g. algae and lichens.
Epiphyte
A plant that grows nonparasitically on another plant, deriving moisture and nutrients from the air. Also known as aerophyte. Cf. text by Steubing.
Euryhaline species
Organisms that are capable of tolerating a wide range of saline conditions.
Euryoecic
Not narrowly limited by ecological conditions. The opposite condition, when organisms are only able to live within a narrow range of ecological conditions, is called "stenoecic", e.g. a plant that does not tolerate any shade, or a trout that requires oxygen-rich water.
Eutrophication
The process by which a body of water or a terrestrial ecosystem becomes rich in plant nutrients; in this volume, reference is principally made to nitrogen and phosphorus.
Evapotranspiration
The combined evaporation of water from the soil surface and transpiration from plants.
Exposure experiments
Experiments in which organisms are exposed to certain environmental conditions, especially pollutants.
Eyrie
The nest of an eagle or other large bird of prey.
Filiform bacteria
Threadlike bacteria.
Flotation processes
The separation of the constituent particles of a mass of pulverized ore by taking advantage of their differing ability to float on a given liquid.
Foliar
Referring to leaves.
Gastropods
A large, morphologically diverse class of the phylum Mollusca, containing the snails, slugs, limpets, and conchs.
Genus (pi. genera)
A class, kind or group of organisms marked by common characteristics or by one common characteristic, specifically: a category of biol ogical classification ranking between the family and the species, comprising structurally or phylogenetically related species or an isolated species exhibiting unusual differentiation, and designated by a Latin or latinized capitalized singular noun.
Germinative capacity
The capacity to reproduce.
Gonads
Organs that produce reproductive cells, especially an ovary or testis.
Gymnosperms
The common name of members of the division Piniphyta; seed-bearing plants having naked ovules at the time of pollination. Example: pine trees.
Halobiontic
Living in water or on the bottom of a saline water body.
Halophilic
Salt-loving; thriving under saline conditions.
Halophobic
Thriving only in extremely salt-poor water; also called haloxenic.
Halophytic
Refers to shore plants capable of thriving on salt-impregnated soils.
Halophytic plant communities
Communities of plants growing on salty soils.
Hard cushion bogs
Marches or mires consisting of hard, solid cushion plants (cf. above).
Herbivorous
Feeding on plants; plant-eating.
Heterophyllous
Having more than one form of leaves on the same plant or stem.
Heterotrophic
Deriving nourishment from organic substances, e.g. parasitic plants and all animals; antonym: autotrophic.
Heterotrophic soil algae
Organisms that nourish themselves by ingesting and breaking down organic matter (these algae are not green).
Hygrophilous
Living or growing in places with moist air, in many cases on moist or wet soils.
Hymenopters
Bees, wasps and the like.
Hypertrophication
A situation in which considerably more plant nutrients are available in an ecosystem than are needed, thus leading to problems.
Idioblast
A plant cell that differs markedly in shape or function from neighboring cells within the same tissue.
In-site production
Production in position, in its original place; autochthonous production, like algae growing in a brook.
Intercostal zone
The zone between the veins or nerves of a leaf.
Ion-selective electrode
A physicochemical method of measuring ion concentrations.
Isoenzyme
Any of the electrophoretically distinct forms of an enzyme, representing different polymeric states but having the same function. Also known as isozyme.
Katabatic winds
Cold winds that drop down from high mountains to warmer valleys during the night. Also known as gravity winds.
Large-lobed foliose lichens
Lichens with large, leaf-like lobes.
Leaf necrosis
Localized death of living tissue in leaves.
Leghemoglobin
Red pigment involved in symbiotic fixation of nitrogen from the air by legumes.
Lichen thalli
A group of organisms consisting of fungi and algae growing together symbiotically.
Limnic water
Fresh water in a lake.
Limnology
The study of the physical, chemical and biological components of fresh water.
Littoral zone
The part of a lake extending from the shore down to the limit for rooted vegetation.
Liverworts
The common name for members of the Hepaticae; small plants, mostly terrestrial, attached to the substrate by rhizoids. Related to hornworts and mosses.
Lotic water
Flowing water, i.e. rivers and streams. Antonym: lentic = standing.
Macchia
A characteristic type of Mediterranean brush or scrub landscape, the result of centuries of fires and grazing by sheep and goats.
Macrophytes
Large aquatic plants, as opposed to phytoplankton and other small algae.
Marchantiales
The thalloid liverworts, an order of the class of the Marchantiopsida, having a flat body composed of several distinct tissue layers, smoother walled and tuberculate-walled rhizoids, and male and female sex organs borne on stalks on separate plants.
Metabolic changes
Chemical changes; the sum of the processes by which a given substance is dealt with in an organism.
Metabolite
A product of metabolism or a substance essential to the metabolism of a given organism or metabolic process.
Metabolization
The chemical and physical processes continuously going on in living organisms and cells, comprising those by which assimilated food is built up into protoplasm and those by which organic compounds are used and broken down into simpler substances and waste, with release of energy for all vital purposes.
Metamorphic rocks
Rocks produced by metamorphism (a change in the constitution of rock, especially a pronounced change effected by pressure, heat and water that results in a more compact and more highly crystalline condition). Example: Gneiss.
Mitochondria
Membrane-bounded particles that are present in the cytoplasm of all eukaryotic cells. Mitochondria contain enzyme systems which are responsible for providing energy in the form of ATP.
Mobilization
Enhancement of mobility.
Molybdates
Salts of molybdenum containing the group MoO4 or MoO2.
Monocotyledons
All plants of the class Liliopsida; they have a single cotyledon (the first leaf of the embryo of seed-bearing plants).
Mormyridae
A fish family, including the so-called Nile perch.
Moss bag test
Cf. texts by Steubing and Arndt.
Multiple layer palisade
Refers to leaves that have several parenchymal layers of densely packed cells containing many chloroplasts.
Mycorrhizae
Symbiotic associations of the roots of higher plants with a fungus. Singular: Mycorrhiza.
Net primary production (NPP)
The net product of photosynthetic assimilation by a green plant, minus immediate metabolic needs (in energy terms).
Nitrogen cycle
Nitrogen metabolism, atmospheric nitrogen fixation, assimilation of nitrogen into proteins and other organic compounds, and the reverse processes.
Nodules
Small knoblike structures (e.g. the nodules of grass blades).
Non-homoiothermal terrestrial
Any animal except mammals and birds. The in
vertebrates
tensity of life and activity of these animals de pends on climatic temperature conditions.
Nuclide
A species of atom characterized by the number of protons, number of neutrons, and energy content in the nucleus, or alternatively by the atomic number, mass number, and atomic mass.
Nutrient leaching
The removal of plant-available nutrients from the soil by being washed out by water.
Orache
Any of a genus of plants of the goosefoot family, widespread in salty and alkaline areas, usually having silvery foliage and small green flowers.
Orographic
Penaining to relief factors such as hills, mountains, plateaus, valleys and slopes; describing the surface of the earth.
Osmotic pressure
The applied pressure required to prevent the flow of a solvent across a membrane which of fers no obstruction to passage of the solvent, but does not allow passage of the solute, and which separates a solution from the pure solvent.
Overlapping accumulation periods
Overlapping time spans for the accumulation of toxins in plants.
Oxidophilic organisms
Organisms that live in oxygen-rich waters.
Paleozoic schists
Schists that originated in the era of geological history extending from the beginning of the Cambrian to the close of the Permian.
Parasitism
An association of two kinds of organism in which the parasite is benefited and the host is usually harmed.
Passive monitoring
Cf. text by Ellenberg - Fig. 4.
Peat horizon
Peat layer.
Pedological
Related to the soil with its living organisms, and including its water, nutrient and other physical components.
Pentacyclic triterpenes
Squalenoids; a group of organic compounds with 5 carbon rings, cf. Iist of chemicals.
Perchloric acid
Cf. Iist of chemicals.
Perioxidase
An enzyme that catalyzes reactions in which hydrogen peroxide is an electron acceptor.
Periphyton
"Aufwuchs"; the organisms attached to under water rooted plants.
Persistent halogenated hydrocarbons
Toxic compounds that are nearly impossible to metabolize, etc. DDT and PCBs.
Phenology
The study of natural phenomena that recur periodically.
Phosphatase activity
The (chemical) activity of enzymes found in body tissues and fluids, that hydrolyze phosphoric acid esters of organic compounds, liberating phosphate ions.
Photochemical oxidant
Any of the chemicals that enter into oxidation reactions in the presence of light or other radiant energy, particularly ultraviolet light.
Photochemical smog
Chemical pollutants in the atmosphere resulting from chemical reactions involving hydrocarbons and nitrogen oxides in the presence of sunlight.
Physicochemical measurement
Measurement of both purely physical and chemical properties, changes and reactions as opposed to the biological monitoring approach.
Phytomonitoring methods
Methods by which the amount and impact of pollution can be evaluated using plants as indicator organisms.
Phytosociological survey
Cf. text by Steubing.
Phytotoxicity
Poisonousness to plants.
Plant tissue
An aggregation of cells more or less similar morphologically and functionally.
Plantaginacae
The family including plantain and ribgrass.
Pleurocarpous
Having the sporophyte in leaf axils along the side of the stem or on lateral branches; refers specifically to mosses.
Pollen germination test
Cf. text by Amdt.
Pollen grain germination
Germination of the haploid microspore of seed bearing plants.
Pollen tube growth
Growth of the pollen tube; a tubular process developed from pollen grain after attachment to stigma, and growing towards the ovule carrying male nuclei to an embryo sac.
Pollution gradients
The rate of regular or graded ascent or descent of pollution.
Pollution response inventory
A survey of bioindication methods or biological measurement approaches.
Polycyclic aromatic hydrocarbons
Organic compounds consisting of two or more hydrocarbon rings; included in many insecticides. Cf. list of chemicals.
Population turnover
The exchange of older organisms (after their death) for younger ones, from the point of view of population dynamics.
Porometrics
Measurement methods for determining stomata! aperture and CO2/H2O gas exchange.
ppm
Parts per million
Predation
The ecological relationship between food organisms and the organisms that feed on them, if the food is still alive when taken. Typical predators are lions, wolves and goshawks; strictly speaking, however, herbivores are also predators.
Primary producers
Green plants.
Protista
A proposed kingdom to include all unicellular organisms lacking a definite cellular arrangement, such as bacteria, algae, diatoms, and fungi.
Protozoa
A diverse phylum of eukaryotic microorganisms; the structure varies from a simple uninucleate protoplast to colonial forms.
Radionuclide
A nuclide that exhibits radioactivity.
Regression analysis
A comparative method for identifying the gradual loss of differentiation and function in an organism; a functional relationship among two or more correlated variables that is often empirically determined from data and used above all to predict values of one variable when the values of the others are known.
Relative standard deviation
Variance.
Remote sensing
The gathering and recording of information without actual contact with the object or area being investigated.
Respiration rate
The rate at which tissues and organisms take up oxygen from their environments and produce carbondioxide.
Rhizome grasses
Grasses with an underground horizontal stem, often thickened and tuber-shaped and possessing buds, nodes and scale-like leaves.
Ribosome
One of the small, complex particles composed of various proteins and three molecules of ribonucleic acid which synthesize proteins within the living cell.
Roast
To heat ore to effect some chemical change that will facilitate smelting.
Root zone
The layer of soil within which plant roots occur.
RPC system
The "reducer-producer-consumer" system, a relatively unsuited method for determining water quality.
Salt electrolysis
Induction of chemical changes by passing an electric current through an electrolyte (a non metallic electric conductor in which current is carried by the motion of ions), in this case salt.
Sapropel
Sediment consisting of dead aquatic organisms, principally occurring in eutrophic waters where anaerobic bacteria decompose organic matter by biochemical means.
Saprophyte
A plant that lives on decaying organic matter.
Schist
A large group of coarse-grained metamorphic rocks which readily split into thin plates or slabs as a result of the alignment of lamellar or prismatic minerals.
Sclerophyllous
Characterized by thick, hard foliage.
Secondary atmospheric pollutants
For instance: ozone, which only emerges under certain climatic and chemical conditions.
Sensitive bioindicators
Cf. text by Ellenberg - Fig. 4.
Sessile ciliates
Ciliates attached to the substrate. Antonym: free-swimming.
Sessile organisms
Organisms attached to the substrate, for instance the common marine mussel Mytilus edulis.
Sheet erosion
Movement of upper soil layers on minimally in clined surfaces, induced by the action of running water.
Siliceous magma
Magma containing silica or silicates.
Soil water capacity
The capacity of the soil to retain water against the pull of gravity.
Species
A taxonomic category ranking immediately below a genus and including closely related, morphologically similar individuals which actually or potentially interbreed.
Specimen tissue
Tissue sampled from an organism ("specimen") that is thought to be representative of the organism or a population or organisms - used here in the context of chemical residue analysis with biological monitors.
Stenobiontic
Said of organisms which only tolerate changes in their environmental conditions within certain narrow limits.
Steranes
Modern name: gonanes; a special class of steroids without angular methyl groups at the 10th and 13th carbon atoms.
Stoma (pi. stomata)
A small opening or pore in a surface, especially one of the minute openings in the epidermis of higher plants which are regulated by guard cells and through which gases and water vapor are exchanged between internal spaces and the external atmosphere.
Stomatal density
The number of stomata per unit area.
Stomatal response
The opening width of stomata is regulated by both internal factors (e.g. internal CO2 concen tration and water vapor pressure) and indirectly by external (environmental) factors.
Subarid climate
A climate with a very pronounced dry season of considerable duration and only a few months of scant rainfall.
Subhumid climate
A climate in which a dry season is clearly present but not pronounced.
Sublethal
Insufficient to cause death, not quite lethal (= causing death, deadly), at least for most of the organisms under observation.
Substrate
The base on which an organism lives, e.g. the soil or a part of another plant (in the case of epiphytes); a substance that is acted upon (e.g. by an enzyme).
Succulent
A plant with juicy, fleshy tissues adapted to conserve water, covered by a surface that minimizes evapotranspiration.
Synecological information
Information about the structure, development and distribution of ecological communities.
Terrestrial ecosystem
Cf. text by Ellenberg.
Thalassogenic
Said of waters that are influenced by marine water.
Thallic tissue
Cf. thallus.
Thallus
A plant tissue or body that is not differentiated into specialized tissue systems or organs such as leaves or stems; it may vary from a single cell to a complex, branching multicellular structure.
Thermal stratification
Tabular strata in standing water (for instance, in most Central European lakes during the summer: warm surface water, medium-temperature boundary layer, cool bottom water), caused by the distinct specific densities of water of differ ent temperatures.
Thermohygrograph
An instrument for measuring and recording variations in atmospheric humidity and temperature.
Third primary quill
The third large feather of the wing of a (large) bird, counting from the body side towards the wing tip.
Toxin
A poisonous substance, poison.
Transpiration resistance
Resistance to diffusion of water vapor.
Transplanted specimens
Organisms, normally plants, taken from a given stand - naturally grown or artificially raised - and planted or exposed at another place. They are taken for experimental purposes as being 1. an item representative of others in the same class or group, and/or 2. a sample selected for testing, examination, or display.
Trichome
An appendage occurring on the cuticles of plants, such as hairs and scales.
Trifoliate
Of leaves, consisting of three leaflets.
Trophic level
Herbivore, carnivore, parasite, saprovore, etc. Herbivores belong to the "first" trophic level, while predators that feed upon herbivores be long to the "second". Predators that normally feed on other predators are situated on the "third" or even higher levels, e.g. sparrow hawks when feeding on insectivorous birds.
Trophic relationships
Feeding relationships; of or relating to nutrition. Trophic relationships constitute one of the principal relationships among organisms of different species in an ecosystem.
Trypanosome
Any of a genus of flagellate protozoans that live as parasites in the blood of human beings and other vertebrates. They are usually transmitted by insect bites, and often cause serious diseases such as sleeping sickness, chagas disease, etc.
Trypanosomiasis
Any disease caused by a trypanosome.
Tubificids
Red blood worms, a family of red, tubivolous, oligochaete annelids (worms).
Ultrastructure
The fine structure of cells as seen with an ultra microscope.
Vascular plant
A plant having vascular bundles for liquid transport, such as phanerogams and Filicales. Mosses or algae are not vascular plants.
VDI Guideline
A guideline of the Association of German Engineers (Verein Deutscher Ingenieure).
Water body
A coherent section of water, i.e. a pond, lake,
Xeromorphic
Having an exterior structure and a shape that is adapted to dry living conditions.
