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7 Indicator Species and Biological Monitoring Living organisms can be used to monitor movements, accumulations, and modifications of materials in their environments and to monitor the biological effects of those materials. They can also be used to indicate the effects of habitat alterations and fragmentation and the effectiveness of management schemes designed to preserve or change individual species or community-level patterns. Toxic substances are used by people because they confer economic or other benefits that are believed to outweigh the dangers they pose. The regulations devised for their use are guided by knowledge of their bio- logical effects. Chemical and physical monitoring can tell the quantities of materials entering or already in the environment and sometimes the fraction that is anthropogenic. But only biological monitoring can tell us what those materials are doing to organisms. Living organisms not only are essential for determining the biological effects of pollutants, but have several advantages over physical and chemical monitoring: Living organisms can function as continuous monitors. They accu- mulate records of past conditions in their tissues. These records can some- times be read and monitored more economically than can records obtained by establishing stations that continuously monitor environmental condi- tions directly. But living organisms can also distort or obscure the records by altering chemicals in their bodies; therefore, detailed information is needed to determine which organisms are best suited to provide continuous records of various contaminants. 81

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82 KINDS OF ECOLOGICAL KNOWLEDGE AND THEIR APPLICATIONS Living organisms can increase the sensitivity of monitoring. Many species can concentrate materials in their tissues and so amplify weak environmental signals. Lipid-soluble pesticides are concentrated in body fat and further concentrated when one organism eats another. Foraging bees bring pollen and nectar to their hives from many nearby sources. Sampling of pollen from bodies of bees has provided a much more com- plete picture of the distribution of several pollutants in the Puget Sound region than was obtained by more expensive chemical monitoring (Bro- menshenk et al., 19851. Living organisms can provide information about complex mixtures of materials. Laboratory studies, for reasons of expense and ability to control concentrations, typically expose organisms to potential toxicants one at a time. In nature, however, organisms often encounter toxicants in complex mixtures. By observing changes in such functions as loco- motion, growth, and reproduction in living organisms, we can determine the effects of those mixtures, even when their exact nature is unknown. (Fortunately, appropriate control measures can often be instituted without knowledge of all the details of a mixture.) Living organisms can provide information about how pollutants affect performance under natural conditions. Test organisms in a laboratory are typically kept in ideal conditions and are seldom subjected to inclement weather, disease, predators, crowding, or food shortages. In nature, how- ever, these insults can occur simultaneously with the presence of the toxic materials of concern. Under such conditions, concentrations of toxicants that would have no effects in the laboratory might be detrimental. Because our concern is to protect organisms under natural conditions, biological monitoring must be an integral part of monitoring schemes, although it must be kept in mind that the variability of natural systems often makes it hard to be certain that an apparent effect is a genuine one. O The use of communities of living organisms for monitoring can pro- vide information about how toxic materials influence patterns of inter- actions among organisms, community patterns, and processes of concern (see Chapter 31. CHOICE OF ORGANISMS TO USE FOR BIOLOGICAL MONITORING Groups of organisms can be chosen for particular monitoring purposes on the basis of the required speed of response (Cairns et al., 1973) or on the basis of sensitivity to temperature changes (Cairns, 1977), for instance.

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INDICATOR SPECIES AND BIOLOGICAL MONITORING 83 In all cases, the monitoring systems should be chosen with a clear un- derstanding of the goals to be achieved, the status of current knowledge, and the ability and commitment to act on the results obtained. Life-history characteristics of organisms strongly influence their utility for various types of biological monitoring. For example, short-lived or- ganisms respond quickly to environmental changes, whereas long-lived ones might integrate stresses over years, decades, or even centuries. Spe- cies with high metabolic rates and, hence, usually high growth rates are often more sensitive to contaminants than are species with low metabolic rates. Sessile organisms are exposed to all the contaminants that enter their immediate environments, whereas mobile organisms can escape many of them by leaving the area. Many organisms stop reproducing under stressful conditions, so changes in fecundity rates can be important signals of environmental change; but special care is required here, because stress stimulates reproduction in some organisms, particularly plants. Even within a category, some organisms are better indicators of envi- ronmental change than others. Vascular plants are effective detectors of air pollution, because particular species are especially sensitive to partic- ular pollutants. For example, the toxic components of photochemical smog in California were unknown until they were revealed by plant assays. Lesions on beans, spinach, and grape leaves indicated the presence of ozone (Middleton, 19561; lesions on annual bluegrass leaves indicated the presence of peroxyacetylnitrate (Bobrov, 19551. The ways in which dif- ferent plants respond to major air pollutants are documented by Weinstein and McCune (19701. Simpler terrestrial plants, such as lichens and mosses, are often more sensitive to airborne pollutants than are vascular plants, because they absorb water and nutrients directly from air and rainwater. As a result, they concentrate pollutants and exhibit toxic effects more quickly than vascular plants, even though they are not generally more sensitive (Hawks- worth, 1971; Lawrey and Hale, 19791. A measure of the magnitude of pollution is the lichen species diversity index, which combines the number of species present and their relative abundances (the abundances are based on extent of coverage, growth form, or degree of luxuriance). In aquatic environments, algae and cyanobacteria are useful indicators of various changes. Increases in nutrients (eutrophication) can be assessed according to increases in biomass of algae (Spirogyra, Oedogonium, Sti- geoclonium, and Cladophora) and several genera of cyanobacteria (such as Oscillatoria in Lake Washington, as described in Chapter 201. Diatoms and some other algae concentrate heavy metals and radioactive materials by a [actor of several thousand. Mollusks have been used as monitors in aquatic environments with a

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84 KINDS OF ECOLOGICAL KNOWLEDGE AND THEIR APPLICATIONS monitoring network known as Mussel Watch (Goldberg et al., 19781. Species that have been used include some in the genera Mytilus, Crass- ostrea, and Ostrea in outer estuaries and coastal marshes; in Geukensia in tidal marshes; and in Anodonta and related genera in freshwater lakes, rivers, and streams (Goldberg et al., 1978; Patrick and Kiry, 19761. Much is known about how pollutants are deposited in mollusk shells and pre- served for long periods. Metals, pesticides, and hydrocarbons are also deposited in soft tissue; they are often rapidly flushed from some soft tissue and can be accumulated there, too. Much more work needs to be done before we will know whether concentrations of most materials in soft tissue can be used effectively to indicate current environmental changes or past environmental contamination. The utility of organisms as biological monitors of environmental changes is greatest when the functional relationships between perturbation and response are understood. Nonetheless, organisms can be useful as indi- cators even if causal relationships are obscure. If a valued ecosystem component disappears or is reduced, attention is directed to a change that might be important. Caution is always necessary, because natural envi- ronments are highly variable. Species that are "typical" of some types of environment can be absent from specific locations for reasons having nothing to do with human disturbance, and jumping to a premature con- clusion might retard progress toward the goal of understanding the causes of environmental changes and how they affect organisms. Some general guidelines in selecting species most useful for particular monitoring purposes are nonetheless possible. For example, top carnivores (the organisms that develop the highest concentrations of persistent, fat- soluble pesticides) are often of special value in detecting environmental changes. They have large home ranges and they typically forage over wide areas, where they can be exposed to materials with a patchy distri- bution that are difficult to detect with fixed monitoring stations. Sea birds are valuable for monitoring, because species that nest in a single location might forage at widely differing distances from the breeding colony; there- fore, knowing which species are encountering which chemicals (as re- vealed by analysis of regurgitated food) helps in locating sources of and areas contaminated by toxic materials (Boersma, in press; Gilman et al., 19791. Sea birds are useful also because the relative ease of measuring their distributions and abundances makes them good monitors of changes in populations of fish and aquatic invertebrates, whose populations are much more difficult to assess. The herring gull (Laws argentatus) was chosen to monitor pollutants in the Great Lakes of Canada and the United States, because it accumulates pollutants only from the lakes, rather than from land, and because it is a year-round resident (pollutant concentrations

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INDICATOR SPECIES AND BIOLOGICAL MONITORING 85 in its tissues and eggs are not influenced by pollution in distant places). Several environmentally important compounds were first identified in her- ring gull tissues, and the gull has helped to monitor the fate of persistent organochlorines after control measures were established (Mineau et al., 1984). Butterflies and moths are well enough known for changes in their dis- tributions and abundances to be detected, and they can evolve rapidly enough for genetic changes induced by environmental changes to appear within a few decades. The familiar cases of industrial melanism among lepidoptera in western Europe and northeastern North America are among the best-documented cases of evolution by natural selection in which environmental pollution was the primary factor in changing the survival rates of some genotypes (Kettlewell, 1973; May and Dobson, in press). Many animals are used by veterinarians, toxicologists, and physicians to monitor human toxicants in the environment (Buck, 1979; Harshbarger and Black, in press; Schwabe, 19841. The expertise of those specialists could usefully be combined with that of ecologists to improve the choice and use of animals as environmental monitors. MONITORING AND ENVIRONMENTAL SPECIMEN BANKING Living organisms can preserve records of environmental materials in their tissues, but these records might change as the organisms age. Even more important, the death and decay of an organism eliminates such records. It is therefore useful for a program of biological monitoring to include specimen banking. The first indication of the utility of specimens as records of former environments was the documented thinning of egg- shells as a result of the widespread use of DDT (Cooke, 1973; Peakall, 1975; Chapter 241. This benefit was, of course, fortuitous the eggs were collected for other purposes. The potential value of preservation and meth- ods for preserving and deciding what to preserve are treated in detail by Lewis, Stein, and Lewis (1984), who point out that appropriate specimens can provide records of trends of pollution over long periods. Moreover, specimens remain available as analytical techniques improve, so we can use new methods retrospectively. Similarly, as new chemicals become of concern, banked specimens can be examined for them, even though no attention was paid to them when the specimens were collected. Banked specimens can also serve as records to determine the effectiveness of pollution control programs. Nonbiological materials, such as lake and marine sediments, also have some of these advantages and should therefore be included in a global banking scheme; but they cannot provide the full

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86 KINDS OF ECOLOGICAL KNOWLEDGE kD THEIR APPLICATIONS range of information obtainable from specimens of living organisms col- lected at specified times and places. The results of monitoring are difficult to evaluate unless the organisms collected can be identified. Faulty identifications could lead to erroneous conclusions about environmental changes and their causes. For this reason, in spite of the cost, it would be useful for monitoring programs to be associated with regional taxonomic centers that could care for the collec- tions and identify the materials. The lack of adequate taxonomic collections and trained persons able to care for them is a serious scientific problem in the United States, as elsewhere, and it adversely affects our ability to follow and interpret human-caused environmental changes. MONITORING OF BIOLOGICAL RESOURCES We have discussed the role of biological monitoring in the detection of pollutants and their effects. Biological monitoring is also needed to provide inventories of biological resources. Human modifications of habitats are profoundly influencing distributions and abundances of species. Species that thrive in disturbed habitats such as croplands, pastures, early succes- sional habitats, and urban environments-are increasing at the expense of species that require old-growth forests, riparian environments, wet- lands, estuaries, and flowing waters. Indeed, many experts believe that current rates of deforestation in the tropics could cause the extinction of as many as a million species within the next half-century, many of them before they have even been named and described (Ehrlich and Ehrlich, 1981; Lovejoy, 1979; Myers, 1979, 19801. An important role of biological monitoring is to determine which species are increasing and which are decreasing in abundance, where losses of species are most serious, and hence where conservation efforts should be directed. Much of this infor- mation is compiled in the "Redbooks" on rare and endangered vertebrates and invertebrates published by the International Union for the Conservation of Nature. Biological monitoring is especially valuable in helping to identify the effects of habitat fragmentation, a common form of alteration of terrestrial environments that results from human activity. Monitoring can help to determine the minimal sizes of patches required by species and how the rate of occupancy of suitable sites declines as distance between habitats increases. For example, the selective loss of nontropical migrant birds with decreasing size of forest patches in eastern North America has been documented by monitoring. Birds are good organisms for biological monitoring, because there are relatively few species, they are nearly all easily recognized, and there are

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INDICATOR SPECIES AND BIOLOGICAL MONITORING 87 large numbers of amateurs who know them well and observe them reg- ularly. Christmas bird counts and breeding-bird censuses have been carried out for many decades and are standardized. They provide excellent long- term records of patterns of distribution and abundances. The northward spread of a number of species of nonmigratory birds as a result of extensive winter feeding of birds in eastern North America has been well documented by Christmas bird counts. The striking spread of the house finch (Car- podacus mexicanus) in the northwestern United States during the last 20 years can be seen clearly in the breeding-bird censuses, including changes in abundances of species with which the house finch might compete (Min- dinger and Hope, 19821. These changes probably indicate as yet unknown environmental changes. MONITORING AND THE IDEA OF A PROJECT AS AN EXPERIMENT A major theme of this report is that many projects intended to produce something of value to human society take place on spatial and temporal scales much greater than can be duplicated in experiments designed purely for scientific purposes. Treating these projects as scientific experiments is a key component of effective environmental decision-making (Chapter 10~. Monitoring can be a vital part of the use of such projects as scientific experiments. The scales of projects are often large, so monitoring often needs to be extensive. In addition, the results of monitoring are more valuable if they are reported and analyzed in forms readily available to scientists and managers. As in other experiments, specimens collected as part of such monitoring should be retained in repositories, where they will be available to future researchers.