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Characterizing Ecosystem Responses to Stress MARK A. HARWELL CHRISTINE C. HARWELL DAVID A. WEINSTEIN JOHN R. KELLY Cornell University Environmental risk assessment and management involve the use of methodologies to assess risks to the health of biological systems, especially the stresses from human activities. The use of appropriate ecological indicators to measure environmental effects of these stresses can allow a realistic evaluation of risks. ECOLOGICAL ll:lSK ASSESSMENT Effective protection and management of environmental systems re- quires an adequate understanding of stress ecology. Three facets are central to the science of stress ecology: 1) how various components of ecosystems are exposed to stress; 2) how ecosystems respond to these stresses; and 3) how ecosystems recover from or adapt to stress. When there is a solid understanding of these relationships, as well as the inherent uncertainties in predicting stress response, then risks to ecological systems can be properly balanced with risks and benefits to other systems of human concern, such as economic or societal systems. Instances of unprotected or unexpected adverse effects on the environment from a particular human activity will continue to occur, along with instances of expensive over pro- tection from effects of other human activities. Risk assessment based on ecological science is essential to minimize these problems. In principle, ecological risk assessment is intended to illustrate and accommodate differences in stress/response relationships and to provide a basis for balancing environmental concerns with other economic and soci- etal issues through the associated process of risk management. However, the current reality of risk assessment and risk management is quite remote from this ideal, for a number of important reasons: 91

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92 ECOLOGICAL RISKS 1. A satisfactory basis does not exist for making cross-comparisons among alternative risks and values; for example, what value is placed on a single human life or on an endangered species? How do you compare the loss of an endangered whale species versus an endangered liverwort species? Ecological and societal values typically cannot be reduced solely to monetary units; consequently, those factors in an environmental management decision that are easier to quantify, such as economic costs of compliance with regulations, often dominate in debates about the effects of human activities on the environment. 2. Even if there were a common method of valuation, there would be great difficulty in establishing a common level of acceptability of risk across different problems. Emotional and subjective factors play a major role in defining social acceptability. Many factors contribute to this disparity, including very different perceptions about voluntary versus involuntary risks, and society's inability to handle infrequent but catastrophic events on the same basis as frequent but relatively low-consequence events. For example, the routine emissions from a nuclear power plant have few, if any, demonstrated adverse impacts on the health of the environment or the general public; nearby residents could receive a much greater dose of radiation from the thorium-daughter products in soils and rocks of the neighborhood, including radon in their homes, or from flying a few times across the country at high altitudes, than from a properly operated nuclear facility. In contrast, a fossil-fuel plant continuously emits a host of compounds that are known to cause adverse ecological and human health effects, including acid precipitation, greenhouse-induced global climate changes, and long-lived alpha-emitting radionuclides. On the other hand, an accident involving the fossil-fuel plant could at most lead to local-scale fires and injuries, whereas an accident at a nuclear facility might cause extensive ecological and human health consequences, as witnessed by increased cancer risks for tens of thousands of inhabitants in Eastern Europe, and has the potential to eradicate a whole lifestyle for cultures in Northern Scandinavia based on herding reindeer populations, all from the single event at Chernobyl. 3. The effectiveness of ecological risk assessment is seriously limited by the inability of scientists accurately to predict ecological responses to stress. There are many reasons for this limitation, including: . the considerable variety of ecosystems and potential types of human disturbances to those ecosystems; the wide range of spatial, temporal, and organizational scales in- herent in any ecosystem; the lack of an adequate baseline database for comparison of dis- turbed and undisturbed ecosystems;

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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT and 93 fundamental limitations in ecological theory and understanding; environmental variability and other irreducible forms of uncertainty associated with stress/response/recovery predictions. ECOLOGICAL RISK MANAGEMENT: REGUI^TORY ENDPOINTS Each state or nation has its own traditions and systems of environmen- tal values and regulations. In the United States, the U.S. Environmental Protection Agency (EPA) is charged with the responsibility of protecting and managing many aspects of the environment. ~ date, the predominant focus at EPA has been on environmental threats to human health, rather than on human actions affecting the health of the environment. This reality may be shifting however, as EPA:s interest grows in using ecological risk assessment as a tool for objective environmental decision making (Chapter 6, this volume). A variety of legislative actions provides the framework for the role of EPIC The language of the laws written by the U.S. Congress typically contains both broad statements as to the law's general purpose and narrower statements or sections in the law which detail the particular activities to be regulated by a government agency such as EPA, sometimes including detailed instructions as to how that regulation is to occur. The exact wording of the legislation, often clarified by a study of the legislation's history, indicates to EPA the directions to follow in formulating regulations and mechanisms to enforce the law. Thus, regulations developed by EPA are one way to translate both general and specific legislative directions provided by Congress (or directions provided by the President's executive orders or by various courts' judicial interpretations) into regulatory actions and requirements. There are sometimes certain issues or phrases in a law that are key to deciding which regulatory actions are to be taken by the government agency; these are often called regulatory endpoints, defined as those regulatory norms that translate fundamental legislative purposes into regulatory decisions or actions (C. Harwell, 1989; Limburg et al., 1986) (Figure 1~. The regulatory endpoints for environmental protection can be very specific, such as the requirement that sulfur dioxide (SO2) and ozone (03) concentrations in urban areas should not exceed particular numerical amounts; that lead (Pb) levels in gasoline should be below specified con- centrations; or that fecal conform counts in effluents from sewage facilities should remain under a certain value. In part, the degree of specificity in regulations often reflects the level of certainty about causal relationships or the simplicity and consensus within society about the endpoint of concern. Other environmental regulatory endpoints, however, are quite generic;

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94 ECOLOGICAL RISKS Congress / Regulatory Endpoints courts / \ generic specific regulatory ~ ~ agencies - ; <` onitoringt Characterizing Ecosystem Responses To Stress ecological understanding / ~ / Ecological / Endpoints human health species-level community -level \:osystem-le: )~> /' \ /issues of \ concern to humans I: Indicators of Ecological Effects intrinsic importance early warning sensitive process/s~uctural select subset of ecological endpoints to monitor FIGURE 1 Environmental decision making process. Regulatory endpoints are specified by legislation, courts, or regulations written by agencies. These must be translated into ecologically meaningful endpoints. focusing on those nroDe~ie~ of Vim. of Urn to humans. For each selected endpoint, one or more specific indicator is appropriate to measure or monitor for changes in that endpoint. The suite of selected indicatom provides the basis for evaluating ecological responses to stress and characterizing ecosystem health. they require EPA to take action on an area of legislative concern, though the specific action to be taken is not designated. For example, EPA is required by several laws to develop regulations that will accomplish the general, overall purpose of environmental and human health protection by: . maintaining and propagating a "balanced indigenous population" in estuarine ecosystems exposed to less-than-secondarily treated municipal effluents Howell, 1984a); preventing point-source discharges to marine ecosystems that cause "unreasonable degradation of the marine environment" (Harwell, 1984b); minimizing 'Significant adverse impacts"; protecting '`areas of biological concern"; preventing ``irreparable harm" to the environment; maintaining Biological integrity"; or not allowing actions that result in "accumulation of toxic materials in the human food chain." The remainder of this chapter focuses on such generic regulatory endpoints, because these tend to be associated with regulation based on ecological responses to human activity, as opposed to the highly specific regulatory endpoints, which tend to focus on technological capabilities or on chemical concentrations.

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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT 95 Generic environmental regulatory endpoints typically do not incorpo- rate language that has clear, intrinsic ecological meaning. For instance, maintaining a "balanced indigenous population" as required by Section 301(h) of the Federal Water Pollution Control Act is actually interpreted in EPAs regulations to relate to maintaining a biological community that is similar to other communities in the region surrounding a local area of disturbance. Thus, the regulatory phrasing is not what was literally specified by the legislation, though it may be what was intended: EPA:s regulatory interpretation of the law refers to a community, rather than a single "population"; the biota of concern are not necessarily "indige- nous" to the area; and since natural populations continuously fluctuate and experience dynamic interactions, it is not clear that "balanced" has any biological meaning at all. Likewise, it is not immediately evident what constitutes "degradation" of an ecosystem, or what "biological integrity" means. Terms like these were often selected by legislators precisely because the words are subject to alternate interpretations or because they allow flex- ibility and discretion on the part of the regulatory agency. Nevertheless, there is a common theme in generic regulatory endpoints, i.e., they call for some measure of maintenance of the health of the ecosystem. The intent is not to preserve all ecosystems in their pristine state, uninfluenced by human activities; such an endpoint is simply not possible for an industrial nation with a quarter-billion human inhabitants. But, on the other hand, the intent is to prevent serious adverse impacts on ecosystems from human activities that are so extensive that the environment is perceived to be excessively degraded or irreversibly disturbed- that is to say, unhealthy. Unfortunately, unlike measures of adverse human health effects (such as mortality, induced cancers, respiratory illnesses, or chromosomal aber- rations), there are no readily comparable, integrative, simple measures or indices of adverse effects on ecosystem health caused by stress. Attempts at drawing an analogy between ecological health and human health (e.g., Rapport et al., 1985) have been unsatisfactory, in part because exposure of ecosystems to stress is very complex, with differential exposure to different parts of the ecosystem; in part because ecosystems are both more diverse and more complex than the human metabolic system; and in part because ecosystems are much less internally integrated, i.e., they have a far less coordinated and controlled response to stress, and fewer mechanisms for compensation and homeostasis. If ecosystems truly were superorganisms, then ecological stress/response/recovery predictions in principle could be as reliable as human health predictions; but the reality is that the science of ecology is not in a position now to meet the needs of ecological risk as- sessment. Nevertheless, we believe that reasonable environmental decision making can be accomplished in the presence of uncertainties (Ha~well et al., 1986; Harwell and Howell, 1989~.

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96 ECOLOGICAL RISKS ECOLOGICAL ENDPOINTS The single most useful criterion to apply to measure ecosystem health is the requirement of relevance to issues of concern to humans. That is, a change in an ecosystem is only considered relevant if it relates directly or indirectly to something affecting humans. By focusing on such human- centered ecological endpoints, a structured way of evaluating ecological effects can be developed, and a framework can be created for incorporat- ing non-ecological issues into environmental decision malting (Figure 1~. While regulatory endpoints are specific goals or standards stated in laws or regulations, ecological endpoints are selected characteristics of ecosystems at various levels, the examination of which can allow evaluation of societally important environmental issues. These issues may have been covered by existing regulatory endpoints or may yet remain to be regulated. Ecological endpoints are categorized vis-a-vis issues of human concern (Table 1~. The first item, human health effects, actually dominates environ- mental regulation/protection in the United States. Our concern here, how- ever, is limited to ecosystems as vectors for human exposure to potentially harmful substances; we do not consider human effects themselves as part of ecological endpoints. For example, a bathing beach contaminated by high fecal coliform counts involves a serious risk to human health. Similarly, radiocesium deposited in fallout on tundra ecosystems and subsequently biomagnified to dangerous levels for human consumption of reindeer is a serious concern. These examples are demonstrably ecological endpoints, even if ecologically no adverse reactions occur. Even though the radioce- sium is unlikely to affect the biota population levels, or productivity, or nutrient cycling rates, its presence in potential human food-chain pathways is prima facie an ecological endpoint. All of the other categories of ecological endpoints in Able 1 are not directly related to human health issues, but are associated with ecological responses and recovery. These can be separated into species-, community-, or ecosystem-level endpoints. Species-level Endpoints: Primary The simplest, primary ecological endpoints concern direct effects on particular species that have a direct interest to humans. Such interest can involve the economic value of the species, such as Douglas fir, salmon, or oysters. Similarly, direct importance can accrue to recreational species, such as the striped bass of the eastern United States, or the variety of deer and gamebird populations throughout North America. Other species do not have a specific, direct economic value, but are of special concern

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HUM 4N EFFECTS ON THE I:E:RRESTRIAL ENVIRONMENT TABLE 1 Ecological endpoints: issues of concern to humans. l e HUMAN HEALTH EFFECTS ~ vector for exposure to humans SPECIES-LEVEL ENDPOINTS direct interest econonnc, aesd~edc, recreational, nuisance, endangered Dies indirect interest (secondary endpoints) hi- species effects Radon , conned don , pollinado n) habitat role ecological role Atrophic relationship functional relationship cndcal species . . - COMMUNITY-LEVEL ENDPOINTS food-web structure species diversity biotic diversity ECOSYSTEM-LEVEL ENDPOINTS ecologically important process economically unportant process water quality habitat quality 97 because of aesthetics or other human values, e.g., dolphins, eagles, wild horses, and grizzly bears. Many species on earth are endangered or threatened with extinc- tion; unprecedented losses of species are underway, especially in tropical biomes, from massive deforestation. A select few endangered species also hold particular recognition, usually because of aesthetic values rather than because they have a particular ecological value; after all, an endangered species typically is too rare to play a major ecological role. Examples are many species of birds (e.g., least tern, California condor); large predators (e.g., Florida panther, Peregrine falcon); or large herbivores (e.g., white rhinoceros, American bison). Finally, many species are of direct concern to humans because of a negative role. Such nuisance species include disease-vectors (e.g., certain species of mosquitoes); exotic plants that outcompete native vegetation (e.g., kudzu, Casunna); and noxious species, such as blue-green algal blooms. Species-level Endpoints: Secondary Indirect effects on species, mediated by effects on other components of the ecosystem, must also be considered. If the ecosystem component

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98 ECOLOG CAL RISKS is another species which is not directly important to humans, it then becomes a secondary ecological endpoint. Its relationship to the species of primary concern can involve several different mechanisms. For instance, bi- specific interactions can be important, i.e., where the primary and secondary species are closely linked through some interrelationships. One example is the predator/prey relationship: if society is concerned with the population levels of blue whales near Antarctica, then there must be a concern for the dynamics of the krill population. In this case, adverse impacts on the density of krill would constitute an ecological endpoint, even though the krill population itself might have little direct concern for humans. Other bi-specific relationships include pollination (e.g., concern for a species of fruit tree might translate into concern for the insects necessary for fertilization); mutualism (where two species mutually benefit from the presence of each other); and competition. The latter has been shown through theoretical studies to be potentially quite important; for example, studies using computer simulation models of forested ecosystems have shown that direct effects of air pollutants on one species of trees may allow another species to become dominant, as it outcompetes the other by being less sensitive to the pollution (Weinstein et al., in prep.~. Also, host/parasite interactions may prove important, such as when air pollutants impact forest tree species indirectly through enhancing the prospects for pest or disease outbreaks (Bedford, 1987~. Other secondary endpoints may be found in ejects mediated by habi- tat alterations, such as changes in the physical structure of the environment that alter the vertical or horizontal heterogeneity of the ecosystem. This is particularly important when a single species dominates the environmental structure for other species in the community, such as mangrove forests, many coniferous forests, seagrass beds? and agroecosystems. Thus, par- ticular concern for habitat-mediated stresses occurs for near-monoculture- dominated ecosystems. For example, mangrove trees provide a complex physical substrate for other plant and animal species, allowing the differ- entiation and development of a series of diverse ecological communities in particular niches within that ecosystem. Loss of the mangroves would consequently result in loss of habitat for many other species that might not be directly affected by the stress that destroys the mangroves, but that might have a particular importance for humans. Another important mechanism for habitat-mediated indirect effects is the amelioration of physicochemical conditions by biota or other com- ponents of the ecosystem. For example, the presence of tree and shrub species in semi-arid environments can induce evapotranspiration, which in turn can increase precipitation regionally; hence, the biota act as an en- hancing pump in the hydrological cycle upon which virtually all terrestrial ecosystems depend. Adverse impacts on this role can indirectly result in

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HUA!4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT 99 other ecological effects, as starkly demonstrated by the current positive feedback from desertification underway in sub-Saharan Africa; indeed, a major component of the drought and famines recently experienced is the human impacts on the environment through biomass harvesting for energy and food. Thus, the ecological effect of concern here (tree and shrub pro- ductivity) is of both direct importance (with respect to the economic value of this resource) and of indirect, habitat-mediated importance (with respect to inducing local- to synoptic-scale reductions in precipitation). Evaluation of this species-level effect becomes an evaluation of an ecological endpoint, determining the ability of that environment to support human life. Species-level Endpoints: Ecological Role Another species-level, indirect effect relates to the ecological role the affected species plays in the community, such as in maintaining the trophic structure of the community. Such critical species have been identified in several ecosystems; a well-known example is provided in Paine's work (1974, 1980) on keystone species, i.e., particular predatory invertebrates whose presence or absence is the determinant of the presence of other species in intertidal ecosystems. In other ecosystems, a few lower trophic- level species control the food availability for an entire suite of trophic levels directly or indirectly consuming that energy resource base. Consequently, a species-level ecological endpoint might be the seagrass species Thalassia, which supports a diverse ecosystem through reliance on it as a detritus base and relatively stable substrate; another might be the wolves that control populations of herbivores through predation. Other examples include the alligator-controlled ecosystems in the Flonda Everglades, known as "alligator holes," in which the alligator determines both the habitat structure and the trophic structure of the ecosystem. Community-level Endpoints Another type of ecological endpoint involves community-level issues. At this level of endpoint is the overall trophic structure per se, not as a mechanism for supporting a particular species of concern but as a charac- teristic of direct importance. Humans have come to value the diversity of ecosystems as having intrinsic worth, and consequently any change in species diversity constitutes an ecological change of concern. This value is reflected in some regulatory endpoints that specify maintenance of species diversity as an endpoint and a measure of overall ecological health. For instance, Section 403(c) of the Federal Water Pollution Control Act specifically calls

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100 ECOLOGICAL RISKS for consideration of changes in species diversity (Hanvell, 1984b). Simi- larly, Section 301(h) of the Federal Water Pollution Control Act indirectly calls for maintenance of species diversity through its "balanced indigenous nnn~lntion" endnnint ns interpreted hv regulations and litigation (Harwell. rare --A---- i- -A --me -c~- 9Ma). The issue of species diversity applies to ecosystem-scale biological units; but the idea also extends across landscape and regional units incorporating many different ecosystems and ecosystem types. Stresses that extend across this spatial scale can result in loss of species, or at least regional-scale loss of species. Consequently, a broader community-level concern arises, often termed a concern for biotic diversity. Thus, the elimination of large numbers of species in the tropics, primarily through human destruction of forests for biomass and for agricultural uses, is of immense importance because of the overall reduction in biotic diversity that is occurring essentially on a global scale. Ecosystem-level Endpoints The final level of ecological endpoints involves direct or indirect effects at the ecosystem level. Here the concern is for maintenance of processes that are of particular importance. Often, the roles that ecosystems perform in ameliorating environmental extremes are greatly underappreciated; but clearly, many instances exist of ecosystem processes providing tremendous economic or other societal benefit to humans. Examples include maintain- ing the biogeochemical cycles in wetlands to decrease the high amounts of nutrients in wastewater; maintaining a forest for water retention and floodcontrol; and maintaining dune ecosystems to protect coastal areas from storms. Other important ecosystem-level endpoints relate to how changes in ecosystem processes cause other changes of concern to humans. In general, changes in biotic populations may not be important, as redundancy or other compensatory mechanisms may prevent adverse changes in ecosystem processes. But the converse is not true, and changes in ecosystem processes almost invariably result in changes in biological constituents. Some ecological endpoints that need assessment are explicitly recog- nized in regulations, such as endpoints relating to water quality of surface waters and endpoints relating to habitat quality. There are no simple measures of such concepts as water or habitat quality, but often physical parameters (e.g., soil structure), chemical parameters (e.g., dissolved oxy- gen levels), or biological parameters (e.g., available habitat for waterfowl, or forage base for deer populations) can be used as surrogates for these ecosystem-level concerns.

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HUAL4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT DEFINING ECOSYSTEM RESPONSES TO STRESS Frequency and Novelty of Stress 101 Qualitatively different responses by ecosystems to stress will depend on the frequency of occurrence and novelty of the disturbance (or closely analogous disturbance) in the evolutionary history of the ecosystem. Thus, the same disturbance can have dramatically different consequences on different ecosystems, e.g., fire affecting grassland ecosystems versus tropical rain forests. In the former case, fire is a natural part of the long-term biogeochemical cycles of the ecosystem, necessary to rejuvenate a biotic community that is adapted to survival or redevelopment after fire. In the case of a tropical rain forest, a fire would lead to extreme disruption of the physical habitat and nutrient reservoirs, and reestablishment of the biotic community would take a very long time, if it were possible at all. Similarly, a particular ecosystem will likely respond differently to different disturbances; for example, the grassland may do well in the presence of fire, but be devastated by overgrazing. Time Scale of Stress An ecosystem's response to stress must also be characterized in rela- tion to the particular time scale of occurrence. Acute disturbances (i.e., those involving abrupt, large-magnitude changes in some characteristic of an ecosystem) can be exemplified by the removal of live biomass (Grime, 1979), or by the removal of total biotic material, including previously liv- ing material such as litter and detritus (Reiners, 1983~. Large-magnitude changes typically involve alterations of species composition, as in the con- version of forests in Vietnam to grass and bamboo ecosystems following the spraying of defoliants (Ischirley, 1969~. Elimination of sensitive species, reduction in pools of organic matter, and decreases in diversity have been observed by numerous researchers to occur simultaneously following acute disturbance (Weinstein and Bunce, 1981; Freedman and Hutchinson, 1980; Woodwell, 1970; and Gordon and Gorham, 1963~. Ecosystems often are adapted to cope with many types of natural dis- turbances, especially chronic stresses that are predictable (e.g., intertidal ecosystems adapted to diurnal and monthly Cycles) or periodic (e.g., grass- land ecosystems adapted to fire). When these stresses are small relative to the scale of the ecosystem, and when they have occurred commonly during historical development of the ecosystem, the disturbance often will be absorbed within the system structure, adding more heterogeneity but not changing the basic ecosystem functioning. For example, in northern temperate forests a response to wind-induced treefalls can be a formation

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HZJM;4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT TABLE 2 Indicators of ecological effects. PURPOSES FOR INDICATORS intrinsic importance - key: indicator is endpoint - e.g., economic species early warning indicator - key: rapid indication of potential effect - use when endpoint is slow or delayed in response - Animal time lag in response to stress; rapid response rate - signal-t~noise low; discrimination low - screening tool; accept false positives sensitive indicator - key: reliability in predicting actual response - use when endpoint is relatively insensitive - stress specificity - signal-t~noise high - minimize false positives processlfunctional indicator - key: endpoint is process - monitoring other than biota; e.g., decomposition rates - complement structural indicators CRl l ELLA FOR SELECI ING INDICATORS signal-to-noise ratio - sensitivity to stress - intrinsic stochasticity rapid response - early exposure; e.g., low atrophic level - quick dynamics; e.g., short life span, short life cycle phase reliabilitylspecifcily of response easeleconomy of monitoring - field earning - lab identification - pre-existing data base; e.g., fisheries catch data - easy process test; e.g., decon~osition, chlorophyll relevance to endpoint - addresses "so what?" question monitoring feedback to regulation - Captive management ., 105 must be with respect to a particular stress, or combination of stresses, since the nature of the different ecosystems may evoke different responses from different stresses. In this light, one cannot accurately characterize a type of ecosystem as being intrinsically resistant; further, the level of resistance may be determined from measuring one indicator of the ecosystem, but differ in measuring another. How an ecosystem responds to perturbation and how readily it recovers, i.e., the stability of an ecosystem, like the ecosystem itself, can only be defined operationally. Sensitivity A similar concept to resistance is the idea of sensitivity. A sensitive ecosystem is one that responds readily to a particular stress; an insensitive ecosystem may be oblivious to the stress. Sensitivity is not identical to

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106 ECOLOGICAL RISKS ~0 `-_ O o m ~v, lo sp. A o OK ~,~ O By, 0 I'" ,~0 o ...,,. TV ~ O O x. o 0:' NV ..' 'I...,, ,,' 1~_ 0 Sp.C 1 Legend: O Species Ecosystem 3< Properties community structure physical structure processes Ecological Endpoints Ecological Indicators O (folded) (shaded) FIGURE 2 Relanons~p among ecosystem properties ecological endpoints, and ecological indicators. Ecosystems are characterized by a variety of properties that exist across many space and time scales; included are species- and communi~-level properties, physical structure, and ecological processes. Stress on an ecosystem can change some or all of these properties. Ecological endpoints (shown in bolded figures) are those ecosystem properties (species, community, structural, or process) for which changes would have importance to humans and thus would represent changes in ecosystem health. Each ecological endpoint is measured or monitored by ecological indicators (shown as shaded figures). Sometimes, the endpoint itself is its own indicator (as in the Sample here for the process, community, and structural endpoints, and for species A and C). Other endpoints are measured indirectly, as for species B and C, and their indicatom are other species, community, structural, or process properties of the ecosystem. resistance, although both measure how much an ecosystem is affected by a disturbance. But sensitivity also has a temporal component, and a system that responds more rapidly than another, or to lower levels of disturbance, is considered to be more sensitive.

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HUAf4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT Recovery and Resilience 107 Another concept of importance is recovery, i.e., how the ecosystem responds following removal of the stress. Again, there are two components, one related to how rapidly the ecosystem recovers, the other to how effectively the ecosystem recovers. The temporal aspect is characterized as the ecosystems' resilience, which is defined as the inverse of the length of time required for an ecosystem to return to near-normal. Note that one cannot define this as a complete return to a pre-perturbed state, because natural heterogeneity might preclude ever attaining that precise state; however, the time required for an ecosystem state to return to a point within a specified range of its pre-stress state could be a measure of resilience (Harwell et al., 1981~. One complicating factor sometimes considered is that the non-perturbed ecosystem may well not be at steady-state, even in the absence of human interference. Properties of the ecosystem may change over time. For ex- ample, diversity of a forest ecosystem will increase during the early stages of ecosystem development, decline in the middle stages of succession, and increase again during the later stages (Woodwell, 1970~. In this case, the ecosystem is characterized by a moving set of values describing the trajectory of the undisturbed ecosystem. How resilient a non-steady-state ecosystem is to disturbance reflects the mechanism of homeorhesis of the ecosystem, i.e., feedbacks that tend to direct the ecosystem's state along a specific time sequence. The analog for the steady-state ecosystem responding to disturbance is homeostasis, a more commonly known term because of its applicability to physiological control of individuals, such as in maintaining a human's body temperature or blood pH. The human analog to homeorhesis is the developmental sequence and timing associated with embryology and with maturation of the individual into an adult. Beyond the resilience issues are questions as to whether the ecosystem effectively ever will return to its pre-perturbed state or trajectory. It is possible that some complex ecosystems, when subjected to particular disturbances, will become irreversibly transformed into another system, having different components, steady-states, and dynamics; this is a well- known characteristic of many ecosystems. For example, deforestation in the coastal hills of Venezuela has changed soil structure, seed sources, and the local physical environment sufficiently that forests have not returned even after the areas were abandoned by humans. This phenomenon repeats the irreversible loss of the great forests in Britain during neolithic times, as humans cleared land for agricultural production and energy resources. Perhaps the above examples merely reflect an exceedingly long time period of recovery, and the ecosystem will eventually recover. Yet for practical purposes, these examples of ecosystem change are permanent.

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108 ECOLOGICAL RISKS Recovery of ecosystems is in part dependent upon the characteristics of the stress (i.e., the disturbance regime, including such factors as the nature of the stress, its frequency, duration, and intensity), and in part the history of the ecosystem (e.g., the level of preadaptation to disturbance, past history of disturbance, and susceptibility of organisms within the ecosystem). An ecosystem that has been subjected to repeated disturbances may tend to deteriorate over time because of loss of nutrient reserves or substrate. Examples of such deterioration can be found in the forests of the San Bernadino Mountains of California following periodic ozone exposures (Miller, 1973), and in salt marshes exposed to a series of oil spills (Baker, 1973~. Recovery from repeated stress may be rapid if most of the important species within the ecosystem complete their life cycles within the interim between disturbance events (Noble and Slatyer, 1980~. Alternatively, for single disturbances of longer duration, recovery will be promoted if the important organisms within the ecosystem are capable of outlasting the toxicant by remaining in a latent or resting stage. For example, poor recovery has been noted in grassland systems exposed to oil- because oil degradation proceeds slowly, and the actively growing portions of the grasses become directly exposed to the toxicant during their growth periods (Hutchinson and Freedman, 1978~. Characterizing recovery of ecosystems has the same problems as char- acterizing the ecosystem response to stress, specifically which indicator to examine. Is an ecosystem recovered when its pools of nutrients are back to the pre-stressed state; or when a specific species has reestablished its pop- ulation at a particular density; or when the residues of a toxic chemical in sediments or in biological tissues have decreased to below some threshold? Just as an ecosystem functions and responds to stress at widely differing rates, hierarchical levels, and spatial extents, it also recovers differentially. There are substantial difficulties added in establishing an appropriate base- line for comparison with the stressed ecosystem, especially since when evaluating homeorhesis, one must not only have an adequate existing base- line but also a representation of what the ecosystem dynamics would have been had the ecosystem not been disturbed. Also, natural heterogeneity and fluctuations again raise the issue of detecting signals from among the noise of natural variations. Summary In summary, the health of an ecosystem is much too complex a concept to be quantified by a single measure. The multiscaled and multilayered nature of ecosystems establishes an almost infinite variety of ways of char- acterizing the ecosystem's state and relationship to some baseline condition.

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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT 109 Simple schemes to overcome this intrinsic complexity of ecosystems are by necessity simplistic and cannot be trusted. This is a true, but unfortunate reality to which society must accommodate; it means there can be no sim- ple, generic answers to the complex problems of environmental protection and decision making. However, an operationally selected suite of indica- tors, chosen in the context of the ecosystem of interest and the regulatory and ecological endpoints of concern, can offer a reasonable and realistic approach to evaluating ecosystem response and recovery to stress (Figure 2~. SELECTION OF INI)ICATORS Given that specific ecological endpoints need to be evaluated for a particular ecosystem and stress, the next step is to identify what indicators should be measured to detect potential changes in the ecosystem (Figure 14. Again there are innumerable components of the ecosystem that could be evaluated, but some careful thought can reduce these to a manageable set of indicators selected to optimize the detection of potential or actual changes in the selected ecological endpoint of concern (Table 2~. The first approach to this process is to focus on the purposes of indicators. Purposes of Indicators Intrinsic Importance Some indicators have intrinsic importance, such as when populations of direct human interest are measured directly. An example is the valuable striped bass population of the Hudson River and other estuaries of the east coast of the United States. Through the regulatory and, especially, the litigation process, measurements of this species have developed into the central concern for major human disturbances to the Hudson, such as involving thermal power plant siting, the management of the PCB-laden sediments in the river, and the recently resolved Westway Project in New York City (Limburg et al., 1986a, b). Striped bass populations became a primary indicator of ecological effects, especially through evaluations of population levels, age structures, recruitment rates, mortality rates, and migratory patterns. Many other examples of the endpoint itself being the indicator include: deer population levels, breeding success in bald eagles, productivity of Douglas fir stands, and harvested yields of shrimp. The common theme for this intrinsic importance criterion is some direct, usually economic, value of the species or processes. Early Warning But a big problem can develop if too much reliance is placed on just monitoring economically important species as the indicator of effects on

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110 ECOLOGICAL RISKS ecological endpoints of concern. In many cases, by the time an effect shows up on the indicator, it is too late for effective management or mitigation. Thus, another category of indicators is warranted, i.e., earAf' warning indicators. The key characteristic of an early warning indicator is for it to respond rapidly to a stress. Often this criterion means the indicator needs to be exposed to the stress early in the introduction of the stress into the ecosystem. Further, the indicator needs to respond rapidly once exposed. Thus, there is both a time lag and a rate of response factor involved here. Since the key issue is the rapid indication of a potential effect, the early warning indicator is a red flag hoisted to signal the need for closer examination of a potential problem. Consequently, the discrimination of the indicator can be rather low, i.e., it need not provide all the information needed to evaluate effects on the ecological endpoints of concern, and tight, causal relationships between the stress and the triggering of the early warning indicator are not required. Hence, this functions as a screening tool, where false positives are acceptable at a relatively high rate (i.e., having the flag go up even though further evaluation demonstrates no ecological effects of concern). Conversely, early warning indicators need to minimize false negatives; thus, they need to avoid missing a warning for a problem which is real. One way of enhancing this protective aspect is to incorporate more than one early warning indicator in an environmental protection scheme. Reliabili~/Sensitivity Another goal is for it to be a reliable indicator, with high capability in characterizing an adverse effect on an ecological endpoint of concern. Note that this category of indicators is focused on actual ecological effects rather than on potential ecological effects. Thus, the key issue is not the rapidity of response, but the reliability for characterizing changes in ecological endpoints. This type of indicator does require strong evidence of causal relationships with the stress, and the response should be relevant to the state of the ecosystem. This type of indicator is used when the ecological endpoint itself is relatively insensitive to the stress, or when it is difficult to separate stress- induced changes from the normal variation that occurs over time and/or space. Stress specificity is essential here if the indicator can demonstrate causality needed to Justin specific management or protection policies. Also, a criterion for this category of indicators is to minimize false positives, since incorrectly predicting unacceptable adverse impacts could lead to uneconomical overregulation. Long-term indicators might be necessary to reflect alterations at large

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HUA~N EFFECTS ON THE TERRESTRIAL ENVIRONMENT 111 spatial/temporal scales, alterations that might not become evident by only examining short-term indicators. As an example, remote sensing of land- use patterns can illustrate loss of estuarine habitats in coastal regions of southwest Florida, alterations that might not be as clearly apparent by monitoring, say, the population levels of tarpon. Process/Function Indicators may be chosen to represent alterations in ecological func- tions and processes. Such process indicators may be the ecological endpoints themselves, but it is more likely that process indicators represent the poten- tial for changes in other ecological endpoints of more immediate concern to humans. Note that process indicators are not excluded from also being early-warning indicators, or reliable indicators of change or of state. Much has been made of the relative value of structural indicators (i.e., biotic indicators of population and community structures) as opposed to functional indicators (i.e., of ecosystem processes; see Kelly et al., 1987 and Kelly, 1989~. Some authors have suggested that structural indicators, involving effects on biotic populations, are more sensitive and better early- warning indicators than functional indicators (cf., Schindler et al., 1985~. Several reasons are offered for this generalization: ecological effects are first manifest as effects on individual organ- isms and subsequently on populations; thus, functional responses would imply prior associated changes in biotic populations performing those func- tions; there is often functional redundancy in ecosystems, so that effects on specific biota may not translate into functional effects; and recovery of biotic structure of an ecosystem often lags behind recovery of functional attributes. However, there are instances where functional indicators respond at least as rapidly and sensitively to stress as structural indicators (Kelly et al., 1987~. The point is not to prefer functional over structural indicators or vice versa, but rather, carefully to select functional indicators that can significantly enhance our ability to evaluate ecological responses to stress. Criteria for Selection of Indicators Sensitivity Criteria can be listed for selecting a particular indicator to measure a specified ecological endpoint. One factor is the sensitivity of the indicator to stress, i.e., how large is the response of the indicator to a unit of stress. This measure of indicator resistance is important with respect to the normal

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112 ECOLOGICAL RISKS variation that the indicator experiences over time and space in the absence of stress. These two factors, sensitivity and variation, combine to form the major determinants of the signal-to-noise ratio for the indicator. A high signal-to-noise ratio is required for sensitive, stress-specific indicators; a low signal-to-noise ratio is acceptable for screening indicators, especially involving inexpensive or easily measured variables. As an example of this issue, consider the purported impacts on the striped bass population in the Hudson River ecosystem in comparison to the natural variability of that species. Having density-independent mecha- nisms as the primary control for these populations means a poor signal-to- noise relationship, and experts were able to argue effectively on both sides of the controversy concerning the presence or absence of demonstrated effects, compensatory mechanisms, and other issues. By contrast, consider the data on CO2 concentrations in the atmosphere at the Mauna Loa ob- servatory in Hawaii (Keeling et al., 1982~. The annual cycle in CO2 levels, related to seasonal turning on and off the primary production potential of the Northern Hemisphere, is clearly discernable; and it is superimposed over a rather constant, inexorable rise in the annually averaged CO2 levels, reflecting effects from human inputs of CO2 and human-caused destruction of primary production. Here the signal-to-noise ratios of both the long-term trend and the annual cycle are quite good, and the indicator is convincing. Rapidity of Response A second criterion relates to the rapidity of response of the indicator, especially with no time lag and a high rate of signal processing, as discussed previously. Early exposure is important; consequently, for some stresses, especially those transmitted through food webs, the rapidly responding indicator is likely to occur at lower trophic levels. Quick response also implies quick population dynamics, such as having a short life span or at least a short duration for one phase of the life cycle; for example, changes in phytoplankton are likely to occur much more rapidly than changes in whale populations. Specificity Another criterion is the specific of the response indicator. High specificity may be critical to establishing causal relationships and, hence, appropriate management decisions. Conversely, broader response charac- teristics (i.e., low specificity) may be much more appropriate for screening indicators.

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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT Ease/Economy of Monitoring 113 The criterion of the ease and/or economy of monitoring has historically been of special importance. In one sense, seeking the most economical indicator is of major benefit, in that a larger data base is likely to be developed. For example, historical records such as fisheries' catch data or board-feet of lumber harvested provide a major means for compar- ing current environmental conditions with those in existence prior to the development of stresses from industrial society. On the other hand, we seem to become too enamored with the ease or historical precedent for indicators; and we may find ourselves focusing efforts on large amounts of data with great precision, but with poor accuracy and little relationship to ecological endpoints of concern. This problem applies to laboratory testing (e.g., bioassays on easily maintained but ecologically insignificant species); field sampling (e.g., counting the 95th species in benthic samples even though looking at the top dozen or so will provide virtually all the relevant information); and pre-existing databases (e.g., fishery catches, where the endpoint is a poor indicator of anthropogenic stress on the environment because of poor signal-to-noise ratios). Relevance A final criterion is the degree of relevance of the indicator to the ecological endpoint of concern. Clearly, if the indicator itself is identical to the endpoint (e.g., the population levels of an endangered species), the relevancy is maximal. Otherwise, the more closely linked the indicator is to the ecological endpoints of concern, the less difficult it is to answer the "so what?" question that often haunts demonstrations of environmental change. Process indicators tend automatically to be considered more relevant than, for example, sensitive species indicators, since loss of a species sensitive to stress, but otherwise not of particular note for humans or ecosystems, raises the 'So what?" question (cf., Kelly et al., 1987~. SUMA/L\RY Ecosystems are complex and varied, multiscaled and multitiered, and subject to continuing change and adaptation. Consequently, a sophisticated approach is needed to characterize ecological effects from human activities, relying on a suite of ecological response/recovery indicators that reflect the status of the variety of facets about the ecosystem, or endpoints, of concern to humans. Focusing on these suites of indicators and endpoints can provide a systematic framework for incorporating scientific knowledge and understanding into a broader process of ecological risk assessment. It is unreasonable and futile to expect that a simple, generically applicable,

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114 ECOLOGICAL RISKS single measure of ecosystem health can ever be realized. However, such a scheme is not required, and an ecological risk assessment methodology for enhancing environmental decision making is a reachable goal for ecological science. Acknowledgment This report is ERC-153a, Ecosystems Research Center, Cornell Uni- versity. The ERC was established under a cooperative agreement between the U.S. Environmental Protection Agengy (EPA) and Cornell. This chap- ter represents the views of the authors, and not necessarily the views of the EPIC REFERENCES Amundson, R.G., and LH. Weinstein. 1980. Effects of airborne fluoride on forest ecosystems. Pp. 63-78 in the Proceedings of the Symposium on the Erects of Air Pollutants on Mediterranean and Temperate Forest Ecosystems. U.S.D.A. Forest Service, Pacific SW Forest Experiment Station, General Technical Report PSW43, Berkeley, California. Baker, J.M. 1973. Recovery of salt marsh vegetation from successive oil spillages. Environ- mental Pollution 4:2~-230. Bedford, B.L., ed. 1987. Modification of plant-pest interactions by air pollutants. ERC-117. Ecosystems Research Center, Cornell University, Ithaca, NY. Bormann, F.H., and G.E. Likens. 1979. Pattern and process in a forested ecosystem. New York: Springer-Verlag. Freedman, B., and T.C. Hutchinson. 1980. Long-term effects of smelter pollution at Sudbury, Ontario, on forest community composition. Canadian Journal of Botany 58:2123-2140. Gordon, A.G., and E. Gorham. 1963. Ecological effects of air pollution from an iron-sintering plant at Wawa, Ontario. Canadian Journal of Botany 41:1063-1078. Gnme, J.P. 1979. Plant Strategies and Vegetation Processes. Chichester, U.K: Wiley and Song Maxwell, CC. 1984a. Regulatory Framework of the Federal Water Pollution Control Act, Section 301(h). ERG-29. Ecosystems Research Center, Cornell University, Ithaca, NY. Maxwell, C.C. 1984b. Analysis of Federal Water Pollution Control Act, Section 403: Ocean Discharge Criteria. ERG-26. Ecosystems Research Center, Cornell University, Ithaca, NY. Harwell, C.C. 1989. Regulatory framework for ecotoxicology. Pp. 497-516 in Ecotoxicology: Problems and Approaches, S.A. Levin, M.A. Howell, J.R. Kelly, and K. Kimball, eds. New York: Springer-Verlag. Maxwell, M.A., W.P. Cropper, and H.L~ Ragsdale. 1978. Nutrient cycling and stability: A reevaluation. Ecology 58:660-666. Harwell, M.A., W.P. Cropper, Jr., and H.L" Ragsdale. 1981. Analyses of transient character- istics of a nutrient cycling model. Ecological Modelling 12:105-131. Maxwell, M.A., T.W. Duke, and J.R. Kelly. 1985. Evaluation of proposed environmental scoring methodology. ERC-106. Ecosystems Research Center, Cornell University, Ithaca, NY. Maxwell, M.A., and T.C. Hutchinson, with W.P. Cropper, Jr., C. C. Maxwell, and H.D. Grover. 1989. Environmental Consequences of Nuclear War. Volume II. Ecological and Agricultural Effects. Second Edition. Chichester, U.K.: John Wiley & Sons. Maxwell, M.^, and C.C. Howell. 1989. Environmental decision making in the presence of uncertainty. Pp. 517-540 in Ecotoxicology: Problems and Approaches, S.A. Levin, M.A. Howell, J.R. Kelly, and K. Kimball, eds. New York: Springer-Verlag.

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