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Environmental Toxicology and Chemistry, Vol. 22, No. 5, pp. 945–957, 2003q 2003 SETAC

Printed in the USA0730-7268/03 $12.00 1 .00

Review

TIME AND SPACE ISSUES IN ECOTOXICOLOGY: POPULATION MODELS,LANDSCAPE PATTERN ANALYSIS, AND LONG-RANGE

ENVIRONMENTAL CHEMISTRY

JORGE ARES*National Patagonic Center, CONICET, P.O. Box 76, 9120 Madryn, Argentina

(Received 10 December 2001; Accepted 18 September 2002)

Abstract—Advances in ecotoxicology addressing problems of time and spatial scales are presented and interpreted in the frameof concepts on population/community dynamics and landscape pattern analysis. Example deterministic/probabilistic modelingexperiments are used to illustrate key concepts. Space and time scales analyzed are single and multigenerations of local populations,metapopulations, community, and ecosystem/landscape. Most population models used in recent ecotoxicology studies are deter-ministic and do not include a formal treatment of spatial processes, like migration or local random extinction. Some metapopulationmodels have been applied with success. Upscaling of ecotoxicological results at the community level is less developed, probablybecause of the inherent complexity of indirect and direct coactions among organisms. Community and ecosystem toxicity endpoints that could find a broad use in regulatory applications have not yet been identified. Some practical issues like the estimationof the potential for the natural attenuation of toxicity and the transport of contaminants along food chains must be addressed atthese scales/levels of biological complexity. The estimation of ecotoxicological effects has been increasingly evolving to integratemodeling and monitoring contaminant transport and fate, landscape pattern analysis, and spatially explicit population dynamics(including direct and indirect communal interactions).

Keywords—Pollution spatial scale Pollution temporal scale Ecotoxicology models

INTRODUCTION

While individuals are the traditional subjects of toxicology,ecotoxicology aims to identify toxic effects on populationsand communities of organisms. Modern societal requirementsof ecotoxicology as a science include the provision of a pictureas complete as possible of the potential effects of pollutingagents at the individual, community, and ecosystem levels,accounting for both direct and indirect effects. At present, theserequirements can be met only to a limited extent. Individualshave a modal life span, but populations and communities donot, although they can eventually become extinct, as shownby examples in the fossil record. Individuals occupy a discretespace in nature, while populations and communities occurwithin highly variable bounds. In ecotoxicology, we need todeal with the problem of finding acceptable temporal and spa-tial scales of analysis for the occurrence of populations andcommunities that would not compromise their conservationand/or health.

In recent years, significant advances were made in the eco-logical theory of population dynamics, ecological modelingtechniques, and landscape analysis tools. Biologists agree indescribing populations as groups of similar specimens result-ing from common evolutionary traits [1]. This definition im-plies that specimens in a population can freely interbreed, acharacteristic probably restricted to small local (panmictic [2])groups. Local populations can be spatially or functionally iso-lated from other similar local groups, and interbreeding be-tween distant specimens might not be so probable as in theirneighborhood. Although local extinction of populations may

* [email protected] at the 22nd Annual Meeting, SETAC North America,

Baltimore, Maryland, USA, November 11–15, 2001.

occur [3], generalized extinction is a less probable phenom-enon because of intergroup migration and recolonization ofempty patches. These systems of local populations are calledmetapopulations, a concept attributed to Harrison and Taylor[4]. Metapopulations are mostly coincident with biologicalspecies. Many species in nature display metapopulation dy-namics, such as Daphnia spp. [5] frogs in temporary ponds[6], butterflies [7], mountain sheep [8], etc. Toxicants maydamage local populations within extents that could be restoredby migration from neighboring populations. Conversely, spec-imens exposed to toxicants could migrate and produce dam-aged progeny in nonpolluted population patches, thus affectingtheir future dynamics. Toxic effects on local populations couldbe dampened by migration of the affected specimens to otherpatches or from healthy individuals into exposed environ-ments.

Communities are human abstractions about groups of pop-ulations sharing common habitat preferences but also inter-acting in direct (predation, competition) and indirect (facili-tation, interference) ways. Communities are characterized bycollective as well as emergent traits. Collective attributes resultfrom the simple aggregation of specimens, like the total num-bers, the total biomass, productivity, etc. Emergent propertiesderive from the interactions between life forms, such as thecapacity to recycle nutrients, the protection of the soil fromerosion, the maintenance of water quality, etc. [9]. Toxicantscould affect collective aspects of communities, like their totalnumbers or biomass or those of some of their component spe-cies, without directly affecting emergent properties like theircapacity to degrade pollutants or recycle nutrients [10]. Whilepartial damage to collective communal properties might beacceptable in some cases, the public could also be interestedin the conservation of specific populations. Ecotoxicologists

946 Environ. Toxicol. Chem. 22, 2003 J. Ares

are expected to formulate recommendations on acceptable endpoints related both to collective and emergent communal at-tributes. Biologists are interested in emergent characteristicsof biotic communities because changes in their intensity anddynamics are in many cases sensitive indicators of environ-mental change, including pollution offenses [11,12]. However,the definition of admissible end-point values of communalemergent properties poses considerable theoretical and prac-tical difficulties.

Managed landscapes occupy a large part of the world sur-face. These include horticultural and agricultural fields, inten-sively cultivated forests, aquaculture areas, intensive grazinglands, areas reserved for military use, shallow mining grounds,etc. These ecosystems differ from less intensively modifiedenvironments in a number of relevant ecotoxicological aspectsrelated to space and time scales of analysis.

Studies in agro ecosystems in Europe and Central Americahave recently shown that managed areas eventually receiveinput doses of potentially toxic substances over extended sur-faces [13–16]. In most managed systems, environmental var-iability is reduced by technical means (land leveling, fertil-ization, irrigation, etc.) to achieve better habitat manipulationand homogeneous behavior of some target species. Managedlandscapes are singularly fragmented, spatial patchiness beingdictated by management decisions and not by the heterogeneityof the natural environment. Relatively small and undisturbedvegetation patches alternate with other more or less large areasdominated by few plant types. These systems are more likelyto undergo erosion processes (water, wind) because the plantcover and the balance of soil organic matter are usually dis-turbed. Accordingly, they are likely to become pollution sourc-es to coastal, inland, and underground waters [17].

Other characteristics of agricultural management are alsoimportant in defining ecotoxicological scenarios in and aroundmanaged land. Pesticide use has been shown to explain animportant part of the biodiversity loss in faunal communitiesof several European countries [18]. Land fragmentation, acharacteristic result of agriculture, can per se modify the ex-posure of organisms to environmental toxicants, as in the caseof many birds and small mammals that tend to select largepatches of less disturbed vegetation for feeding, breeding, andnesting. In environments fragmented to small patches, spe-cialist, large-home-range vertebrates are rare or under stress[19,20]. Downstream water and air from large patches arecleaner than from small patches [21,22]. Small patches canconstitute stepping stones for species migration and recolo-nization [23].

In this review, selected recent advances in ecotoxicologyand environmental chemistry addressing problems of time andspatial scales will be presented and interpreted in the frameof present concepts of population and community dynamicsand landscape pattern analysis. Space and time scales analyzedrefer to single and multigenerations of local populations, meta-populations, communities, and ecosystems.

SINGLE POPULATIONS

Scaling ecotoxic responses from individual to populationlevels—Time scales

The 1994 Science and Technology Achievement Award ofthe U.S. Environmental Protection Agency was in recognitionof the merits of T. Hallam and coworkers’ studies about theeffect of sublethal narcosis on the persistence of Daphnia spp.populations [24]. The study evaluated the effect of nonpolar

toxicants on age-structured Daphnia populations. Lipid con-tent varies in different age classes of the daphnids and narcoticinhibition is differentially exerted on lipid as compared withstructural fractions of the daphnid body. Sublethal exposureproduces a predominance of very young and very old indi-viduals that leads to collapsing population dynamics and even-tual extinction. The authors concluded that toxic stress at asublethal level (16-d median effective concentration [EC50]for growth of specific age classes) may be expected to producepopulation extinction. The need to evaluate toxicity on themost sensitive age classes of biological populations is nowwidely recognized [25]. Acute oral toxicity studies with altri-cial passerine species, focusing on European starlings and red-winged blackbirds, have consistently shown increasing nest-ling sensitivity to organophosphates with decreasing age [26].The European starling (Sturnus vulgaris) appears to be anextreme case, with nearly a 100-fold increase in sensitivity tothe pesticide diazinon in nestlings as compared with adults[27]. In this case, increasing amounts of the enzyme butyr-ylcholinesterase protect the older starlings, and its selectiveremoval can experimentally decrease adult median lethal dose(LD50) values down toward those of the nestlings. Analogouspopulation effects could result from different metabolic activ-ities and lipid tissue partitions between sexes, resulting in dif-ferent pollutant loads [28–30]. Animal size and nutritionalstatus have been identified as possible reasons for the fre-quently observed seasonal dependence of LD50 values forvarious toxics in specimens collected under field conditionsin Leptocheirus plumosus [31], Palaemonetes pugio [32],Acartia tonsa [33], and Corophium volutator [34].

Unstructured [35,36] and age-specific [37,38] deterministicpopulation models have been used with varying degrees ofsuccess to provide guidance for protecting biological specieswhen using toxicological evidence obtained at a single-organ-ism level. Deterministic matrix models have recently been usedto evaluate toxic effects at a mysid population level based ondata obtained with standard toxicity tests [39,40]. Althoughconvenient computer routines to run deterministic models arereadily available, this type seems to be too simple to allow arealistic representation of natural populations. Developmentsin the understanding of population dynamics [41–44] indicatethat dynamic demographic processes are best interpreted inthe frame of probabilistic rather than deterministic analysis.

Stochasticity in population models

Consider a stochastic version of the simple birth–death pro-cess described in Newman and Jagoe [45], such as the onedepicted in Figure 1. A single population of size N increasesbecause of births and decreases because of deaths due to nat-ural causes and the eventual effect of environmental toxicants.Heritage and habitat effects influence both birth and naturaldeath, with intrinsic rates of both processes (b, m) assumedas normally distributed around a central characteristic value.Even when both central values are equal (b 5 m 5 0.2) andin the absence of toxic-induced mortality (t 5 0), the popu-lation can experience severe fluctuations, nearing extinction ifa temporary uneven compensation of stochastic birth–deathprocesses occurs (Fig. 1a). A slightly increased average mor-tality induced by an environmental toxic can be expected toresult in probabilistic outcomes where the population ap-proaches local extinction. No-observed-effect level-type re-sponses and temporarily increasing trends are also possible (t5 0.05; Fig. 1b). Note that the toxic death rate t assumed in

Time and space scales in ecotoxicology Environ. Toxicol. Chem. 22, 2003 947

Fig. 1. Five realizations of a stochastic birth–death population modelof the type

dN/dt 5 bN 2 (m 1 t)N

where b (birth rate) and m (mortality rate) are normally distributedwith mean 5 0.02 and standard deviation 5 0.05 (a) under no-ob-served-effect level (t 5 0) and (b) in a toxic environment with ex-posure equivalent to a lethal dose 0.05 (t 5 0.05) exposure level.

this case amounts to depleting by 5% the population stock inevery generation. This would correspond to a lethal concen-tration 0.05 (LC05), or increasing the mean natural death ratem by 20%. The ecological relevance of considering unusuallylow LC threshold values has been identified in important eco-system components such as fish [46]. Because of chance, smalllocal populations have a high risk of extinction, even whenthe expected equilibrium population size is positive [47]. Thisexample shows that LCs should be interpreted with caution inestimating sustainable exposures at the population level evenif, for practical reasons, lethal concentration/effect concentra-tion (LCs/ECs) values are usually the only data available [48].The exercise in Figure 1 also prompts an interest in inspectingthe ratio of toxic-induced to natural mortality rates (t/m), orthe ratio of t to the standard deviation of m, as potentiallyuseful end-point parameters to estimate extinction risk.

By applying extinction-time models, various authors haveshown [49–51] that other parameters relative to the stochasticvariation of growth–mortality rates can be relevant in evalu-ating toxic effects on planktonic and rotifer populations. Em-pirical models relating dose to intrinsic population growth rateproved adequate to develop response functions of populationchronic toxicity [49]. Forbes et al. [52] performed modelingexperiments on the properties of various parameters definedat the individual level, like LC50 and EC50, and studied theirbehavior as possible predictors of responses at the population

level. They defined the concept of elasticity, which in modelingparlance is equivalent to the sensitivity of population growthrates to different life-stage parameters (juvenile mortality,adult reproduction rate, etc.). In a case where probabilisticanalysis was applied to the simulation of silver bioaccumu-lation in aquatic ecosystems [53], it was shown that the sta-tistical distribution of many toxicologically relevant parame-ters is nonnormal. Accordingly, realistic ecotoxicological mod-eling should include adequate estimates of the probabilityfunctions of the various parameters characteristic of populationdynamics.

Transgeneration effects

The above analyses still ignore eventual transgenerationtoxic effects, like those mediated by endocrine disruption, em-bryonic toxicity, or sublethal effects, on the parental generationthat could affect the fitness of progenies. Evidence of the oc-currence of these effects is abundant. It has been shown thatparental exposure to mercury and Arochlort 1268 (Monsanto,St. Louis, MO, USA) produce altered sex ratios and repro-duction potential in the offspring generation in Fundulus het-eroclitus, a dominant forage fish in southeastern U.S. saltmarshes [54]. Yokota et al. [55] showed that bisphenol seri-ously affects early life stages of Japanese medaka (Oryziaslatipes) by modifying sex ratios and suppressing growth. Ham-mers-Wirtz and Ratte [56] presented experimental evidenceindicating the need to consider neonate fitness in assessingtoxicity thresholds of dispersogen A with the Daphnia repro-duction test.

Although the occurrence of many endocrine-disrupting ef-fects of pollutants in invertebrates and vertebrates is undis-puted, evidence on the significance of transgeneration effectsmediated by endocrine disruption, in terms of wildlife declineor extinction, is scarce, as indicated in a recent revision [57].This included the well-known cases of tributylin-exposed mol-lusk populations and the effects of spills of organochlorinepesticides in alligator populations in Lake Apopka (FL, USA)as well as unpublished multigeneration experiments with stick-lebacks exposed to environmentally relevant concentrations ofethynylestradiol and nonylphenol.

Transgeneration effects can have practical importance whenusing bioindicators of water quality because pollutant-resistantforms can increase after exposure during several generations.In Daphnia magna, rearing under Zn deficiency resulted inlower Zn tolerance, higher variation in brood size, and in-creased sensitivity to pH [58].

METAPOPULATIONS

Space scales

Inherent in early experiments and models of ecotoxicity isthe assumption that the environment is to a large extent hor-izontally isotropic. Populations were also assumed to be spa-tially unstructured. None of these have been supported byempirical evidence and more recent studies and theory on theviability of natural populations [59,60]. Populations are notuniformly distributed in space. Organisms with sessile or near-static individuals like terrestrial plants, lichens, etc., are onlyfound at suitable environmental patches, while mobile organ-isms are distributed in a complex spatial pattern resulting fromvegetation patchiness, behavior, and the distribution of otherinteracting populations. Individuals interact more intensivelywith others in the same or nearby environmental patches (local


Fig. 2. The spatial distribution of suitable habitats for plant and animal organisms in agricultural landscapes depends on geomorphologicallimitations, the history of land occupation, access to irrigation water, etc. (a) The distribution of vegetation cover (crops, pastures, etc.) at Ascasubiarea (lower Colorado River basin, Argentina) as represented by a gray-palette image of the green vegetation index. The black arrow shows theapproximate point were pioneering farmers first started activities and land subdivision at the beginning of the last century (San Adolfo colony,Ascasubi, Argentina). (b) The intensity of subdivision and diversification of land use as characterized by a corresponding image of the fragmentationindex. Land fragmentation grades from areas represented in black (high fragmentation) to white (low fragmentation).

populations), and migration between patches constitutes animportant factor in regulating the total population numbers[41]. Populations are highly structured in space, and this hasconsequences in their response to toxic stress. Spatial struc-turing is evident in insects where populations are small orisolated, prone to extinction because of climatic events or be-cause their habitat is transient [61–63]. Local dynamics havealso been observed in other organisms, like in herbs [64], snails[65], mammals [66], etc. In some cases, local behavior maybe combined with transgeneration phenomena, as in Gam-marus pulex, where juvenile forms tend to occupy areas withlow adult densities, a probable anticannibalistic response [67].

As a result of this type of phenomena, the dynamics ofnatural populations depend on the degree of environmentalheterogeneity, i.e., the rate at which key environmental prop-erties change in space. This is called habitat fragmentation[68–70] and can be quantified through several ad hoc param-eters. A usual procedure is subdividing a landscape image insquare kernels of 9, 25 . . . 49, etc., pixels and computing afragmentation index (FI) of the type

FI 5 (n 2 1)/(c 2 1)

where n is the number of different classes present in kernelsof c pixels considered (9, 25 . . . 49, etc). In the frame of astudy on the spatial distribution of pesticides at the lowerColorado River basin in Argentina [71], we inspected a the-matic mapper satellite image of the Ascasubi area, where farm-ing activities started early last century (Fig. 2). Pioneeringfarmers selected the best land to start activities, and the suc-cessive occupation of surrounding areas also followed thistrend. High-quality land was subdivided to a greater extentthan poor-quality land in successive farmer generations. Also,farming is more intensive in highly valued and highly frag-mented land (Fig. 2a, lower left) than in lower quality areas

(Fig. 2b, upper right), where activities are more extensive.Pesticide applications in older farming areas occur on smallerpatches and at higher and more frequent doses than in largerfarming units at the newer areas.

Dilution or concentration of applied toxics can be antici-pated, depending on the size of the treated area. Fugacity mod-eling [72] predicts that the amount of pesticides remaining insmall agricultural units is reduced in comparison with largerproduction areas even if the same agronomic receipts (pesticideloads/unit land surface) were applied in both cases. This isbecause the perimeter/area relation decreases nonproportion-ally to a reduction in area. Air advection occurs through somepart of the field perimeter (; 1/4 at a time), and the minimumperimeter to area ratio in 5-ha fields is 1.6E22 as comparedwith 4.42E24 in 400-ha fields. Assuming a mixing air masswith a height at about 1,000 m, the residence times of advectiveair are 2.0E23 d and 1.8E22 d at the smaller and larger fields,respectively. The faster turnover of clean air from outsidethrough the smaller areas results in lower pollutant exposures.Similar reasoning can be applied to water advective flows.Fugacity estimates corresponding to several pesticides used incitrus crops of Misiones province (Argentina) [73] predictnearly 10-fold reductions of pesticide concentrations in soilsand waters and human exposure risks at typical 5-ha crops ascompared with 400-ha crops with the same management sys-tem (Fig. 3).

Pollutants distributed in patchy environments may producesource-sink population behavior in exposed biota. Salminen etal. [74] specifically tested this hypothesis in Cognettia sphag-netorum, an enchytraeid worm commonly used to quantifysoil pollution. They found that worms avoided patches of soilpolluted with copper when unpolluted areas were available,and their movements followed predictions based on density-dependent mechanisms. As a consequence of this, nonstratified


Fig. 3. Pesticide exposure evaluated in terms of human risks relativeto acceptable daily intake (ADI) resulting from environmental ex-posure to agricultural pesticides in citrus crops of different size atMisiones, Argentina. (a) Five-hectare citrus fields. (b) Four hundred-hectare citrus fields. Note the different horizontal scales.

soil sampling could distort estimates of the relation betweenpopulation density and average soil pollution.

Pulliam [75] discussed the relevance of the metapopulationconcept in evaluating the toxicology of wildlife. The mostdirect implication is in the analysis of exposures, i.e., the shareof times spent in each habitat type by mobile biota, as estimatedthrough direct visualization of animals, radio tracking com-bined with geographic information system analyses, etc. [76].Other ecotoxicological implications of the metapopulationstructure of biota must also be taken into consideration. Bycombining genotoxicity and population genetic analyses, it hasbeen shown that migration can mask pollutant exposures tar-geted to selected components of the biota [77]. Consideringrealistic population spatial distributions has practical relevancein assessing the effects of pyrethroid pesticides used in cottoncrops. Maund et al. [78] showed that cost-efficient consider-ation of landscape fragmentation patterns produced exposurerisk estimates considerably lower than those obtained withnonspatially structured, standard regulatory methods [79,80].Through the use of satellite imagery and geographic infor-mation system techniques, the authors estimated the proba-bilistic distribution of areas cultivated with cotton and theirvicinity to ponds where aquatic life should be protected inMississippi, USA. They compared their results with the cor-responding U.S. Environmental Protection Agency Tier II sce-nario for the protection of aquatic life in relation with pesti-cides applied to cotton crops. The latter assumes a standardlandscape configuration consisting of a 10-ha pond completelysurrounded by 10 ha of cotton crops, with high levels of ero-sion, runoff, and drift entering the pond. Cypermetrin expo-sures computed from the analysis of real landscape scenarioswere 50 to 100 times lower than those obtained using the U.S.Environmental Protection Agency standard model pond andparameters.

Landscape fragmentation is also relevant in considering thedynamics of plant and animal populations in agricultural land-scapes [81]. Kruess and Tscharntke [82] studied several groupsof insect seed feeders in the pods of Vicia sepium and theirparasitoids in an agricultural landscape consisting in patchesof various sizes. They concluded that the patch area was themajor determinant of species diversity and abundance of en-dophagous parasites in the seed feeders. Also, colonizationsuccess of the plant pests was greatly reduced in isolated en-vironments. These results have obvious ecotoxicological rel-evance. Phytophagous insects are usual targets of applied in-

secticides, which in most cases also affect their parasitoids.The complexity of toxic effects on these predator–prey systems(parasitoid–herbivore host–plant) is further enhanced by thefragmentation of the habitats where they occur. Similar find-ings have been reported in the case of pollinator Apoideaeinsects [83] and rape pollen beetles [84].

Freshman and Menzie [85] presented a model using stan-dardized hypothetical landscapes, with simple rules for animalmovements through the landscape. Another example is thePARET model developed in the frame of ECOFRAM [86].This model includes stochasticity in pollutant effects, sublethalend points, exposure estimates, and pesticide fate discrimi-nated on the basis of landscape structure and time-scaled treat-ment of pollutant fate and persistence within exposed biota.Examples of geographic information system approaches usingdata on real landscapes and population behavior have also beenpresented [87–89].

COMMUNITIES

Time and spatial issues

For convenience, the ecological literature identifies directinteractions among populations in communities as those oc-curring with direct participation of two or more species or lifeforms, like in predation or in competition events involvingsome form of obvious mechanical interference, either in ani-mals or plants. A large body of ecological literature is alsodedicated to so-called indirect effects, where life forms interactthrough modification of some external habitat factors, inducedscarcity of a common prey, etc.

Direct effects under toxic stress

Predation, parasitism, and herbivory are similar forms ofinteraction among organisms that have been identified as gen-eralized predation [9]. In the first case, the prey death occurssuddenly, while during parasitism, it generally occurs aftersome time. Herbivory might not necessarily lead to prey death.In all cases, the predator benefits (i.e., its fitness increases)from the interaction but also depends on the continued exis-tence of prey. Toxicants can modify the dynamics of (gener-alized) predator–prey systems by acting on the prey and mak-ing it scarcer or weaker; by acting on the predator, making itless effective or abundant by poisoning the predator throughingestion of contaminated prey, etc.

Consider a simple (Lotka–Volterra) model of a prey–pred-ator system devoid of any spatial effects [90] in which toxicstress to the predator is introduced analogously to the singlepopulation case in Figure 1 (Fig. 4). In the absence of toxiceffects (t 5 0; Fig. 4a), the predator increases the death ofprey individuals, while the abundance of prey accelerates thegrowth of the population of the (successful) predator. As aconsequence of these, both populations show cycling numbersin time, the predator catching up and controlling the preywhenever it increases, declining afterwards as a consequenceof prey scarcity. If the predator is under sublethal toxic stress(t 5 0.05; Fig. 4b), its rate of increase might not be highenough to control prey increases. The prey population escapespredator control and grows exponentially until the environmentsets some other limit to its increase (i.e., food–space scarcity,etc.). At the same time, the abundance of prey produces apositive effect in the population growth of the predator, whichmight compensate the toxic effect. In this case, the prey feedsthe predator but this latter is no longer able to control the prey.


Fig. 4. Dynamics of a stochastic predator–prey system of the type

dN /dt 5 bN 2 mN 2 pN , dN /dt 5 b9N 1 fN 2 tN 2 m9N ,1 1 1 2 2 2 1 2 2

where N1, N2, b, b9, m, m9 are the prey and predator densities andtheir birth (normally distributed, mean 5 0.3, standard deviation 50.05) and mortality (normally distributed, mean 5 0.2, standard de-viation 5 0.05) rates, respectively; f is the rate of predator increasedue to the benefit of the prey (0.1) and p is the death rate of the preydue to predation (0.1); t is the lethal toxicity rate (a) under no-ob-served-effect-level exposure to a contaminant (t 5 0) and (b) underexposure equivalent to a lethal dose 0.05 (t 5 0.05).

The effects of toxics on similar predator–prey systems mayalso differ depending on their relative sensitivity to the toxi-cant, as shown in microcosm experiments [91]. The authorsstudied the effect of several toxics contained in wood-pre-serving substances on the pair vole (Microtus canicaudus,predator)–cricket (Acheta domestica, prey). The predator in-creased or decreased the catch, depending on exposure to par-ticular toxics, probably reflecting increased catching ability ordecreased prey escape. Evidence of toxic inhibition of predatorability has also been shown in experiments where the catchof Artemia salina by the grass shrimp Palaemonetes pugiodiminished after exposing the shrimps to a diet rich in Cd [92].

Predator–prey ecotoxic relations have been inspected inrelation to variations in the abundance of predators at hightrophic levels. This is based on the idea that organisms withcolonizing ability can rapidly occupy disturbed habitats andturn into trophic links to higher predators that would bioac-cumulate so far untapped pollutants. This hypothesis was test-ed in relation to zebra mussels (Dreissena sp.) invading thesouthern Great Lakes and several waterfowl species that feedon them and are known to be increasing in recent years. Inlesser scaup (Aythya affinis) total polychlorinated biphenylconcentration in carcasses did not exceed known effect levelsbut exceeded the U.S. Food and Drug Administration thresholdfor consumption of poultry, indicating a potential risk to hu-man health. Selenium liver concentrations were, in most cases,in the potentially harmful range for the studied waterfowl spe-cies, although the concentrations in dreissenid mussels were

similar to other industrialized sites where zebra mussels hadbeen sampled [93].

Immunotoxicity is a direct interference of toxics with in-terpopulation coactions of parasitic type. A wide spectrum ofpollutants, including terrestrial pesticides, heavy metals, po-lychlorinated biphenyls, polynuclear aromatic hydrocarbons,organotins, and complex mixtures in contaminated sedimentsand harbor dredgings, have been implicated in immunotoxicresponse of bivalves, oligochaetes, gastropods, crustaceans,and tunicates [94]. However, reports of field immunotoxicityevidence are scarce, probably because diseased organismsmight be rapidly eliminated. Pizl [95] found that earthwormsfrom fields treated with a triazine herbicide were infected withmonocystid gregarine parasites. Exposure of the oyster Cras-sostrea virginica to the insecticides DDT, toxaphene, and para-thion led to the development of an unidentified mycelian fungalinfection [96]. Latent infection of C. virginica with the path-ogenic protozoan Perkinsus marinus was enhanced followingexposure to the carcinogen n-nitrosodiethylamine [97].

Herbivore interactions were apparently involved in the spa-tial distribution of Collembola species in a field polluted bycopper [98]. In this case, the distribution of total numbers ofsoil Collembola was positively correlated with the total Cucontent in samples from a grid in a field that had been usedby a wood preservation facility. Through the use of multivar-iate analysis of community distribution data, a slightly strongerordination effect of Cu upon Collembolan numbers was shown.However, soil Cu was also positively correlated with humusand total C content of soil samples. This latter could be in-terpreted as the consequence of Cu limiting organic matterdecomposition because of toxicity on microorganisms. Col-lembola are detritus grazers, and they tend to concentrate innumbers at places where food is more abundant. Accordingly,the humus content might have been the leading variable inshaping microinvertebrate distributions. This data set illus-trates the complexities inherent in identifying toxicity effectsat the level of interacting populations. Multivariate statisticaltechniques often require transforming the original data in orderto assume predetermined distributions, and confidence testsfor the rejection of null hypothesis might not be available forcomplex data configurations. Multiple correlations among en-vironmental and community descriptors limit the formulationof statistically significant conclusions.

Indirect effects

The analysis of indirect effects can be easily visualized inthe case of so-called keystone species [99]. These are a classof organisms that play specific and important roles in main-taining ecosystem core processes like primary production, wa-ter balance, nutrient cycling, etc. It is intuitively appealing thattoxic effects on these organisms would have a greater ecolog-ical impact than comparable effects on nonkey types. Salminenand Haimi [100] presented a case where Zn toxicity influencedsoil microbes via its toxic effect on the keystone species Cog-nettia sphagnetorum (Enchytraeidae, Oligochaeta). Enchy-traeidae, a dominant component of soil microfauna, seem tobe effective regulators of soil microbial biomass and nitrogen–carbon cycles, and they seem to be more sensitive to soilpollution than other groups in below-ground food webs.

Scheffield and Lochmiller [101] have recently reported theresults of a microcosm study on the effect of exposing a com-munity of small mammals in a prairie grassland ecosystem tosubchronic levels of the pesticide diazinon. They set out a field


Fig. 5. A flow-compartment model of a population system homologousto the description in Sheffield and Lochmiller [101]. The dynamicsof Sigmodon hispidus and Microtus ochrogaster populations are de-scribed in terms of birth–death processes as well as that of a genericarthropod composing their diets. A generic toxicant (Toxic) simul-taneously increases arthropod mortality (Arthr toxicity) and interfereswith female rodent reproduction at characteristic specific rates (Pregtox 1, Preg tox 2). The arthropod population partially controls birthrates of the mammals through serving as alternative diet item withseeds. Birth–death rates set to steady-state population values after 50generations.

experiment where they limited the displacement of introducedpopulations of hispid cotton rats (Sigmodon hispidus), prairievoles (Microtus ochrogaster), and other native small mammalsof the Oklahoma (USA) tall-grass prairies while exposing themto controlled applications of diazinon in 0.1-ha exclosures. Thesurvival of the small mammals was evaluated by capture–recapture techniques, and detailed necropsies were performedat the end of a 30-d exposure period in order to evaluate theeffect of the pesticide on the fertility and pregnancy rates. Theauthors reported slight reductions in the trappability of thespecies, probably indicating some increased female and maleadult mortality. Most important, female reproductive produc-tivity was strikingly reduced in both species, as estimated bythe mean number of embryos per female, the percentage ofpregnant females, and the percentage of females giving birth.The target arthropod populations in the plots were drasticallyreduced.

Some interesting characteristics of these species can be usedto illustrate the potential complexity of indirect populationeffects. Sigmodon hispidus is the most numerous rodent in thegrasslands of the southern Great Plains and, although predom-inantly herbivorous, is known to consume arthropods, seeds,and eventually soil, while M. ochrogaster is predominantlyherbivorous but will consume arthropods when available. Ac-cordingly, exposures to the pesticide through the diet are ex-pected as well as effects from simultaneous arthropod preyscarcity.

Interpreting indirect effects with simulation models

Simulation models can be used as tools to explore feasiblecommunity indirect effects. Modeling has been applied to in-terpret and quantify biota–sediment partitions of polycyclicaromatic hydrocarbons [102]. In this case, the accumulationof pollutants in various trophic levels (benthic invertebrates,crayfish, sunfish) was estimated with a deterministic model ofsimultaneous difference equations. Ready-to-use computercodes combining population demography–toxicity relationsand food-web information are available [103] or can be easilybuilt with adequate simulation software.

As an example of this latter case, consider a feasible para-metric scenario of the sigmodon–microtus–arthropod systemunder toxic stress described in [101] (Fig. 5). The model isbuilt with the simulation language Stella [104] and expressespopulation changes in terms of growth–death processes, likein [45], and prey–predator dynamics, like in [90]. Additionally,two variables representing the density of Sigmodon sp. andMicrotus sp. embryos are included in order to fully representthe system described in Sheffield and Lochmiller [101]. In thissymbolic language, boxes represent stocks (population num-bers) while the thick arrows represent birth and death flows.Thinner arrows and circular symbols are controlling factors orintermediate parameters or variables. Diazinon (Toxic) in-creases the arthropod death flow (Arthr death) to an extentdescribed by a specific arthropod toxicity rate (Arthr toxicity).The pesticide also reduces rodent fertility as characterized byspecific toxicity rates (Preg tox 1, Preg tox 2). The arthropodand the seed stocks influence the birth rates of both rodentspecies through their share in the diet. For convenience of theexercise here presented, all other stocks and flow parametersare conveniently initialized based on the data supplied by theauthors or reasonable guesses derived from them in order toproduce a steady-state condition after some few rodent gen-erations.

Such a system allows exploring relevant aspects of the ef-fects of toxicity on a multispecies system like this. For in-stance, it is of relevance whether the amount of embryos pro-duced at each generation can be expected to be controlled bydirect toxicity on pregnant females (Preg tox 1, Preg tox 2)or through reduction of the arthropod share in their diet (Arthrtoxicity). This can be addressed through a sensitivity analysisof the model responses by increasing each of Preg tox 1–Pregtox 2 or Arthr toxicity while maintaining the other at a constantlevel. The results are shown in Figure 6. See that changingArthr toxicity from 0 to 0.l gradually reduces the number ofS. hispidus embryos from about 80 to about 60 in 50 gener-ations (Fig. 6a). Changing Preg tox 1 in the same range whilekeeping Arthr toxicity at the 0.1 level does not change theamount of embryos (Fig. 6b). Even a zero level of diazinontoxicity on the rodent females cannot revert the prey-scarcityeffect produced by increased arthropod mortality.

Other cases of indirect effects

Field studies on grassland bird–insect systems producedvarying evidence on the absence [105] or occurrence [106] ofindirect effects of pesticides on the predators. In a recent re-view on 40 species of farmland birds in the United Kingdom[107], the authors concluded that 50% of these were in decline.


Fig. 6. Results of a sensitivity analysis of the production of Sigmodonsp. embryos depending on the relative impact of environmental toxicson the pregnancy rate of the rodent or on the death rate of preyarthropods, as predicted by the model described in Figure 5. (a) Toxic-induced arthropod mortality rate (Arthr toxicity) varies from 0.1 to 0at 0.025 intervals while keeping Sigmodon hispidus pregnancy tox-icity rate (Preg tox 1) at the maximum level (0.1). (b) Toxic-inducedS. hispidus pregnancy toxicity rate varies from 0.1 to 0 at 0.025intervals while keeping arthropod mortality rate at the maximum level(0.1).

There was evidence of short- and long-term declines in theabundance of many of the types of invertebrates and plants onwhich these birds feed and that these declines were, in part,attributable to the effects of pesticides. Indirect effects on smallmammals feeding on pesticide-sprayed arthropod communitieshave been known for some time in terrestrial [108–110] andaquatic ecosystems [111]. Because most population processes(birth, death, predation intensity, etc.) are influenced by habitatconditions (temperatures, water balance, nutrient availability,etc.), it is to be expected that weather-mediated and seasonalchanges in population processes would hinder the effectiveuse of techniques for the evaluation of toxic risks that ignorethese effects [112].

Schultz and Liess [113] presented an interesting exampleof some indirect toxic end points at the community level thatrelates intra- and interspecific processes with spatial and tem-poral phenomena. They arranged a series of compartments inmultispecies stream microcosms and were able to show thatthe tendency of juvenile Gammarus pulex to spatially avoidadult Gammaridae was reduced by exposure to fenvalerate,probably resulting in increased cannibalism. Because adultGammaridae also prey on other invertebrate species like cad-disflies, this might have contributed to decrease by an orderof magnitude the apparent lethal effects of fenvalerate on cad-disflies in the same microcosms, as compared with others withsingle caddisfly populations.

Pseudocommunal ecotoxicity end points

On occasions, ecotoxicity studies are conducted usingwhole communities as research subjects because the evaluationof effects on separate individual species or life forms is notpossible under practical conditions. This approach should beconsidered as addressing a mixture of organisms, but it shouldbe noted that it could not supply information on either director indirect effects at the community level. End points of thesestudies are eventually limited to collective communal attri-butes, and emergent characteristics cannot be evaluated. Usualcases are in studies involving bacterial communities of soilsand sediments like in Cartwright et al. [114], where the effectof phthalate plasticizers on soil microbial assemblies was eval-uated. As end points, the authors selected the phthalate deg-radation rate of intact soil microbial populations, the total num-ber of cultivable bacteria, evenness, and diversity indices. Inseveral cases, bacterial numbers decreased at the beginning ofthe exposure to phthalates, without recovering even after 16d. No significant effects of phthalate toxicity were detected inevenness or diversity indices. The rate and extent of phthalatedegradation capacity of the microbial community decreasedwith increasing toxic concentration. It should be noted that,in this case, only evenness and diversity are emergent com-munity end points being evaluated. Total numbers (a collectiveattribute) could be reduced by a proportional toxic effect onall life forms, and phthalate degradation capacity could be aconsequence of the reduction in total numbers, not an impli-cation of communal effects in the sense of altered direct orindirect interactions between species or functional groups.

A second example of pseudocommunal end points is a re-cent study of Lahr and Banister [115], who reported resultswith aquatic invertebrates of a system of temporary ponds intropical Senegal. The ponds usually receive runoff from nearbyareas where pyrethroid insecticides are applied to control mi-gratory locusts, a plague in groundnut crops and pastures inthe region. The invertebrate zooplankton consists of about 80species of mainly Cladocera, Copepoda, and Ostracoda. Mac-roinvertebrates are dominated by fairy shrimps (Brachiopoda,Anostraca) and backswimmers (Hemiptera, Notonectida).Clam shrimps, dragonflies, damselflies, water mites, and leech-es are also present. In this scenario, the pond community occursin spatial patches, and the persistence of several life formsdepends on recolonization by flying specimens (Anisops spp.,Notonectida), while other forms may depend on the washoutof sediment containing dry-resistant eggs (fairy shrimps). Theexperiment consisted of fumigating the ponds with variouspyrethroid insecticides and assessing the status of individualpopulations of aquatic invertebrates during the treatment sea-son and its following year. Statistically significant decrementsin population numbers after fumigation were reported for someCladocera as well as other effects suggested by the authors’based on their expertise. Several demographic reductions re-covered after four to six weeks. Some of the tested pyrethroidsdecimated the fairy shrimp Streptocephalus spp., and therewas no recovery during the remainder of the rainy season.Effects on backswimmers were transient, and numbers recov-ered during the same season. All species, even those that haddisappeared during the application season, reappeared in usualnumbers the following year. All these results refer to collectiveattributes of the invertebrate community. Some of the observedchanges coincide with observations in similar systems [116],but others, as in the case of shrimps and Chironomidae larvae,


did not [115]. The comparisons among cases are limited dueto the multiplicity of factors that could operate in controllinginvertebrate numbers. The authors also commented on the oc-currence of some emergent communal traits (which they callsecondary effects). Populations of the copepod Paradiaptomusrex increased 150- to 200-fold after fumigations, a fact thatthe authors attributed to reduced predation or reduced com-petition with other Cladocerans. A similar trend was observedin the Ostracod Heterocypris simmetrica, but these constitutedemergent hypotheses rather than experimental findings.

ECOSYSTEMS

Introducing long-range contaminant fate and temporalscales

Short-range transport and fate of environmental chemicalsreleased from point sources is a relatively well-understoodarea, and numerous procedures and modeling techniques areavailable to formulate estimates [117,118]. However, based onrecent literature reviews, there does not appear to be any short-range residue computer model currently available that couldbe used to adequately generate distributions of contaminantconcentrations in all relevant environmental media for use instochastic exposure assessments. Some existing residue mod-els could possibly serve together as a good foundation for sucha model. These include the spray drift model AgDRIFT [119];the leaching/runoff model PRZM 3 [120]; the surface-watermodel EXAMS [121]; the uptake, translocation, accumulation,and biodegradation plant contamination model [122]; theSNAPS/PLANTX plant contamination model [123]; and thesoil–plant–air fugacity plant-contamination model [124].

Analytical procedures to estimate long-range (10s to 100sof km) fate require combining techniques at various scales,like point source and fugacity modeling [125,126], and thecomparison of long-range dispersal of persistent and nonper-sistent contaminants injected at a single environmental com-partment [127]. Long-range environmental chemistry hasfound its main application in identifying so-called persistentcontaminants [128]. Because contaminant transport dependson the characteristic flow velocities of the transporting phases(air, water, dust, sediment, etc.), substances found to be trans-ported over long distances are usually persistent [129]. Ac-cordingly, long-range transport is usually related to the anal-ysis of chronic exposures of low intensity over large areas,characteristic of long-lived/large-size and mobile biota.

The long-range environmental behavior of persistent con-taminants depends to a large extent on their capacity to par-tition in air, water, or both. Boundary criteria at a vapor pres-sure 1027 Pa and water solubility 1026 g/m3 have been sug-gested to classify most contaminants of long-range environ-mental relevance [130]. Low-volatile/low-soluble substancesmay nevertheless slightly partition in fats, and equilibria withpure phases must be considered. Substances that exist in var-ious species, like mercury, may display mixed behavior. Un-derstanding the ecological relevance of a contaminant requiresadditional knowledge on its emission rate. This is usually es-timated via production figures, discharge monitoring records,etc. Once acquired, the equilibrium concentration of the con-taminant in various environmental compartments (air, water,inorganic, organic solid phases) can be estimated with themultimedia environmental models techniques [131,132].

Although most of the applications of these techniques havebeen in modeling chemical fate in wide regions [133,134],they can in principle be solved at any spatial scale, provided

adequate input data are available. Solving the fugacity algo-rithm in nested areas (global, continental, regional) allows abetter estimation of advective pollutant flows, and the qualityof estimates can serve most screening purposes, as indicatedin a recent validation study with actual monitoring data [135].This flexibility of partition modeling has been explored withsuccess to estimate the tissue exposure (uptake–release) ofpolychlorinated biphenyls during the lifetime in the belugawhale (Delphinapterus leucas) with a physiologically basedpharmacokinetic approach [136]. The method is suitable forother hydrophobic contaminants and large aquatic mammalsand improves usual physiologically based pharmacokinetictechniques [137] that do not consider animal size changesduring its lifetime. By applying the partition model, the authorswere able to explain the differences observed during lifetimeaccumulation of hydrophobic contaminants in males as dif-ferent from females, which eliminate pollutants during birthand lactation episodes. The algebra of fugacity allows for anestimate of contaminant intake–excretion equilibria in air andwater interphases. The approach constitutes an attempt to com-pile a contaminant mass balance using a simplistic represen-tation of the animal as a set of interconnected compartmentsand prompts the need for innovative sampling techniques toassess the status of exposure of these animals to persistentcontaminants. These should include the simultaneous moni-toring of milk, blubber, blood, and feces in order to interpretthe equilibria involved.

Trophic relations in the ecosystem can modify the partitionof contaminants in various phases. A recent study by Ridal etal. [138] incorporated indirect effects mediated by nutrientsupply in a study on aquatic enclosures where food webs weresimultaneously manipulated. Several organochlorine pesti-cides at concentrations below toxicity values for zooplanktonicinvertebrates were added to aquatic mesocosms where thenumbers of zooplanktivorous fishes in combination with N andP fertilization were simultaneously manipulated. The increaseof densities of zooplanktivorous fishes resulted in an increasein phytoplanktonic organisms by depleting their predators,while nutrients (nitrogen, phosphorus) increased the biomassof primary producers. The average size of plankton diminishedwith either nutrient or planktivorous fish addition, with cor-responding increases in relative surface area of suspended par-ticulates. The lipid content of organisms at all trophic levelsincreased with nutrient addition. As a result of these complexinteractions, differences in the organochlorine concentrationin the plankton varied within an order of magnitude after 107d of mesocosm life. Nutrient addition produced a nearly two-fold increase of several organochlorine residues in fishes andzooplankton. The system illustrates the possible complexity oftrophic web–toxicity interactions in aquatic ecosystems.

An important concept linked to the ecosystem level of or-ganization is that of natural and managed attenuation of tox-icity. In the long run, pollutant decay occurs at the ecosystemlevel as a combined result of inorganic and organic processes.It has been suggested [139] that some ecosystems could bemanaged in ways that would promote the decomposition ofcritical pollutants, like polycyclic aromatic hydrocarbon andmethylmercury in some wetlands where the degree of floodingcould be controlled [140]. Management of aquatic ecosystemsto enhance polycyclic aromatic hydrocarbon decompositionrequires a knowledge of the environmental conditions that reg-ulate the speed of degradation and the use of mass-balancemodeling, as done by Su et al. [141] in the case of the Lower


Fox River (MI, USA) and in shallow coastal marine sediments[142].

Some species can play key ecosystem roles in nutrient trans-fer, trophic webs, etc. If pollutants stress these species, eco-system functions can be altered and other life forms can beindirectly affected. It has been shown that the consumptionrate of Gammarus sp., an amphipod feeding on sediment deadplant material, is restricted when exposed to plant debris con-taminated with motorway runoff [143]. This is probably dueto increased amphipod mortality and a reduction in voluntaryintake because Hyphomicetae fungi do not colonize pollutedplant material. Gammarus spp. is the main organism in sed-iment organic recycling [144], and a limitation in its activitycan delay or block the availability of nutrients to other or-ganisms.

Ecosystem models can provide insights into complex com-munity–ecosystem interactions and responses to natural andanthropogenic disturbances. Rivkin et al. [145] reported resultsof applying a total-system marine pelagic model [146] to in-terpret the effects of added NH4 and dissolved organic carbonin produced water from oil drilling operations on the structureof marine phytoplankton. Small phytoplanktons increase whenthe flows of these materials increase, which in turn causeslimitation to the growth of selective planktonic grazers, likethe copepods, which are not able to graze on small cells. Othereffects, like an increased flow of matter to demersal systemsand a shift in the relative importance of pelagic and demersalfisheries, could also result.

Bioconcentration in the trophic web is also an importantissue in considering ecosystem processes. Because trophic re-lations are characterized by a high degree of variability, theiranalysis is probably best approached with probabilistic tech-niques [147]. From the point of view of developing regulatorycriteria, it is to be expected that setting acceptable limits forecosystem processes like trophic activity or decompositionrates might pose considerable difficulties [148].

The low sensitivity of community diversity indices as endpoints of complex toxin–organism interactions can mask theircorrelation to chemical exposure estimates. Hartwell et al.[149] did not find significant correlations between chemicalexposures in the water column 1 sediments and in severalbioassays including weeds, fishes, copepods, bacteria, etc., andfish diversity indices in surveys at the South River (MD, USA).

CONCLUSIONS

Recent ecotoxicological work across scales–levels of or-ganization emphasized scaling up from the individual to thepopulation level. In many cases, the population models useddid not incorporate the current state of the art in biologicalmodeling. Most models used are deterministic and spatiallyunexplicit. Migration and transgeneration effects are seldomconsidered. An improved model to interpret ecotoxic effectsat a higher level of refinement is the PARET model recentlydeveloped for application in agroecosystem environments. Anext generation of models of this type will probably incor-porate formal treatments of population dynamics, includinglife-history changes in body weight, sublethal end points otherthan reproductive capacity, secondary exposure routes, andindirect effects among organisms like those arising from tro-phic relations.

The evaluation of ecotoxic effects at the population levelwill probably evolve in the near future toward incorporatingmore sophisticated techniques of population biology, including

the analysis of sublethal and transgeneration end points, theanalysis of spatial environmental variability, as well as theanalysis of indirect effects among organisms. These will prob-ably require the use of specific tests for sublethal effects likethose deriving from endocrine disrupting and modulatingchemicals in the parental and its successive generations.

Upscaling at the community level is less developed. Usualindices in community ecology (diversity, evenness) do notseem to be relevant in describing toxicological effects at thecommunity level, mostly of an indirect nature. The interpre-tation of ecotoxic processes at the community level shouldprobably be based on corresponding simulation models. Thismight in turn require a modeling approach at the stage ofexperimental design in order to be able to translate the ob-served responses in terms of the trophic relations existingamong organisms.

Ecosystem studies indicate that the consideration of trophicrelations and top-down effects is important in understandingcommunity structure, which can in turn modify the distributionof pollutants in various environmental phases. Again, simu-lation models seem to be the necessary and adequate tool tofully understand the outcomes of mesocosm or real-world ex-periments. Existing ecosystem-level models of the aquatic en-vironment seem to be adequate to interpret pollutant partitionand effects.

Acknowledgement—Some results from the author were generated inthe frame of Project PIP 956 Consejo Nacional de InvestigacionesCientıficas y Tecnicas (Argentina) and Programa para Sanidad Citrı-cola de la Prov. de Misiones, Secretary of Agriculture, Argentina.Comments of two anonymous reviewers were constructive in pre-paring a final version.

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