Assessing the Impact of Multiple Stressors on Aquatic Biota: The

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Assessing the Impact of Multiple Stressors on Aquatic Biota: The Receptor’s Side Matters H. Segner,*,† M. Schmitt-Jansen,‡ and S. Sabater§,∥ †

Centre for Fish and Wildlife Health, Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty, University of Bern, PO Box 8466, CH-3001 Bern, Switzerland ‡ Helmholtz-Centre for Environmental ResearchUFZ, Department Bioanalytical Ecotoxicology, Permoserstrasse 15, 04318 Leipzig, Germany § Catalan Institute for Water Research (ICRA), Parc Científic i Tecnològic de la Universitat de Girona, Carrer Emili Grahit 101, Edifici H2O, 17003 Girona, Spain ∥ Institute of Aquatic Ecology, University of Girona, Campus de Montilivi, 17071 Girona, Spain derived from effect threshold concentrations determined in laboratory toxicity tests.1 This approach neglects the fact that toxic chemicals in the environment do not act in isolation, but their impact on biota is modulated by the presence of other biotic and abiotic stressors.2−8 Interactions can take place both on the exposure and on the effect side9,10 and can lead to significant shifts in chemical toxicity.11 As an example, climate change-related alterations of environmental temperatures influence environmental transport and persistence of chemicals, as well as chemical uptake and bioaccumulation, transfer along foodwebs, and sensitivity of species and communities to the toxicants.12−15 Vice versa, exposure to chemical stressors can modify the response of biological systems to nonchemical Aquatic ecosystems are confronted with multiple stress factors. (biological or physical) stressors.15 For instance, chemical Current approaches to assess the risk of anthropogenic exposure modulates the susceptibility of organisms to infectious stressors to aquatic ecosystems are developed for single pathogens.7,16−18 Importantly, the cumulative effects of several stressors and determine stressor effects primarily as a function stressors may differ markedly from effects of the single of stressor properties. The cumulative impact of several stressors19−24 and can result in nonlinear environmental effects stressors, however, may differ markedly from the impact of and ecological surprises.25−27 That said, it is obvious that the single stressors and can result in nonlinear effects and concepts and approaches suitable for the risk assessment of ecological surprises. To meet the challenge of diagnosing and single chemical stressors cannot be directly transferred to predicting multiple stressor impacts, assessment strategies multiple stressor assessment, but that a new framework needs should focus on properties of the biological receptors rather to be developed for this purpose. than on stressor properties. This change of paradigm is required In the following, we will discuss why hazard and risk because (i) multiple stressors affect multiple biological targets assessment of multiple stressors is different to that of chemical at multiple organizational levels, (ii) biological receptors differ in their sensitivities, vulnerabilities, and response dynamics to stressors and which implications this has for the assessment the individual stressors, and (iii) biological receptors function concepts. Our central hypothesis is that moving from single as networks, so that actions of stressors at disparate sites within stressor assessment to multiple stressor assessment requires the network can lead via indirect or cascading effects, to moving from a focus on stressor properties to an increasing unexpected outcomes. focus on the properties of biological receptors. Some Terminology. As a basis for the following discussion, INTRODUCTION several terms are defined. A first term is the “biological Among the environmental stressors potentially impacting receptor”, which here is understood as any biological system structures and functions of ecosystems, ecotoxicology deals that can be impacted by stressors, regardless of its biological with the effects of toxic chemicals on biota. Confronted with complexity, ranging from molecular entities to ecological the complexity of the biosphere, reductionist concepts have communities. Biological receptors are characterized by “traits”, been established to assess the risk of contaminants to which are intrinsic molecular, physiological (e.g., detoxification capabilities) and ecological (e.g., feeding types, reproductive ecosystems and to protect them against adverse effects of strategy) properties of receptors that drive their response man-made pollution. These concepts build mainly on chemical capacity and behavior to stressors.28,29 A further relevant term benchmarking, that is comparison of estimates of environis “network”, which is understood as a set of nodes of biological mental concentrations of the chemicals against those considered to be not harmful to biota, the so-called “predicted Published: June 6, 2014 no effect concentrations” (PNEC). Typically, PNECs are

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receptors linked through functional processes. For instance, the nodes in a molecular network would be genes and proteins which interact via regulatory cascades. In an ecological network, such as a foodweb, the nodes consist of species linked by trophic relationships and nutrient as well as energy flow. Importantly, the linkages and interactions between nodes can lead to buffering and resilience of the network toward stressors. The term “stressor” refers to any external abiotic or biotic factor that moves a biological system out of its normal operating range.30 Stress is the internal response of the biological system to the stressor. The stressor impact depends on stressor intensity, timing, and duration, as well as on the physiological or ecological properties of the receptor. The stress response may be transient and involves adaptive or compensatory mechanisms (e.g., physiological acclimation at the individual level or replacement of sensitive versus tolerant species at the community level). As adaptive or compensatory responses to stressors cost energy,30 stress means a chronic drain of metabolic energy from biological systems. Stress can be relieved by returning to the original homeostatic state, or by establishing a new stable state. Importantly, the stress response of a biological system should be seen as multivariate response. Changing the Perspective: From the Stressor to the Receptor Side. Current ecotoxicological hazard and risk assessment evaluates toxicity primarily from the chemical’s point of view. It neglects possible combination effects with other stressors and the fact this interaction can significantly change chemical toxicity.3,11,15 In addition, it neglects the role of receptor properties in the toxic response, for instance, the adaptive and compensatory capacities of biological receptors such as molecular networks, populations, or ecological communities.15,28−32 Traditionally, ecotoxicology determines the inherent toxicity of chemicals using single species tests and a limited set of apical end points (survival, growth, reproduction). In a simplified aquatic food chain perspective, algae are selected to represent producers, daphnids for primary consumers, and fish for secondary consumers.1 Biological effects of chemicals are described as a function of chemical dose, structure, and physicochemistry,1 and thus, chemical toxicity can be predicted on the basis of chemical structure and physicochemistry, as it is exemplified in (quantitative) structure activity relationships (QSAR). Standardized laboratory testing conditions seek to eliminate the possible influence of nonchemical stressors on chemical toxicity. In this perspective, toxicity is understood as an intrinsic property of the chemical, and the influence of receptor properties is reflected mainly through species-specific slopes of the dose response curve or the QSAR regression. Which challenges do arise when moving from chemical risk assessment to risk assessment of multiple stressors? A first complication is the fact that chemical, biological, and physical stressors differ in their inherent energy, as well as temporal and spatial scales.32−34 Smaller-scale or local stressors (e.g., chemical pollution) differ from larger-scale stressors (e.g., global warming) in their duration and intensity (Figure 1), implying unequal sizes of effects upon species responses, species diversity, as well as ecosystem functioning and recovery.33−37 These differences between stressors in terms of intensity, frequency, temporal, and spatial scales (Figure 1) is one of the complicating factors in the assessment of the combined effects of stressors. A next level of complexity arises from the diversity of biological responses to the various stressors. Depending on

Figure 1. Chemical, biological, and physical stressors differ in their inherent properties which are relevant for the biological receptors. The intensity and frequency of each type of stressors influence reversibility or irreversibility of their effects.

physiological and ecological traits of the receptors,38−43 as well as on the temporal changes in their traits and characteristics,44 responses of biological receptors to individual stressors can differ largely. This includes differences in dose−response behavior, in response quality as well as in sensitivity. Concentration−response curves of biological receptors can differ for different stressors,38 for instance, while toxic chemicals typically induce sigmoid concentration−response curves,1 temperature typically produces an optimum curve−differences, which complicate the analysis of combination effects of physical, biological, and chemical stressors.38,39 Also response qualities vary across biological receptors: For instance, an organism may respond to pathogen infection with an activation of the immune system, while it responds to reduced food availability with a decrease of growthhow to compare these responses and quantify possible combination effects ? For this type of problems, it would need a “common currency” which enables to convert the different responses into one common unit. Another complication originates from the fact that biological receptors differ in their sensitivity and response dynamics toward individual stressors. For instance, while a flood pulse may be a stressor for one species, it may be a dispersal factor for another species. Here, the question is how to recognize which receptors are likely to be affected by which stressor and which stressor combination? Finally, biological systems are organized in networks, be it at the molecular or the ecological level. Multiple stressors may have different primary targets, so that at a first glance one would not expect a combination effect of these stressors. However, the action of one stressor on a specific node in the network can alter the processes connecting this node to other nodes, and this can change network functioning as well as the stressor tolerance of other nodes in the network. Network-mediated combination effects may explain why in a number of studies surprising, nonlinear outcomes of multiple stressor exposures were observed, which could not be extrapolated from the single stressor effects.23−27,45 The discussion above highlights the problems in assessing multiple stressor effects. The responses of biological receptors to stressors vary with biological scale, physiological and ecological traits, and receptor interactions and network organization. These factors are already a challenge in assessing single stressor effects, but the problem aggravates for multiple stressor effects. As indicated by Hooper et al.,15 it is impossible to collect empirical data on all possible combinations and 7691



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interactions, but guidance would be needed to find the way through the complexity of multiple stressor assessment, as well as to move from empirical to predictive approaches. Placing focus on the receptor rather than on the stressor side could provide such guidance. It is the receptor side that can provide unifying effect parameters that express diverse qualities of different stressors in one common currency; we will exemplify this for biological energy metabolism. A next argument why it is the receptor side that matters is the fact that biological receptors differ in their physiological and ecological tolerance toward different stressors. Although this may appear trivial at first glance, it means that two receptors can largely differ in their response toward the same stressor combination. Knowledge of such differences is essential to identify which stressor combinations are likely to affect specific receptors. Finally, multiple stressor combinations do not only act through direct effects on individual receptors, but they also can have indirect effects, either by modulating the response capacity of an individual stressor (e.g., toxicant exposure may increase sensitivity to pathogens, see above) or by modulating the response capacity of another receptor (e.g., via food web relationships). Also here, knowledge of the network organization of biological receptors is essential to assess the combined impacts of multiple stressors. Assessing the Impact of Multiple Stressors Needs Common Effect Metrics. The fact that multiple stressors can have both direct and indirect effects on different receptors and on receptor interactions complicates the assessment of their combined effects. Lethality, for instance, is useful as an effect metrics for the toxic impact of chemical mixtures. However, lethality is inappropriate to quantify the joint effects of chemical exposure and habitat change. To overcome such difficulties in measuring combined actions of different types of stressors, effects assessment of multiple stressors requires a common descriptor, which is able to measure effects of chemical, physical as well as biological stressors. Energy investment is such a “common currency” of biological receptors, as it is involved in almost all structural and functional responses to stressors at all levels of biological organization.8,46 The energy costs of organisms and communities increase under the presence of stressors, and this increase relates to the intensity and duration of stressor impacts, rather than to the nature of the stressors. Thus, energy parameters appear to be suitable to integrate the effects of different stressors into one currency, and to extrapolate effects across levels of biological organization. Importantly, measures of energy metabolism reflect also tradeoffs between stressor impacts: under the influence of stressors, an increasing part of the available energy is allocated to adaptive or compensatory measures, implicating trade-offs with other energy-consuming processes.46−48 In this way, the energy metrics could be used to develop quantitative models that would predict the combined effects of multiple stressors. Numerous studies exemplified the value of energy metabolism as common currency to integrate stressor effects and their trade-offs. Examples include the study of Ng and Carla49 who demonstrated how impacts by global warming and by xenobiotics on fish are linked via energy metabolism, or the study of Laskowski et al.11 who used energy metabolism to assess combined temperature and phenanthrene effects on potworms (Enchytraeus doerjesi). Anestis et al.50 used energy parameters to unravel the combination effects of seawater temperature and parasites on Mytilus galloprovincalis, Jokela et al.51 could explain the combination effect of parasites, anoxia,

and starvation on snails on the basis of energy parameters, and Porter et al.52 modeled by means of energy parameters the combination effects of elevated temperature and salinity on coral production in Florida Bay. Practical measurement of energy metabolism can be achieved in various ways, for instance, through calorimetry, respirometry, or by determining photosynthesis rates (e.g., ref 47), but also by such easy-tomeasure parameters like body growth. An excellent example is provided by the study of Coors and De Meester,5 who assessed the combination effects of three stressors, predation threat, parasitism, and pesticide exposure, on Daphnia magna by measuring the investments of the test animals in growth (age and size at maturity) and in reproduction (offspring size and number). Changes in the ratios of uptake, production, and loss of energy can be quantified in models, such as the Dynamic Energy Budget (DEB),46 which provide quantitative estimates of the energy costs of organism responses to stressors. An example is provided by the study of Petter et al.54 who employed DEB analysis to assess the combined effects of alterations in temperature and food supply on Corbicula f luminea. In addition, these authors demonstrated how integration of DEB data into a physiologically based population model enables prediction of population-level consequences of the combined activity of stressors. Such models allow to extrapolate from altered energy flow at the organism level to altered population growth rates under consideration of life history attributes.46,55 Thus, energy metabolism does not only support the quantitative integration of joint stressor effects within one level of biological organization, but also across different levels of hierarchy. Assessing the Impact of Multiple Stressors Needs Knowledge on Receptor-Specific Sensitivities and Vulnerabilities. Biological receptors differ in their inherent sensitivity to stressors. The sensitivity of a species to a given stressor is largely determined both by its physiological reaction norms and its ecological life history characteristics.56,57 In ecotoxicology, species sensitivity distributions (SSD) are used to map the variation of species sensitivities to chemicals.54,58 This approach is suitable for nonchemical stressors as well, and is promising for combined stressor assessments, as recently shown by Verbrugge et al.59 However, the SSD approach is mostly descriptive, that is, it does not explain why a certain species is sensitive or tolerant. For multiple stressor assessment, it will be crucial to move from a descriptive species identity approach, as currently used in SSD, to explanatory approaches which integrate physiological and ecological traits of species (e.g., refs 43, 57, and 60). Trait-based approaches such as the Species At Risk Index (SPEAR) have been implemented as indicator systems for toxic impacts.61,62 However, it is important to keep in mind that traits are not invariant, but show phenotypic plasticity, for example, through physiological acclimation or the impact of other stressors, and they can vary over life history.28,63 The response of biological receptors to stressors depends not only on intrinsic sensitivity, but on additional factors, for example, likelihood of stressor exposure, or recovery potential/ resilience. The composite of these parameters has been named vulnerability.54,64 Both sensitivity and vulnerability information are needed to diagnose or predict which receptors are likely to be impacted by which stressor combinations. Assessing the Impact of Multiple Stressors Needs to Consider Interactions within Receptor Networks. In 7692



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ing them more susceptible to parasite infections. At the same time, the agrochemicals favored snail intermediate hosts of the parasites, thereby increasing the infection pressure to the amphibians. Thus, both direct and indirect effects contributed to the ecological outcome of the stressor combination. Importantly, multiple stressor interactions can also lead to buffering effects in that they promote genetic or phenotypic adjustments of receptors. This has been well studied for communities, where stressors may cause a rearrangement of species composition (or of its overall physiological functioning) in that stressor-sensitive species are replaced by stressortolerant ones. In ecotoxicology, this has been formulated in the PICT (pollution induced community tolerance) concept,69 which assumes that a community will shift toward a more tolerant community when stressors exert a selection pressure. However, induced tolerance may come at a cost, as species displacement may result in the loss of diversity and functions of the biological community, and therefore in impaired ecosystem functioning and stability.32,45 Also at the organism level, induced tolerance comes at a cost, since energy investment into protective mechanisms necessitates trade-offs in other processes. Given that receptors differ in their sensitivity and vulnerability to stressors, and that complex stressor interactions occur in receptor networks, it is not surprising that exposure of biota to multiple stressors often leads to unexpected effects. Generally, while the combined effects of chemicals are often additive,40 available evidence indicates that the combination of chemical with nonchemical stressors often result in more-thanadditive effects what can give rise to “ecological surprises”.22,25−27,70

evaluating the combined effects of stressors, we have to discriminate basically two scenarios: in the first scenario, two stressors, for example, a physical and a chemical stressor, may target the same trait of a biological receptor (receptor A in Figure 2). In this case, the combination effect is the result of the

Figure 2. Combination effects of multiple stressors via receptor networks. In this example,the physical stressor interferes with receptor B and one (physiological or ecological) trait of receptor A, the biological stressor impacts receptor C and one trait of receptor A, and the chemical stressor impacts only receptor A but all three traits of this receptor (for instance, the chemical may act on the endocrine system, the immune system, and the growth system). The overall effect of the chemical stressor arises as a combination of the three individual actions and their interactions. In addition, the response capability of receptor A to the chemical stressor can be modulated by the fact that this receptor is also directly impacted by the physical and the biological stressors. These stressors may also indirectly modulate the response capability of receptor A, in that their effect on receptors B and C results in altered interactions with receptor A. For instance, receptor B may be a prey species of receptor A, and the physical stressor may reduce abundance of receptor B. This would impair the nutritional basis of receptor B and is likely to render it more sensitive to the toxic effect of the chemical stressor.

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CONCLUSIONS Chemical contamination is one of the dominant stressors in many river basins worldwide. With improvements of water quality over the last decades, the importance of stressors other than chemicals for deterioration of aquatic ecosystems is becoming more evident. The ecological degradation of aquatic systems is increasingly perceived to result from the cumulative impact of multiple anthropogenic stressors (e.g., refs 20, 22, 27, 71, and 72). In fact, as highlighted by Tockner et al.,73 multiple stressor scenarios prevail for more than 150 European catchments. This reality does not agree with current approaches of ecotoxicological risk assessment which focus on chemical stressors only.8,35 While for chemical risk assessment, the focus on the stressor properties may hold, this is no longer appropriate for multiple stressor assessment, since the stressors are too diverse in their biologically relevant properties. To overcome this problem, increasing attention should be given to receptor properties in assessing the combined effects of multiple stressors. Practically, a tiered or phased approach may be followed (Figure 3). A first action would be to establish an inventory of the stressors, wherein they are evaluated with respect to their potential importance and possible causative relation to biological changes. Through the inventory, a hierarchy of stressors may be established, pointing to those stressors that are suspected to be the main drivers of ecological change in the studied system (e.g., ref 52). The inventory of stressors is a standard approach in risk assessment35,74 and provides the basis to the next step, the inventory of potentially af fected biological receptors. This steps aims to identify those biological receptors which are likely to be responsive to the key stressors. This

direct effect of the two stressors on the same biological target. In the second scenario, the stressors have different targets. For instance, the chemical stressor may impact receptor A, and this leads to an altered interaction with receptor B, and this in turn may modulate the response capacity of receptor B to the physical stressor. In this case, the combination effect arises from an indirect interaction.53,64−68 The classical ecological example of such indirect actions are bottom-up or top-down effects of stressors in foodwebs, for example, herbicide-induced reduction in phytoplankton biomass impairs the nutritional condition of the phytoplankton consumers and thereby impairs their response capacity to other stressors.68 An example of combination effects arising from interactions within physiological networks is presented inthe study of Wenger et al.18 who exposed fish to an estrogen concentration which did not cause any adverse effect, however, when the estrogen-exposed fish were challenged by a pathogen, they showed significantly higher mortalities than control fish. Apparently, the estrogen exposure impacted through endocrine-immune network interactions the immunocompetence of the fish and thereby reduced their capacity for pathogen defense. Field studies illustrate how complex multistressor interactions can be. Rohr et al.,66 for example, observed that the decline of the amphibian Rana pipiens was correlated to both agrochemical exposure and parasite infection. One of the agrochemicals had a direct immunosuppressive effect on the amphibians, thereby render7693



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network maps, that is, understanding which receptors or receptor processes are interlinked, as well as comprehending the network pathways through which the stressor effects on one specific receptor can be propagated to other receptors.65,78 Network interactions as a mechanism underlying combination effects of multiple stressors occur both at the molecularphysiological and at the ecological level. Ecotoxicology for long has been focusing on apical, whole-organism end points as they are input parameters for demographic processes. Only more recently, the value of understanding toxic mechanisms at the suborganism level for addressing uncertainties in risk assessment, for grouping of chemicals or for extrapolations has been recognized. It is for this reason why we consequently emphasized throughout this Feature the stressor interactions and effects both at the molecular−physiological and the ecological level (see Figures 2 and 3). The final step would be to integrate the accumulated information from the individual steps on stressor characteristics, receptor sensitivities and network interactions. This decision process requires utilization of sophisticated data analytical tools, for instance, epidemiological studies, modeling approaches such as matrix- and ranking modeling, or structural equation modeling (e.g., refs 35, 77, and 79). In addition to statistics, however, for the foreseeable future, decision making will still depend to a large extent on expert knowledge of mechanistic and ecological processes. The concepts discussed in this essay are indeed not revolutionary, but evolutionary. Here, we may learn a lesson from the adverse outcome pathway (AOP) concept, which was recently introduced into toxicology. The AOP concept builds on existing ideas and approaches but evolves them further into a consistent framework for organizing and structuring data and information on stressor effects.15,79 Similarly, for multiple stressor assessment, the suggested framework will give increasing emphasis on receptor-driven approaches to deal with the diversity in intensity, specificity, temporal, and spatial scale of stressors.

Figure 3. Possible tiered approach to multistressor assessment.

analysis can be done at the molecular-physiological levels, for example, by identifying which disease pathways might be responsive, it can be done at the species level, for instance, by using stressor-specific SSDs,59 and it can be done at the community level, for example, by identifying community traits which make the community vulnerable to the stressors.43,64 Admittedly, many of the required tools are not yet in place, and the necessary data and information bases are limited and dispersed, however, 20 years ago, available information and databases on chemical toxicity were similarly limited, but they developed as soon as the concepts of chemical risk assessment were established and requirements became clear. It is the concept which is first, and the database will follow. Having identified candidate stressors and receptors, the next step is to evaluate the “multistressor response profile” of the receptors. This includes the evaluation of possible stressor combination effects using, for instance, combination experiments in the laboratory (refs 2, 5, and 52−54; see also reviews 3, 7, and 11), or by applying mechanistic knowledge in weightof-evidence approaches, as has been done in many field studies to unravel multistressor effects (e.g., refs 72 and 75−77; see also reviews in refs 10 and 11). Such analyses have to take into account that sensitivities and vulnerabilities of biological receptors are not fixed, but variable; they can change temporally, for instance, during the lifespan of an organism, they can differ between life stages, or for an ecosystem, they can change with the seasonal phenotype, etc.44 Also, the multistressor impact on a specific receptor must not be seen in isolation, but, as discussed above, the effects can be modulated via network interactions. For instance, Petter et al.,54 when studying the combined effects of temperature and food availability on C. f luminea found that the temporal interaction between the two stressors was the most important determinant for the combination effect. Excellent examples on the importance of interactions for multistressor responses at the community level are provided in the studies of Flöder et al.65 and Rohr et al.66 To obtain an overview on possibly relevant interactions, again an inventory would be helpful, based on

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AUTHOR INFORMATION

Corresponding Author

*Tel: +41 31 631 2441 or 2465. Fax: +41 31 631 2611. E-mail: [email protected]. Notes

The authors declare no competing financial interest. Biographies Helmut Segner is professor at the Veterinary Faculty of the University of Bern and heads the Centre for Fish and Wildlife Health. His recent research has focused on the interactions between abiotic environmental stressors, infectious pathogens, and the adaptive response capabilities of fish. Dr. Mechthild Schmitt-Jansen is Scientist in the Helmholtz-Centre for Environmental ResearchUFZ, Germany in the research field of aquatic ecotoxicology. In her research, she investigates the community ecology of stream biofilms. Further research interests include the metabolic responses of photoautotrophic organisms to phytotoxicants. Sergi Sabater is Professor of Ecology at the University of Girona and senior researcher at the Catalan Institute for Water Research (ICRA). His research interest is on fluvial ecosystems and, particularly, on the ecology and ecotoxicology of river biofilms, the metabolism and functioning of fluvial systems, and the effects of global change and water scarcity on fluvial systems. 7694



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