Resilience to heat waves in the aquatic snail Lymnaea stagnalis: Additive and interactive effects with micropollutants

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Multiple stressors and multifunctionality: limited effects on an illuminated benthic system

The bulk of experiments that study stressor effects on ecosystem functioning consider only individual functions one at a time, and such narrow focus may well bias our understanding of the overall impact on ecosystem functioning. We used data from six published experiments in which marine illuminated sediment systems were exposed to nutrient enrichment, toxicants, sedimentation and warming, either alone or in combination. Measured functions were primary production, community respiration, inorganic nitrogen and phosphorus fluxes, and autotrophic biomass. We calculated two indices of multifunctionality that simultaneously considered all six functions: (i) a weighted average level of the functions and (ii) the number of functions that simultaneously exceed a critical threshold level. Stressors affected individual functions both positively and negatively, but multifunctionality was generally unaffected by both single and joint stressors. The filtering capacity of coastal illuminated sediment systems thus appears resilient to exposure to moderate levels of multiple stressors, most probably due to the robustness of the benthic microalgal community. We recommend using a multifunctionality approach in future studies on cumulative stressor effects on ecosystem functioning, particularly when considering functions related to ecosystem services.     

Conceptualizing ecosystem tipping points within a physiological framework

Connecting the nonlinear and often counterintuitive physiological effects of multiple environmental drivers to the emergent impacts on ecosystems is a fundamental challenge. Unfortunately, the disconnect between the way “stressors” (e.g., warming) is considered in organismal (physiological) and ecological (community) contexts continues to hamper progress. Environmental drivers typically elicit biphasic physiological responses, where performance declines at levels above and below some optimum. It is also well understood that species exhibit highly variable response surfaces to these changes so that the optimum level of any environmental driver can vary among interacting species. Thus, species interactions are unlikely to go unaltered under environmental change. However, while these nonlinear, species‐specific physiological relationships between environment and performance appear to be general, rarely are they incorporated into predictions of ecological tipping points. Instead, most ecosystem‐level studies focus on varying levels of “stress” and frequently assume that any deviation from “normal” environmental conditions has similar effects, albeit with different magnitudes, on all of the species within a community. We consider a framework that realigns the positive and negative physiological effects of changes in climatic and nonclimatic drivers with indirect ecological responses. Using a series of simple models based on direct physiological responses to temperature and ocean pCO₂, we explore how variation in environment‐performance relationships among primary producers and consumers translates into community‐level effects via trophic interactions. These models show that even in the absence of direct mortality, mismatched responses resulting from often subtle changes in the physical environment can lead to substantial ecosystem‐level change.     

Testing local and global stressor impacts on a coastal foundation species using an ecologically realistic framework

Despite the abundance of literature on organismal responses to multiple environmental stressors, most studies have not matched the timing of experimental manipulations with the temporal pattern of stressors in nature. We test the interactive effects of diel‐cycling hypoxia with both warming and decreased salinities using ecologically realistic exposures. Surprisingly, we found no evidence of negative synergistic effects on Olympia oyster growth; rather, we found only additive and opposing effects of hypoxia (detrimental) and warming (beneficial). We suspect that diel‐cycling provided a temporal refuge that allowed physiological compensation. We also tested for latent effects of warming and hypoxia to low‐salinity tolerance using a seasonal delay between stressor events. However, we did not find a latent effect, rather a threshold survival response to low salinity that was independent of early life‐history exposure to warming or hypoxia. The absence of synergism is likely the result of stressor treatments that mirror the natural timing of environmental stressors. We provide environmental context for laboratory experimental data by examining field time series environmental data from four North American west coast estuaries and find heterogeneous environmental signals that characterize each estuary, suggesting that the potential stressor exposure to oysters will drastically differ over moderate spatial scales. This heterogeneity implies that efforts to conserve and restore oysters will require an adaptive approach that incorporates knowledge of local conditions. We conclude that studies of multiple environmental stressors can be greatly improved by integrating ecologically realistic exposure and timing of stressors found in nature with organismal life‐history traits.     

Experimental nitrogen and phosphorus enrichment stimulates multiple trophic levels of algal and detrital-based food webs: a global meta-analysis from streams and rivers

Anthropogenic increases in nitrogen (N) and phosphorus (P) concentrations can strongly influence the structure and function of ecosystems. Even though lotic ecosystems receive cumulative inputs of nutrients applied to and deposited on land, no comprehensive assessment has quantified nutrient-enrichment effects within streams and rivers. We conducted a meta-analysis of published studies that experimentally increased concentrations of N and/or P in streams and rivers to examine how enrichment alters ecosystem structure (state: primary producer and consumer biomass and abundance) and function (rate: primary production, leaf breakdown rates, metabolism) at multiple trophic levels (primary producer, microbial heterotroph, primary and secondary consumers, and integrated ecosystem). Our synthesis included 184 studies, 885 experiments, and 3497 biotic responses to nutrient enrichment. We documented widespread increases in organismal biomass and abundance (mean response = +48%) and rates of ecosystem processes (+54%) to enrichment across multiple trophic levels, with no large differences in responses among trophic levels or between autotrophic or heterotrophic food-web pathways. Responses to nutrient enrichment varied with the nutrient added (N, P, or both) depending on rate versus state variable and experiment type, and were greater in flume and whole-stream experiments than in experiments using nutrient-diffusing substrata. Generally, nutrient-enrichment effects also increased with water temperature and light, and decreased under elevated ambient concentrations of inorganic N and/or P. Overall, increased concentrations of N and/or P altered multiple food-web pathways and trophic levels in lotic ecosystems. Our results indicate that preservation or restoration of biodiversity and ecosystem functions of streams and rivers requires management of nutrient inputs and consideration of multiple trophic pathways.     

Seagrass ecosystem multifunctionality under the rise of a flagship marine megaherbivore

Large grazers (megaherbivores) have a profound impact on ecosystem functioning. However, how ecosystem multifunctionality is affected by changes in megaherbivore populations remains poorly understood. Understanding the total impact on ecosystem multifunctionality requires an integrative ecosystem approach, which is especially challenging to obtain in marine systems. We assessed the effects of experimentally simulated grazing intensity scenarios on ecosystem functions and multifunctionality in a tropical Caribbean seagrass ecosystem. As a model, we selected a key marine megaherbivore, the green turtle, whose ecological role is rapidly unfolding in numerous foraging areas where populations are recovering through conservation after centuries of decline, with an increase in recorded overgrazing episodes. To quantify the effects, we employed a novel integrated index of seagrass ecosystem multifunctionality based upon multiple, well-recognized measures of seagrass ecosystem functions that reflect ecosystem services. Experiments revealed that intermediate turtle grazing resulted in the highest rates of nutrient cycling and carbon storage, while sediment stabilization, decomposition rates, epifauna richness, and fish biomass are highest in the absence of turtle grazing. In contrast, intense grazing resulted in disproportionally large effects on ecosystem functions and a collapse of multifunctionality. These results imply that (i) the return of a megaherbivore can exert strong effects on coastal ecosystem functions and multifunctionality, (ii) conservation efforts that are skewed toward megaherbivores, but ignore their key drivers like predators or habitat, will likely result in overgrazing-induced loss of multifunctionality, and (iii) the multifunctionality index shows great potential as a quantitative tool to assess ecosystem performance. Considerable and rapid alterations in megaherbivore abundance (both through extinction and conservation) cause an imbalance in ecosystem functioning and substantially alter or even compromise ecosystem services that help to negate global change effects. An integrative ecosystem approach in environmental management is urgently required to protect and enhance ecosystem multifunctionality.     

Exposure to a heat wave under food limitation makes an agricultural insecticide lethal: a mechanistic laboratory experiment

Extreme temperatures and exposure to agricultural pesticides are becoming more frequent and intense under global change. Their combination may be especially problematic when animals suffer food limitation. We exposed Coenagrion puella damselfly larvae to a simulated heat wave combined with food limitation and subsequently to a widespread agricultural pesticide (chlorpyrifos) in an indoor laboratory experiment designed to obtain mechanistic insights in the direct effects of these stressors in isolation and when combined. The heat wave reduced immune function (activity of phenoloxidase, PO) and metabolic rate (activity of the electron transport system, ETS). Starvation had both immediate and delayed negative sublethal effects on growth rate and physiology (reductions in Hsp70 levels, total fat content, and activity levels of PO and ETS). Exposure to chlorpyrifos negatively affected all response variables. While the immediate effects of the heat wave were subtle, our results indicate the importance of delayed effects in shaping the total fitness impact of a heat wave when followed by pesticide exposure. Firstly, the combination of delayed negative effects of the heat wave and starvation, and the immediate negative effect of chlorpyrifos considerably (71%) reduced larval growth rate. Secondly and more strikingly, chlorpyrifos only caused considerable (ca. 48%) mortality in larvae that were previously exposed to the combination of the heat wave and starvation. This strong delayed synergism for mortality could be explained by the cumulative metabolic depression caused by each of these stressors. Further studies with increased realism are needed to evaluate the consequences of the here‐identified delayed synergisms at the level of populations and communities. This is especially important as this synergism provides a novel explanation for the poorly understood potential of heat waves and of sublethal pesticide concentrations to cause mass mortality.     

Subsidy‐stress and multiple‐stressor effects along gradients of deposited fine sediment and dissolved nutrients in a regional set of streams and rivers

1. Stream managers need to understand relationships between multiple stressors and ecological responses. We examined responses of benthic invertebrates and algae along two land‐use‐related stressor gradients of concern in running waters. Our correlative study of the consequences of augmented deposited fine sediment and nutrient concentrations was conducted in a regional set of streams and rivers monitored by a water management authority in New Zealand and incorporated a wide range of catchment geologies and stream orders. 2. We used multiple linear regression analysis and an information‐theoretic approach to select the best predictive models for our biological response variables by testing multiple competing hypotheses that include nonlinear subsidy‐stress relationships and interactive effects between the two stressors. 3. Patterns consistent with a subsidy‐stress response to increasing dissolved inorganic nitrogen concentration were found for the relative abundances of the common invertebrate genera Pycnocentrodes and Deleatidium and for the relative abundance of total individuals in the EPT orders (Ephemeroptera, Plecoptera, Trichoptera). 4. Fine sediment seemed the more pervasive stressor, apparently counteracting and overwhelming any initial subsidy effect of increased nutrients, and accounting for more of the variance in biological response variables. Relationships with high nutrient concentrations were weaker and modelled with less certainty, probably reflecting the indirect modes of action of nutrients compared to those underlying sediment effects. Nevertheless, in several cases, the models indicated that nutrients interacted synergistically with fine sediment, lending further weight to the conclusion that managers need to address both stressors to achieve the best outcomes.     

Biotic interactions modify multiple‐stressor effects on juvenile brown trout in an experimental stream food web

Agricultural land use results in multiple stressors affecting stream ecosystems. Flow reduction due to water abstraction, elevated levels of nutrients and chemical contaminants are common agricultural stressors worldwide. Concurrently, stream ecosystems are also increasingly affected by climate change. Interactions among multiple co‐occurring stressors result in biological responses that cannot be predicted from single‐stressor effects (i.e. synergisms and antagonisms). At the ecosystem level, multiple‐stressor effects can be further modified by biotic interactions (e.g. trophic interactions). We conducted a field experiment using 128 flow‐through stream mesocosms to examine the individual and combined effects of water abstraction, nutrient enrichment and elevated levels of the nitrification inhibitor dicyandiamide (DCD) on survival, condition and gut content of juvenile brown trout and on benthic abundance of their invertebrate prey. Flow velocity reduction decreased fish survival (?12% compared to controls) and condition (?8% compared to initial condition), whereas effects of nutrient and DCD additions and interactions among these stressors were not significant. Negative effects of flow velocity reduction on fish survival and condition were consistent with effects on fish gut content (?25% compared to controls) and abundance of dominant invertebrate prey (?30% compared to controls), suggesting a negative metabolic balance driving fish mortality and condition decline, which was confirmed by structural equation modelling. Fish mortality under reduced flow velocity increased as maximal daily water temperatures approached the upper limit of their tolerance range, reflecting synergistic interactions between these stressors. Our study highlights the importance of indirect stressor effects such as those transferred through trophic interactions, which need to be considered when assessing and managing fish populations and stream food webs in multiple‐stressor situations. However, in real streams, compensatory mechanisms and behavioural responses, as well as seasonal and spatial variation, may alter the intensity of stressor effects and the sensitivity of trout populations.     

Compensating for delayed hatching reduces offspring immune response and increases life‐history costs

Organisms are exposed to multiple sources of stress in nature. When confronted with a stressful period affecting growth and development, compensatory responses allow the restoration of individual fitness, providing an important buffering mechanism against climatic and other environmental variability. However, tradeoffs between increased growth/development and other physiological traits are predicted to prevent these high growth and development rates from becoming constitutive. Here, we investigated how compensatory responses in growth and development affect immune responses. By using low temperature to stop embryonic development, we exposed moor frog Rana arvalis tadpoles to two levels of time‐constraints: non‐delayed hatching and 12‐day delayed hatching. In a common garden experiment, we recorded larval growth and development, as well as their immune response, measured as the inflammatory reaction after the injection of phytohaemagglutinin (PHA). Tadpoles originating from delayed hatching treatments had a lower immune response to PHA challenge than those from the non‐delayed hatching treatment. In general, tadpoles from the delayed hatching treatment reached metamorphosis faster and at a smaller size than control tadpoles. However, immune‐challenged tadpoles were not able to accelerate their development in response to delayed hatching. Our results indicate that 1) the innate immune response can be reduced in organisms undergoing compensatory developmental responses in growth and development and 2) compensatory capacity can be reduced when organisms are immunologically challenged. These dual findings reveal the complexity of handling multiple stressors and highlight the importance of examining the costs and limits of mounting an immune response in the context of increasing phenological instability ascribed to climate change.     

Environmental context determines multi‐trophic effects of consumer species loss

Loss of biodiversity and nutrient enrichment are two of the main human impacts on ecosystems globally, yet we understand very little about the interactive effects of multiple stressors on natural communities and how this relates to biodiversity and ecosystem functioning. Advancing our understanding requires the following: (1) incorporation of processes occurring within and among trophic levels in natural ecosystems and (2) tests of context‐dependency of species loss effects. We examined the effects of loss of a key predator and two groups of its prey on algal assemblages at both ambient and enriched nutrient conditions in a marine benthic system and tested for interactions between the loss of functional diversity and nutrient enrichment on ecosystem functioning. We found that enrichment interacted with food web structure to alter the effects of species loss in natural communities. At ambient conditions, the loss of primary consumers led to an increase in biomass of algae, whereas predator loss caused a reduction in algal biomass (i.e. a trophic cascade). However, contrary to expectations, we found that nutrient enrichment negated the cascading effect of predators on algae. Moreover, algal assemblage structure varied in distinct ways in response to mussel loss, grazer loss, predator loss and with nutrient enrichment, with compensatory shifts in algal abundance driven by variation in responses of different algal species to different environmental conditions and the presence of different consumers. We identified and characterized several context‐dependent mechanisms driving direct and indirect effects of consumers. Our findings highlight the need to consider environmental context when examining potential species redundancies in particular with regard to changing environmental conditions. Furthermore, non‐trophic interactions based on empirical evidence must be incorporated into food web‐based ecological models to improve understanding of community responses to global change.     

A review and meta‐analysis of the effects of multiple abiotic stressors on marine embryos and larvae

Marine organisms are simultaneously exposed to anthropogenic stressors with likely interactive effects, including synergisms in which the combined effects of multiple stressors are greater than the sum of individual effects. Early life stages of marine organisms are potentially vulnerable to the stressors associated with global change, but identifying general patterns across studies, species and response variables is challenging. This review represents the first meta‐analysis of multistressor studies to target early marine life stages (embryo to larvae), particularly between temperature, salinity and pH as these are the best studied. Knowledge gaps in research on multiple abiotic stressors and early life stages are also identified. The meta‐analysis yielded several key results: (1) Synergistic interactions (65% of individual tests) are more common than additive (17%) or antagonistic (17%) interactions. (2) Larvae are generally more vulnerable than embryos to thermal and pH stress. (3) Survival is more likely than sublethal responses to be affected by thermal, salinity and pH stress. (4) Interaction types vary among stressors, ontogenetic stages and biological responses, but they are more consistent among phyla. (5) Ocean acidification is a greater stressor for calcifying than noncalcifying larvae. Despite being more ecologically realistic than single‐factor studies, multifactorial studies may still oversimplify complex systems, and so meta‐analyses of the data from them must be cautiously interpreted with regard to extrapolation to field conditions. Nonetheless, our results identify taxa with early life stages that may be particularly vulnerable (e.g. molluscs, echinoderms) or robust (e.g. arthropods, cnidarians) to abiotic stress. We provide a list of recommendations for future multiple stressor studies, particularly those focussed on early marine life stages.     

Multiple stressor effects on coral reef ecosystems

Global climate change has profound implications on species distributions and ecosystem functioning. In the coastal zone, ecological responses may be driven by various biogeochemical and physical environmental factors. Synergistic interactions can occur when the combined effects of stressors exceed their individual effects. The Red Sea, characterized by strong gradients in temperature, salinity, and nutrients along the latitudinal axis provides a unique opportunity to study ecological responses over a range of these environmental variables. Using multiple linear regression models integrating in situ, satellite and oceanographic data, we investigated the response of coral reef taxa to local stressors and recent climate variability. Taxa and functional groups responded to a combination of climate (temperature, salinity, air‐sea heat fluxes, irradiance, wind speed), fishing pressure and biogeochemical (chlorophyll a and nutrients ‐ phosphate, nitrate, nitrite) factors. The regression model for each species showed interactive effects of climate, fishing pressure and nutrient variables. The nature of the effects (antagonistic or synergistic) was dependent on the species and stressor pair. Variables consistently associated with the highest number of synergistic interactions included heat flux terms, temperature, and wind speed followed by fishing pressure. Hard corals and coralline algae abundance were sensitive to changing environmental conditions where synergistic interactions decreased their percentage cover. These synergistic interactions suggest that the negative effects of fishing pressure and eutrophication may exacerbate the impact of climate change on corals. A high number of interactions were also recorded for algae, however for this group, synergistic interactions increased algal abundance. This study is unique in applying regression analysis to multiple environmental variables simultaneously to understand stressor interactions in the field. The observed responses have important implications for understanding climate change impacts on marine ecosystems and whether managing local stressors, such as nutrient enrichment and fishing activities, may help mitigate global drivers of change.     

A step towards understanding plant responses to multiple environmental stresses: a genome‐wide study

In natural habitats, especially in arid areas, plants are often simultaneously exposed to multiple abiotic stresses, such as salt, osmotic and heat stresses. However, most analyses of gene expression in stress responses examine individual stresses. In this report, we compare gene expression in individual and combined stresses. We show that combined stress treatments with salt, mannitol and heat induce a unique pattern of gene expression that is not a simple merge of the individual stress responses. Under multiple stress conditions, expression of most heat and salt stress‐responsive genes increased to levels similar to or higher than those measured in single stress conditions, but osmotic stress‐responsive genes increased to lower levels. Genes up‐regulated to higher levels under multiple stress condition than single stress conditions include genes for heat shock proteins, heat shock regulators and late embryogenesis abundant proteins (LEAs), which protect other proteins from damage caused by stresses, suggesting their importance in multiple stress condition. Based on this analysis, we identify candidate genes for engineering crop plants tolerant to multiple stresses.     

Effect of dung beetle species richness and chemical perturbation on multiple ecosystem functions

1. The relationship between biodiversity and ecosystem functioning is typically positive but saturating, suggesting widespread functional redundancy within ecological communities. However, theory predicts that apparent redundancy can be reduced or removed when systems are perturbed, or when multifunctionality (the simultaneous delivery of multiple functions) is considered. 2. Manipulative experiments were used to test whether higher levels of dung beetle species richness enhanced individual functions and multifunctionality, and whether these relationships were influenced by perturbation (in this case, non‐target exposure to the veterinary anthelmintic ivermectin). The four ecosystem functions tested were dung removal, primary productivity, soil faunal feeding activity and reduction in soil bulk density. 3. For individual functions, perturbation had limited effects on functioning, with only dung removal significantly (negatively) affected. Species richness did not, on its own, explain significant variation in the delivery of individual functions. In the case of primary productivity, an interaction between richness and perturbation was found: species‐rich dung beetle assemblages enhanced forage growth in the unperturbed treatment, relative to the perturbed treatment. 4. Using a composite ‘multifunctionality index’ it was found that species‐rich dung beetle assemblages delivered marginally higher levels of multifunctionality in unperturbed conditions; however, this benefit was lost under perturbation. Using a relatively new and robust method of assessing diversity–multifunctionality relationships across a range of thresholds, no significant effect of species richness on multifunctionality was found.     

When things don't add up: quantifying impacts of multiple stressors from individual metabolism to ecosystem processing

Ecosystems are exposed to multiple stressors which can compromise functioning and service delivery. These stressors often co‐occur and interact in different ways which are not yet fully understood. Here, we applied a population model representing a freshwater amphipod feeding on leaf litter in forested streams. We simulated impacts of hypothetical stressors, individually and in pairwise combinations that target the individuals' feeding, maintenance, growth and reproduction. Impacts were quantified by examining responses at three levels of biological organisation: individual‐level body sizes and cumulative reproduction, population‐level abundance and biomass and ecosystem‐level leaf litter decomposition. Interactive effects of multiple stressors at the individual level were mostly antagonistic, that is, less negative than expected. Most population‐ and ecosystem‐level responses to multiple stressors were stronger than expected from an additive model, that is, synergistic. Our results suggest that across levels of biological organisation responses to multiple stressors are rarely only additive. We suggest methods for efficiently quantifying impacts of multiple stressors at different levels of biological organisation.     

Multiple nutrients and herbivores interact to govern diversity,productivity, composition,and infection in a successional grassland

In spite of increasing awareness that interactions between herbivory and the supply rates of multiple nutrients control biodiversity, ecosystem functions and ecosystem services in ecological communities, few experimental studies have concurrently examined the independent and joint effects of multiple nutrients and mammalian consumers on these responses in natural systems. Here we quantify the independent and interactive effects of multiple concurrent changes to resources and consumers in an invaded annual grassland community in California. In a two‐year study using thirty‐seven 400‐m² plots, we examine interactions among four nutrient treatments (N, P, K and micronutrients) and a keystone herbivore (pocket gopher Thomomys bottae) on four plant community outcomes: 1) plant diversity, 2) functional group composition, 3) net biomass production, an important ecosystem function, and 4) infection risk by a group of viral pathogens shared by crop and non‐crop grasses (barley and cereal yellow dwarf viruses), an important regulating ecosystem service. We found that grassland biodiversity and infection risk were controlled by nutrient identity and supply ratio whereas nutrients interacted strongly with consumers to control grassland composition and net primary productivity. The most important insights arising from this multi‐factor experiment are that net biomass production increased with phosphorus or nitrogen supply; however, when gophers were present, nitrogen caused no net effect on biomass production. In addition, infection risk was driven by phosphorus, nitrogen and micronutrient supply. Infection in a sentinel host increased strongly with the addition of micronutrients or phosphorus; however, infection declined with increasing N/P supply ratio, indicating stoichiometric control of infection risk. Finally, in spite of manipulating multiple factors, plant species richness declined with nitrogen, alone. The importance of higher‐order interactions demonstrates that a multi‐factor approach is critical for effective predictions in a world in which anthropogenic activities are simultaneously changing herbivore abundance and the relative supply of many nutrients.     

IMMUNE RESPONSE TO PARASITISM REDUCES RESISTANCE OF DROSOPHILA MELANOGASTER TO DESICCATION AND STARVATION

Abstract In natural populations, organisms experience simultaneously biotic (e.g., competitors and parasites) and abiotic (e.g., temperature and humidity) stresses. Thus, species must have the capacity to respond to combinations of stressors. How does interaction between biotic and abiotic stress affect organismal performance? To address this question, I studied stress resistance of adult Drosophila melanogaster that survived parasitic attack (as larvae) by the parasitoid Asobara tabida. To determine the impact of genotype on stress resistance, I measured survival under desiccation and starvation of flies within isofemale (genetic) lines. Survivors of parasitism had slightly reduced survivorship compared to unparasitized relatives when both were unstressed, and this difference was exacerbated by desiccation and starvation. These results indicate multiple stressors can compound each other's individual negative effects on fitness. Moreover, isofemale lines differed in their sensitivity to environmental stress and to parasitism. Consequently, genotypic differences in sensitivity to stress may reflect differences in investment priorities between traits that promote survival over other life‐history characters.     

Describing and understanding behavioral responses to multiple stressors and multiple stimuli

Understanding the effects of environmental change on natural ecosystems is a major challenge, particularly when multiple stressors interact to produce unexpected “ecological surprises” in the form of complex, nonadditive effects that can amplify or reduce their individual effects. Animals often respond behaviorally to environmental change, and multiple stressors can have both population‐level and community‐level effects. However, the individual, not combined, effects of stressors on animal behavior are commonly studied. There is a need to understand how animals respond to the more complex combinations of stressors that occur in nature, which requires a systematic and rigorous approach to quantify the various potential behavioral responses to the independent and interactive effects of stressors. We illustrate a robust, systematic approach for understanding behavioral responses to multiple stressors based on integrating schemes used to quantitatively classify interactions in multiple‐stressor research and to qualitatively view interactions between multiple stimuli in behavioral experiments. We introduce and unify the two frameworks, highlighting their conceptual and methodological similarities, and use four case studies to demonstrate how this unification could improve our interpretation of interactions in behavioral experiments and guide efforts to manage the effects of multiple stressors. Our unified approach: (1) provides behavioral ecologists with a more rigorous and systematic way to quantify how animals respond to interactions between multiple stimuli, an important theoretical advance, (2) helps us better understand how animals behave when they encounter multiple, potentially interacting stressors, and (3) contributes more generally to the understanding of “ecological surprises” in multiple stressors research.     

Patterns of benthic algae and cyanobacteria along twin‐stressor gradients of nutrients and fine sediment: a stream mesocosm experiment

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