Stressor richness intensifies productivity loss but mitigates biodiversity loss

Ecosystems are subject to a multitude of anthropogenic environmental changes. Experimental research in the field of multiple stressors has typically involved varying the number of stressors, here termed stressor richness, but without controlling for total stressor intensity. Mistaking stressor intensity effects for stressor richness effects can misinform management decisions when there is a trade‐off between mitigating these two factors. We incorporate multiple stressors into three community models and show that, at a fixed total stressor intensity, increasing stressor richness aggravates joint stressor effects on ecosystem functioning, but reduces effects on species persistence and composition. In addition, stressor richness weakens the positive selection and negative complementarity effects on ecosystem function. We identify the among‐species variation of stressor effects on traits as a key determinant of the resulting community‐level stressor effects. Taken together, our results unravel the mechanisms linking multiple environmental changes to biodiversity and ecosystem function.     

Evidence for multiple stressor interactions and effects on coral reefs

Concern is growing about the potential effects of interacting multiple stressors, especially as the global climate changes. We provide a comprehensive review of multiple stressor interactions in coral reef ecosystems, which are widely considered to be one of the most sensitive ecosystems to global change. First, we synthesized coral reef studies that examined interactions of two or more stressors, highlighting stressor interactions (where one stressor directly influences another) and potentially synergistic effects on response variables (where two stressors interact to produce an effect that is greater than purely additive). For stressor‐stressor interactions, we found 176 studies that examined at least 2 of the 13 stressors of interest. Applying network analysis to analyze relationships between stressors, we found that pathogens were exacerbated by more costressors than any other stressor, with ca. 78% of studies reporting an enhancing effect by another stressor. Sedimentation, storms, and water temperature directly affected the largest number of other stressors. Pathogens, nutrients, and crown‐of‐thorns starfish were the most‐influenced stressors. We found 187 studies that examined the effects of two or more stressors on a third dependent variable. The interaction of irradiance and temperature on corals has been the subject of more research (62 studies, 33% of the total) than any other combination of stressors, with many studies reporting a synergistic effect on coral symbiont photosynthetic performance (n = 19). Second, we performed a quantitative meta‐analysis of existing literature on this most‐studied interaction (irradiance and temperature). We found that the mean effect size of combined treatments was statistically indistinguishable from a purely additive interaction, although it should be noted that the sample size was relatively small (n = 26). Overall, although in aggregate a large body of literature examines stressor effects on coral reefs and coral organisms, considerable gaps remain for numerous stressor interactions and effects, and insufficient quantitative evidence exists to suggest that the prevailing type of stressor interaction is synergistic.     

An improved null model for assessing the net effects of multiple stressors on communities

Ecological stressors (i.e., environmental factors outside their normal range of variation) can mediate each other through their interactions, leading to unexpected combined effects on communities. Determining whether the net effect of stressors is ecologically surprising requires comparing their cumulative impact to a null model that represents the linear combination of their individual effects (i.e., an additive expectation). However, we show that standard additive and multiplicative null models that base their predictions on the effects of single stressors on community properties (e.g., species richness or biomass) do not provide this linear expectation, leading to incorrect interpretations of antagonistic and synergistic responses by communities. We present an alternative, the compositional null model, which instead bases its predictions on the effects of stressors on individual species, and then aggregates them to the community level. Simulations demonstrate the improved ability of the compositional null model to accurately provide a linear expectation of the net effect of stressors. We simulate the response of communities to paired stressors that affect species in a purely additive fashion and compare the relative abilities of the compositional null model and two standard community property null models (additive and multiplicative) to predict these linear changes in species richness and community biomass across different combinations (both positive, negative, or opposite) and intensities of stressors. The compositional model predicts the linear effects of multiple stressors under almost all scenarios, allowing for proper classification of net effects, whereas the standard null models do not. Our findings suggest that current estimates of the prevalence of ecological surprises on communities based on community property null models are unreliable, and should be improved by integrating the responses of individual species to the community level as does our compositional null model.     

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.     

Interactive and cumulative effects of multiple human stressors in marine systems

Humans impact natural systems in a multitude of ways, yet the cumulative effect of multiple stressors on ecological communities remains largely unknown. Here we synthesized 171 studies that manipulated two or more stressors in marine and coastal systems and found that cumulative effects in individual studies were additive (26%), synergistic (36%), and antagonistic (38%). The overall interaction effect across all studies was synergistic, but interaction type varied by response level (community: antagonistic, population: synergistic), trophic level (autotrophs: antagonistic, heterotrophs: synergistic), and specific stressor pair (seven pairs additive, three pairs each synergistic and antagonistic). Addition of a third stressor changed interaction effects significantly in two‐thirds of all cases and doubled the number of synergistic interactions. Given that most studies were performed in laboratories where stressor effects can be carefully isolated, these three‐stressor results suggest that synergies may be quite common in nature where more than two stressors almost always coexist. While significant gaps exist in multiple stressor research, our results suggest an immediate need to account for stressor interactions in ecological studies and conservation planning.     

Using a newly introduced framework to measure ecological stressor interactions

Understanding how stressors combine to affect population abundances and trajectories is a fundamental ecological problem with increasingly important implications worldwide. Generalisations about interactions among stressors are challenging due to different categorisation methods and how stressors vary across species and systems. Here, we propose using a newly introduced framework to analyse data from the last 25 years on ecological stressor interactions, for example combined effects of temperature, salinity and nutrients on population survival and growth. We contrast our results with the most commonly used existing method – analysis of variance (ANOVA) – and show that ANOVA assumptions are often violated and have inherent limitations for detecting interactions. Moreover, we argue that rescaling – examining relative rather than absolute responses – is critical for ensuring that any interaction measure is independent of the strength of single‐stressor effects. In contrast, non‐rescaled measures – like ANOVA – find fewer interactions when single‐stressor effects are weak. After re‐examining 840 two‐stressor combinations, we conclude that antagonism and additivity are the most frequent interaction types, in strong contrast to previous reports that synergy dominates yet supportive of more recent studies that find more antagonism. Consequently, measuring and re‐assessing the frequency of stressor interaction types is imperative for a better understanding of how stressors affect populations.     

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.     

Integrating animal behaviour into research on multiple environmental stressors: a conceptual framework

While a large body of research has focused on the physiological effects of multiple environmental stressors, how behavioural and life-history plasticity mediate multiple-stressor effects remains underexplored. Behavioural plasticity can not only drive organism-level responses to stressors directly but can also mediate physiological responses. Here, we provide a conceptual framework incorporating four fundamental trade-offs that explicitly link animal behaviour to life-history-based pathways for energy allocation, shaping the impact of multiple stressors on fitness. We first address how small-scale behavioural changes can either mediate or drive conflicts between the effects of multiple stressors and alternative physiological responses. We then discuss how animal behaviour gives rise to three additional understudied and interrelated trade-offs: balancing the benefits and risks of obtaining the energy needed to cope with stressors, allocation of energy between life-history traits and stressor responses, and larger-scale escape from stressors in space or time via large-scale movement or dormancy. Finally, we outline how these trade-offs interactively affect fitness and qualitative ecological outcomes resulting from multiple stressors. Our framework suggests that explicitly considering animal behaviour should enrich our mechanistic understanding of stressor effects, help explain extensive context dependence observed in these effects, and highlight promising avenues for future empirical and theoretical research.     

Grazer diversity affects resistance to multiple stressors in an experimental seagrass ecosystem

When multiple stressors act simultaneously, their effects on ecosystems become more difficult to predict. In the face of multiple stressors, diverse ecosystems may be more stable if species respond differently to stressors or if functionally similar species can compensate for stressor effects on focal species. Many habitats around the globe are threatened by multiple stressors, including highly productive seagrass habitats. For example, in Chesapeake Bay, USA, regional climate change predictions suggest that elevated temperature and freshwater inputs are likely to be increasingly important stressors. Using seagrass mesocosms as a model system, we tested whether species richness of crustacean grazers buffers ecosystem properties against the impacts of elevated temperature and freshwater pulse stressors in a fully factorial experiment. Grazer species responded to pulsed salinity changes differently; abundance of Elasmopus levis responded negatively to freshwater pulses, whereas abundance of Gammarus mucronatus and Erichsonella attenuata responded positively or neutrally. Consistent with the hypothesis that biodiversity provides resistance stability, biomass of epiphytic algae that form the base of the food web was less affected by stressors in species‐rich grazer treatments than in single‐species grazer treatments. Stochastic (among‐replicate) variation of sessile invertebrate biomass within treatments was also reduced in more diverse grazer treatments. Therefore, grazer species richness tended to increase the resistance stability of both major components of the seagrass fouling community, algae and invertebrates, in the face of environmental stressors. Finally, in our model system, multi‐stressor impacts suggested a pattern of antagonism contrary to previous assumptions of synergistic stressor effects. Overall, our results confirm that invertebrate grazer species are functionally diverse in their response to environmental stressors, but are largely functionally redundant in their grazing effects leading to greater resistance stability of certain ecosystem properties in diverse grazer assemblages even when influenced by multiple environmental stressors.     

Effects of an invasive consumer on zooplankton communities are unaltered by nutrient inputs

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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 anthropogenic stressors cause ecological surprises in boreal lakes

The number of combinations of anthropogenic stressors affecting global change is increasing; however, few studies have empirically tested for their interactive effects on ecosystems. Most importantly, interactions among ecological stressors generate nonadditive effects that cannot be easily predicted based on single‐stressor studies. Here, we corroborate findings from an in situ mesocosm experiment with evidence from a whole‐ecosystem manipulation to demonstrate for the first time that interactions between climate and acidification determine their cumulative impact on the food‐web structure of coldwater lakes. Interactions among warming, drought, and acidification, rather than the sum of their individual effects, best explained significant changes in planktonic consumer and producer biomass over a 23‐year period. Further, these stressors interactively exerted significant synergistic and antagonistic effects on consumers and producers, respectively. The observed prevalence of long‐ and short‐term ecological surprises involving the cumulative impacts of multiple anthropogenic stressors highlights the high degree of uncertainty surrounding current forecasts of the consequences of global change.     

Quantifying the evidence for ecological synergies

There is increasing concern that multiple drivers of ecological change will interact synergistically to accelerate biodiversity loss. However, the prevalence and magnitude of these interactions remain one of the largest uncertainties in projections of future ecological change. We address this uncertainty by performing a meta-analysis of 112 published factorial experiments that evaluated the impacts of multiple stressors on animal mortality in freshwater, marine and terrestrial communities. We found that, on average, mortalities from the combined action of two stressors were not synergistic and this result was consistent across studies investigating different stressors, study organisms and life-history stages. Furthermore, only one-third of relevant experiments displayed truly synergistic effects, which does not support the prevailing ecological paradigm that synergies are rampant. However, in more than three-quarters of relevant experiments, the outcome of multiple stressor interactions was non-additive (i.e. synergies or antagonisms), suggesting that ecological surprises may be more common than simple additive effects.     

The cumulative impacts of anthropogenic stressors vary markedly along environmental gradients

Understanding the cumulative effects of multiple stressors on biodiversity is key to managing their impacts. Stressor interactions are often studied using an additive/antagonistic/synergistic typology, aimed at identifying situations where individual stressor effects are reduced or amplified when they act in combination. Here, we analysed variation in the family richness of stream macroinvertebrates in the groups Ephemeroptera, Plecoptera and Trichoptera (EPT) at 4658 sites spanning a 32° latitudinal range in eastern Australia in relation to two largely human-induced stressors, salinity and turbidity, and two environmental gradients, temperature and slope. The cumulative and interactive effect of salinity and turbidity on EPT family richness varied across the landscape and by habitat (edge or riffle) such that we observed additive, antagonistic and synergistic outcomes depending on the environmental context. Our findings highlight the importance of understanding the consistency of multiple stressor impacts, which will involve higher-order interactions between multiple stressors and environmental factors.     

Impacts of multiple anthropogenic stressors on stream macroinvertebrate community composition and functional diversity

Ensuring the provision of essential ecosystem services in systems affected by multiple stressors is a key challenge for theoretical and applied ecology. Trait‐based approaches have increasingly been used in multiple‐stressor research in freshwaters because they potentially provide a powerful method to explore the mechanisms underlying changes in populations and communities. Individual benthic macroinvertebrate traits associated with mobility, life history, morphology, and feeding habits are often used to determine how environmental drivers structure stream communities. However, to date multiple‐stressor research on stream invertebrates has focused more on taxonomic than on functional metrics. We conducted a fully crossed, 4‐factor experiment in 64 stream mesocosms fed by a pristine montane stream (21 days of colonization, 21 days of manipulations) and investigated the effects of nutrient enrichment, flow velocity reduction and sedimentation on invertebrate community, taxon, functional diversity and trait variables after 2 and 3 weeks of stressor exposure. 89% of the community structure metrics, 59% of the common taxa, 50% of functional diversity metrics, and 79% of functional traits responded to at least one stressor each. Deposited fine sediment and flow velocity reduction had the strongest impacts, affecting invertebrate abundances and diversity, and their effects translated into a reduction of functional redundancy. Stressor effects often varied between sampling occasions, further complicating the prediction of multiple‐stressor effects on communities. Overall, our study suggests that future research combining community, trait, and functional diversity assessments can improve our understanding of multiple‐stressor effects and their interactions in running waters.     

Impact of multiple stressors on juvenile fish in estuaries of the northeast Pacific

A key step in identifying global change impacts on species and ecosystems is to quantify effects of multiple stressors. To date, the science of global change has been dominated by regional field studies, experimental manipulation, meta‐analyses, conceptual models, reviews, and studies focusing on a single stressor or species over broad spatial and temporal scales. Here, we provide one of the first studies for coastal systems examining multiple stressor effects across broad scales, focused on the nursery function of 20 estuaries spanning 1,600 km of coastline, 25 years of monitoring, and seven fish and invertebrate species along the northeast Pacific coast. We hypothesized those species most estuarine dependent and negatively impacted by human activities would have lower presence and abundances in estuaries with greater anthropogenic land cover, pollution, and water flow stress. We found significant negative relationships between juveniles of two of seven species (Chinook salmon and English sole) and estuarine stressors. Chinook salmon were less likely to occur and were less abundant in estuaries with greater pollution stress. They were also less abundant in estuaries with greater flow stress, although this relationship was marginally insignificant. English sole were less abundant in estuaries with greater land cover stress. Together, we provide new empirical evidence that effects of stressors on two fish species culminate in detectable trends along the northeast Pacific coast, elevating the need for protection from pollution, land cover, and flow stressors to their habitats. Lack of response among the other five species could be related to differing resistance to specific stressors, type and precision of the stressor metrics, and limitations in catch data across estuaries and habitats. Acquiring improved measurements of impacts to species will guide future management actions, and help predict how estuarine nursery functions can be optimized given anthropogenic stressors and climate change scenarios.     

Managing for Interactions between Local and Global Stressors of Ecosystems

Global stressors, including climate change, are a major threat to ecosystems, but they cannot be halted by local actions. Ecosystem management is thus attempting to compensate for the impacts of global stressors by reducing local stressors, such as overfishing. This approach assumes that stressors interact additively or synergistically, whereby the combined effect of two stressors is at least the sum of their isolated effects. It is not clear, however, how management should proceed for antagonistic interactions among stressors, where multiple stressors do not have an additive or greater impact. Research to date has focussed on identifying synergisms among stressors, but antagonisms may be just as common. We examined the effectiveness of management when faced with different types of interactions in two systems – seagrass and fish communities – where the global stressor was climate change but the local stressors were different. When there were synergisms, mitigating local stressors delivered greater gains, whereas when there were antagonisms, management of local stressors was ineffective or even degraded ecosystems. These results suggest that reducing a local stressor can compensate for climate change impacts if there is a synergistic interaction. Conversely, if there is an antagonistic interaction, management of local stressors will have the greatest benefits in areas of refuge from climate change. A balanced research agenda, investigating both antagonistic and synergistic interaction types, is needed to inform management priorities.     

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.     

Net effects of multiple stressors in freshwater ecosystems: a meta‐analysis

The accelerating rate of global change has focused attention on the cumulative impacts of novel and extreme environmental changes (i.e. stressors), especially in marine ecosystems. As integrators of local catchment and regional processes, freshwater ecosystems are also ranked highly sensitive to the net effects of multiple stressors, yet there has not been a large‐scale quantitative synthesis. We analysed data from 88 papers including 286 responses of freshwater ecosystems to paired stressors and discovered that overall, their cumulative mean effect size was less than the sum of their single effects (i.e. an antagonistic interaction). Net effects of dual stressors on diversity and functional performance response metrics were additive and antagonistic, respectively. Across individual studies, a simple vote‐counting method revealed that the net effects of stressor pairs were frequently more antagonistic (41%) than synergistic (28%), additive (16%) or reversed (15%). Here, we define a reversal as occurring when the net impact of two stressors is in the opposite direction (negative or positive) from that of the sum of their single effects. While warming paired with nutrification resulted in additive net effects, the overall mean net effect of warming combined with a second stressor was antagonistic. Most importantly, the mean net effects across all stressor pairs and response metrics were consistently antagonistic or additive, contrasting the greater prevalence of reported synergies in marine systems. Here, a possible explanation for more antagonistic responses by freshwater biota to stressors is that the inherent greater environmental variability of smaller aquatic ecosystems fosters greater potential for acclimation and co‐adaptation to multiple stressors.     

Can biological traits of stream invertebrates help disentangle the effects of multiple stressors in an agricultural catchment?

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