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.     

Reconceptualizing synergism and antagonism among multiple stressors

The potential for complex synergistic or antagonistic interactions between multiple stressors presents one of the largest uncertainties when predicting ecological change but, despite common use of the terms in the scientific literature, a consensus on their operational definition is still lacking. The identification of synergism or antagonism is generally straightforward when stressors operate in the same direction, but if individual stressor effects oppose each other, the definition of synergism is paradoxical because what is synergistic to one stressor's effect direction is antagonistic to the others. In their highly cited meta‐analysis, Crain et al. (Ecology Letters, 11, 2008: 1304) assumed in situations with opposing individual effects that synergy only occurs when the cumulative effect is more negative than the additive sum of the opposing individual effects. We argue against this and propose a new systematic classification based on an additive effects model that combines the magnitude and response direction of the cumulative effect and the interaction effect. A new class of “mitigating synergism” is identified, where cumulative effects are reversed and enhanced. We applied our directional classification to the dataset compiled by Crain et al. (Ecology Letters, 11, 2008: 1304) to determine the prevalence of synergistic, antagonistic, and additive interactions. Compared to their original analysis, we report differences in the representation of interaction classes by interaction type and we document examples of mitigating synergism, highlighting the importance of incorporating individual stressor effect directions in the determination of synergisms and antagonisms. This is particularly pertinent given a general bias in ecology toward investigating and reporting adverse multiple stressor effects (double negative). We emphasize the need for reconsideration by the ecological community of the interpretation of synergism and antagonism in situations where individual stressor effects oppose each other or where cumulative effects are reversed and enhanced.     

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.     

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.     

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.     

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.     

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.     

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

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Effects of fishing and acidification‐related benthic mortality on the southeast Australian marine ecosystem

Oceanic uptake of anthropogenic carbon dioxide (CO₂) is altering the carbonate chemistry of seawater, with potentially negative consequences for many calcifying marine organisms. At the same time, increasing fisheries exploitation is impacting on marine ecosystems. Here, using increased benthic‐invertebrate mortality as a proxy for effects of ocean acidification, the potential impact of the two stressors of fishing and acidification on the southeast Australian marine ecosystem to year 2050 was explored. The individual and interaction effects of the two stressors on biomass and diversity were examined for the entire ecosystem and for regional assemblages. For 61 functional groups or species, the cumulative effects of moderate ocean acidification and fishing were additive (30%), synergistic (33%), and antagonistic (37%). Strong ocean acidification resulted in additive (22%), synergistic (40%), and antagonistic (38%) effects. The greatest impact was on the demersal food web, with fishing impacting predation and acidification affecting benthic production. Areas that have been subject to intensive fishing were the most susceptible to acidification effect, although fishing also mitigated some of the decline in biodiversity observed with moderate acidification. The model suggested that ocean acidification and long‐term fisheries exploitation could act synergistically with the increasing sensitivity to change from long‐term (decades) fisheries exploitation potentially causing unexpected restructuring of the pelagic and demersal food webs. Major regime shifts occur around year 2040. Greater focus is needed on how differential fisheries exploitation of marine resources may exacerbate or accelerate effects of environmental changes such as ocean acidification.     

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.     

Stressor intensity determines antagonistic interactions between species invasion and multiple stressor effects on ecosystem functioning

Biological invasions, nutrient enrichment and ocean warming are known to threaten biodiversity and ecosystem functioning. The independent effects of these ecological stressors are well studied, however, we lack understanding of their cumulative effects, which may be additive, antagonistic or synergistic. For example, the impacts of biological invasions are often determined by environmental context, which suggests that the effects of invasive species may vary with other stressors such as pollution or climate change. This study examined the effects of an invasive seaweed (Sargassum muticum) on the structure and functioning of a synthetic macroalgal assemblage and tested explicitly whether these effects varied with nutrient enrichment and ocean warming. Overall, the presence of S. muticum increased assemblage productivity rates and warming altered algal assemblage structure, which was characterised by a decrease in kelp and an increase in ephemeral green algae. The effects of S. muticum on total algal biomass accumulation, however, varied with nutrient enrichment and warming, producing antagonistic cumulative effects on total algal biomass accumulation. These findings show that the nature of stressor interactions may vary with stressor intensity and among response variables, which leads to less predictable consequences for the structure and functioning of communities.     

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.     

Interactive multiple‐stressor effects of the antibiotic monensin,cattle effluent and light on stream periphyton

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Individual and combined effects of fine sediment and the herbicide glyphosate on benthic macroinvertebrates and stream ecosystem function

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Identifying the interacting roles of stressors in driving the global loss of canopy‐forming to mat‐forming algae in marine ecosystems

Identifying the type and strength of interactions between local anthropogenic and other stressors can help to set achievable management targets for degraded marine ecosystems and support their resilience by identifying local actions. We undertook a meta‐analysis, using data from 118 studies to test the hypothesis that ongoing global declines in the dominant habitat along temperate rocky coastlines, forests of canopy‐forming algae and/or their replacement by mat‐forming algae are driven by the nonadditive interactions between local anthropogenic stressors that can be addressed through management actions (fishing, heavy metal pollution, nutrient enrichment and high sediment loads) and other stressors (presence of competitors or grazers, removal of canopy algae, limiting or excessive light, low or high salinity, increasing temperature, high wave exposure and high UV or CO₂), not as easily amenable to management actions. In general, the cumulative effects of local anthropogenic and other stressors had negative effects on the growth and survival of canopy‐forming algae. Conversely, the growth or survival of mat‐forming algae was either unaffected or significantly enhanced by the same pairs of stressors. Contrary to our predictions, the majority of interactions between stressors were additive. There were however synergistic interactions between nutrient enrichment and heavy metals, the presence of competitors, low light and increasing temperature, leading to amplified negative effects on canopy‐forming algae. There were also synergistic interactions between nutrient enrichment and increasing CO₂ and temperature leading to amplified positive effects on mat‐forming algae. Our review of the current literature shows that management of nutrient levels, rather than fishing, heavy metal pollution or high sediment loads, would provide the greatest opportunity for preventing the shift from canopy to mat‐forming algae, particularly in enclosed bays or estuaries because of the higher prevalence of synergistic interactions between nutrient enrichment with other local and global stressors, and as such it should be prioritized.     

Interactions among ecosystem stressors and their importance in conservation

Interactions between multiple ecosystem stressors are expected to jeopardize biological processes, functions and biodiversity. The scientific community has declared stressor interactions—notably synergies—a key issue for conservation and management. Here, we review ecological literature over the past four decades to evaluate trends in the reporting of ecological interactions (synergies, antagonisms and additive effects) and highlight the implications and importance to conservation. Despite increasing popularity, and ever-finer terminologies, we find that synergies are (still) not the most prevalent type of interaction, and that conservation practitioners need to appreciate and manage for all interaction outcomes, including antagonistic and additive effects. However, it will not be possible to identify the effect of every interaction on every organism''s physiology and every ecosystem function because the number of stressors, and their potential interactions, are growing rapidly. Predicting the type of interactions may be possible in the near-future, using meta-analyses, conservation-oriented experiments and adaptive monitoring. Pending a general framework for predicting interactions, conservation management should enact interventions that are robust to uncertainty in interaction type and that continue to bolster biological resilience in a stressful world.     

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.     

Interactive effects of global change factors on soil respiration and its components: a meta‐analysis

As the second largest carbon (C) flux between the atmosphere and terrestrial ecosystems, soil respiration (Rs) plays vital roles in regulating atmospheric CO₂ concentration ([CO₂]) and climatic dynamics in the earth system. Although numerous manipulative studies and a few meta‐analyses have been conducted to determine the responses of Rs and its two components [i.e., autotrophic (Ra) and heterotrophic (Rh) respiration] to single global change factors, the interactive effects of the multiple factors are still unclear. In this study, we performed a meta‐analysis of 150 multiple‐factor (≥2) studies to examine the main and interactive effects of global change factors on Rs and its two components. Our results showed that elevated [CO₂] (E), nitrogen addition (N), irrigation (I), and warming (W) induced significant increases in Rs by 28.6%, 8.8%, 9.7%, and 7.1%, respectively. The combined effects of the multiple factors, EN, EW, DE, IE, IN, IW, IEW, and DEW, were also significantly positive on Rs to a greater extent than those of the single‐factor ones. For all the individual studies, the additive interactions were predominant on Rs (90.6%) and its components (≈70.0%) relative to synergistic and antagonistic ones. However, the different combinations of global change factors (e.g., EN, NW, EW, IW) indicated that the three types of interactions were all important, with two combinations for synergistic effects, two for antagonistic, and five for additive when at least eight independent experiments were considered. In addition, the interactions of elevated [CO₂] and warming had opposite effects on Ra and Rh, suggesting that different processes may influence their responses to the multifactor interactions. Our study highlights the crucial importance of the interactive effects among the multiple factors on Rs and its components, which could inform regional and global models to assess the climate–biosphere feedbacks and improve predictions of the future states of the ecological and climate systems.     

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

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