Regional impacts of warming on biodiversity and biomass in high latitude stream ecosystems across the Northern Hemisphere.

Warming can have profound impacts on ecological communities. However, explorations of how differences in biogeography and productivity might reshape the effect of warming have been limited to theoretical or proxy-based approaches: for instance, studies of latitudinal temperature gradients are often conflated with other drivers (e.g., species richness). Here, we overcome these limitations by using local geothermal temperature gradients across multiple high-latitude stream ecosystems. Each suite of streams (6-11 warmed by 1-15°C above ambient) is set within one of five regions (37 streams total); because the heating comes from the bedrock and is not confounded by changes in chemistry, we can isolate the effect of temperature. We found a negative overall relationship between diatom and invertebrate species richness and temperature, but the strength of the relationship varied regionally, declining more strongly in regions with low terrestrial productivity. Total invertebrate biomass increased with temperature in all regions. The latter pattern combined with the former suggests that the increased biomass of tolerant species might compensate for the loss of sensitive species. Our results show that the impact of warming can be dependent on regional conditions, demonstrating that local variation should be included in future climate projections rather than simply assuming universal relationships.

The combined effects of treated sewage discharge and land use on rivers.

Freshwater ecosystems are increasingly threatened by multiple anthropogenic stressors. Release of treated sewage effluent and pollution from agricultural or urban sources can independently reduce water quality with implications for ecological communities. However, our knowledge of the combined effects of these stressors is limited. We performed a field study to quantify the combined effect of treated sewage discharge and land use on nutrient concentrations, sewage fungus presence and communities of macroinvertebrates and benthic algae. Over three seasons in four rivers we found that a model which included an interaction between sewage pollution and time of the year (i.e. months) was the best predictor of nutrient concentrations and the abundance of algae and sewage fungus. Both macroinvertebrate and algae communities shifted downstream of sewage input. Specifically, more tolerant groups, such as cyanobacteria and oligochaetes, were more abundant. The EPT (Ephemeroptera, Plecoptera and Tricoptera) water quality score was best explained by an interaction between month and agriculture in the surrounding landscape. Overall, our results show that sewage discharge has a significant impact on water quality and benthic riverine communities, regardless of the surrounding land uses. Agricultural inputs, however, could be more important than treated sewage discharge in reducing the abundance of sensitive invertebrate taxa. We need both improvements to wastewater treatment processes and reductions in agricultural pollution to reduce threats to vulnerable freshwater communities.

Winter is coming: Interactions of multiple stressors in winter and implications for the natural world.

Winter is a key driver of ecological processes in freshwater, marine and terrestrial ecosystems, particularly in higher latitudes. Species have evolved various adaptive strategies to cope with food limitations and the cold and dark wintertime. However, human-induced climate change and other anthropogenic stressors are impacting organisms in winter in unpredictable ways. In this paper, we show that global change experiments investigating multiple stressors have predominantly been conducted during summer months. However, effects of anthropogenic stressors sometimes differ between winter and other seasons, necessitating comprehensive investigations. Here, we outline a framework for understanding the different effects of anthropogenic stressors in winter compared to other seasons and discuss the primary mechanisms that will alter ecological responses of organisms (microbes, animals and plants). For instance, while the magnitude of some anthropogenic stressors can be greater in winter than in other seasons (e.g. some pollutants), others may alleviate natural winter stress (e.g. warmer temperatures). These changes can have immediate, delayed or carry-over effects on organisms during winter or later seasons. Interactions between stressors may also vary with season. We call for a renewed research direction focusing on multiple stressor effects on winter ecology and evolution to fully understand, and predict, how ecosystems will fare under changing winters. We also argue the importance of incorporating the interactions of anthropogenic stressors with winter into ecological risk assessments, management and conservation efforts.

What does the future look like for kelp when facing multiple stressors?

As primary producers and ecosystem engineers, kelp (generally Order Laminariales) are ecologically important, and their decline could have far-reaching consequences. Kelp are valuable in forming habitats for fish and invertebrates and are crucial for adaptation to climate change by creating coastal defenses and in providing key functions, such as carbon sequestration and food provision. Kelp are threatened by multiple stressors, such as climate change, over-harvesting of predators, and pollution. In this opinion paper, we discuss how these stressors may interact to affect kelp, and how this varies under different contexts. We argue that more research that bridges kelp conservation and multiple stressor theory is needed and outline key questions that should be addressed as a priority. For instance, it is important to understand how previous exposure (either to earlier generations or life stages) determines responses to emerging stressors, and how responses in kelp scale up to alter food webs and ecosystem functioning. By increasing the temporal and biological complexity of kelp research in this way, we will improve our understanding allowing better predictions. This research is essential for the effective conservation and potential restoration of kelp in our rapidly changing world.

Local stressors mask the effects of warming in freshwater ecosystems.

Climate warming is a ubiquitous stressor in freshwater ecosystems, yet its interactive effects with other stressors are poorly understood. We address this knowledge gap by testing the ability of three contrasting null models to predict the joint impacts of warming and a range of other aquatic stressors using a new database of 296 experimental combinations. Despite concerns that stressors will interact to cause synergisms, we found that net impacts were usually best explained by the effect of the stronger stressor alone (the dominance null model), especially if this stressor was a local disturbance associated with human land use. Prediction accuracy depended on stressor identity and how asymmetric stressors were in the magnitude of their effects. These findings suggest we can effectively predict the impacts of multiple stressors by focusing on the stronger stressor, as habitat alteration, nutrients and contamination often override the biological consequences of higher temperatures in freshwater ecosystems.

Are experiment sample sizes adequate to detect biologically important interactions between multiple stressors?

As most ecosystems are being challenged by multiple, co-occurring stressors, an important challenge is to understand and predict how stressors interact to affect biological responses. A popular approach is to design factorial experiments that measure biological responses to pairs of stressors and compare the observed response to a null model expectation. Unfortunately, we believe experiment sample sizes are inadequate to detect most non-null stressor interaction responses, greatly hindering progress. Using both real and simulated data, we show sample sizes typical of many experiments (<6) can (i) only detect very large deviations from the additive null model, implying many important non-null stressor-pair interactions are being missed, and (ii) potentially lead to mostly statistical outliers being reported. Computer code that simulates data under either additive or multiplicative null models is provided to estimate statistical power for user-defined responses and sample sizes, and we recommend this is used to aid experimental design and interpretation of results. We suspect that most experiments may require 20 or more replicates per treatment to have adequate power to detect nonadditive. However, estimates of power need to be made while considering the smallest interaction of interest, i.e., the lower limit for a biologically important interaction, which is likely to be system-specific, meaning a general guide is unavailable. We discuss ways in which the smallest interaction of interest can be chosen, and how sample sizes can be increased. Our main analyses relate to the additive null model, but we show similar problems occur for the multiplicative null model, and we encourage similar investigations into the statistical power of other null models and inference methods. Without knowledge of the detection abilities of the statistical tools at hand or the definition of the smallest meaningful interaction, we will undoubtedly continue to miss important ecosystem stressor interactions.

Interactive effects of multiple stressors vary with consumer interactions, stressor dynamics and magnitude.

Predicting the impacts of multiple stressors is important for informing ecosystem management but is impeded by a lack of a general framework for predicting whether stressors interact synergistically, additively or antagonistically. Here, we use process-based models to study how interactions generalise across three levels of biological organisation (physiological, population and consumer-resource) for a two-stressor experiment on a seagrass model system. We found that the same underlying processes could result in synergistic, additive or antagonistic interactions, with interaction type depending on initial conditions, experiment duration, stressor dynamics and consumer presence. Our results help explain why meta-analyses of multiple stressor experimental results have struggled to identify predictors of consistently non-additive interactions in the natural environment. Experiments run over extended temporal scales, with treatments across gradients of stressor magnitude, are needed to identify the processes that underpin how stressors interact and provide useful predictions to management.

Combined effects of heatwaves and micropollutants on freshwater ecosystems: Towards an integrated assessment of extreme events in multiple stressors research.

Freshwater ecosystems are strongly influenced by weather extremes such as heatwaves (HWs), which are predicted to increase in frequency and magnitude in the future. In addition to these climate extremes, the freshwater realm is impacted by the exposure to various classes of chemicals emitted by anthropogenic activities. Currently, there is limited knowledge on how the combined exposure to HWs and chemicals affects the structure and functioning of freshwater ecosystems. Here, we review the available literature describing the single and combined effects of HWs and chemicals on different levels of biological organization, to obtain a holistic view of their potential interactive effects. We only found a few studies (13 out of the 61 studies included in this review) that investigated the biological effects of HWs in combination with chemical pollution. The reported interactive effects of HWs and chemicals varied largely not only within the different trophic levels but also depending on the studied endpoints for populations or individuals. Hence, owing also to the little number of studies available, no consistent interactive effects could be highlighted at any level of biological organization. Moreover, we found an imbalance towards single species and population experiments, with only five studies using a multitrophic approach. This results in a knowledge gap for relevant community and ecosystem level endpoints, which prevents the exploration of important indirect effects that can compromise food web stability. Moreover, this knowledge gap impairs the validity of chemical risk assessments and our ability to protect ecosystems. Finally, we highlight the urgency of integrating extreme events into multiple stressors studies and provide specific recommendations to guide further experimental research in this regard.

Invasive carp alter trophic niches of consumers and basal resources in African reservoirs.

Environmental pollution and biological invasions are key drivers of biodiversity change. However, the effects of invasion and pollution on food webs remain largely unexplored. Here, we used stable isotopes to examine the effects of common carp Cyprinus carpio and pollution on trophic dynamics in six small reservoirs. Our results revealed that the trophic niche widths of invertebrates, vertebrates, and invasive carp did not significantly differ among reservoirs with different pollution statuses. However, we found low niche conservatism among reservoirs, suggesting that while niche width may remain consistent, there is a shift in the position of the niches in isotopic space under both pollution and invasion scenarios. Niche conservatism among reservoirs was generally higher in invertebrates, but this was also regardless of reservoir condition (i.e. presence or absence of pollution and invasion). These results suggest that invasion by species coupled with organic pollution may cause subtle yet differing effects on components of a food web (basal end-members, invertebrates and vertebrates). Our findings provide a baseline measure of the potential in the development of detection and response strategies for carp invasions and organic pollution.

The Temporal Dynamics of Multiple Stressor Effects: From Individuals to Ecosystems.

Multiple stressors, such as warming and invasions, often occur together and have nonadditive effects. Most studies to date assume that stressors operate in perfect synchrony, but this will rarely be the case in reality. Stressor sequence and overlap will have implications for ecological memory - the ability of past stressors to influence future responses. Moreover, stressors are usually defined in an anthropocentric context: what we consider a short-term stressor, such as a flood, will span multiple generations of microbes. We argue that to predict responses to multiple stressors from individuals to the whole ecosystem, it is necessary to consider metabolic rates, which determine the timescales at which individuals operate and therefore, ultimately, the ecological memory at different levels of ecological organization.

Towards a unified study of multiple stressors: divisions and common goals across research disciplines.

Anthropogenic environmental changes, or 'stressors', increasingly threaten biodiversity and ecosystem functioning worldwide. Multiple-stressor research is a rapidly expanding field of science that seeks to understand and ultimately predict the interactions between stressors. Reviews and meta-analyses of the primary scientific literature have largely been specific to either freshwater, marine or terrestrial ecology, or ecotoxicology. In this cross-disciplinary study, we review the state of knowledge within and among these disciplines to highlight commonality and division in multiple-stressor research. Our review goes beyond a description of previous research by using quantitative bibliometric analysis to identify the division between disciplines and link previously disconnected research communities. Towards a unified research framework, we discuss the shared goal of increased realism through both ecological and temporal complexity, with the overarching aim of improving predictive power. In a rapidly changing world, advancing our understanding of the cumulative ecological impacts of multiple stressors is critical for biodiversity conservation and ecosystem management. Identifying and overcoming the barriers to interdisciplinary knowledge exchange is necessary in rising to this challenge. Division between ecosystem types and disciplines is largely a human creation. Species and stressors cross these borders and so should the scientists who study them.

Estimating δ15N fractionation and adjusting the lipid correction equation using Southern African freshwater fishes.

Stable isotope analysis is an important tool for characterising food web structure; however, interpretation of isotope data can often be flawed. For instance, lipid normalisation and trophic fractionation values are often assumed to be constant, but can vary considerably between ecosystems, species and tissues. Here, previously determined lipid normalisation equations and trophic fractionation values were re-evaluated using freshwater fish species from three rivers in the Upper Zambezian floodplain ecoregion in southern Africa. The parameters commonly used in lipid normalisation equations were not correct for the 18 model species (new D and I parameters were estimated as D = 4.46‰ [95% CI: 2.62, 4.85] and constant I = 0 [95% CI: 0, 0.17]). We suggest that future isotopic analyses on freshwater fishes use our new values if the species under consideration do not have a high lipid content in their white muscle tissue. Nitrogen fractionation values varied between species and river basin; however, the average value closely matched that calculated in previous studies on other species (δ15N fractionation factor of 3.37 ± 1.30 ‰). Here we have highlighted the need to treat stable isotope data correctly in food web studies to avoid misinterpretation of the data.

Trophic overlap between fish and riparian spiders: potential impacts of an invasive fish on terrestrial consumers.

Studies on resource sharing and partitioning generally consider species that occur in the same habitat. However, subsidies between linked habitats, such as streams and riparian zones, create potential for competition between populations which never directly interact. Evidence suggests that the abundance of riparian consumers declines after fish invasion and a subsequent increase in resource sharing of emerging insects. However, diet overlap has not been investigated. Here, we examine the trophic niche of native fish, invasive fish, and native spiders in South Africa using stable isotope analysis. We compared spider abundance and diet at upstream fishless and downstream fish sites and quantified niche overlap with invasive and native fish. Spider abundance was consistently higher at upstream fishless sites compared with paired downstream fish sites, suggesting that the fish reduced aquatic resource availability to riparian consumers. Spiders incorporated more aquatic than terrestrial insects in their diet, with aquatic insects accounting for 45-90% of spider mass. In three of four invaded trout rivers, we found that the average proportion of aquatic resources in web-building spider diet was higher at fishless sites compared to fish sites. The probability of web-building and ground spiders overlapping into the trophic niche of invasive brown and rainbow trout was as high as 26 and 51%, respectively. In contrast, the probability of spiders overlapping into the trophic niche of native fish was always less than 5%. Our results suggest that spiders share resources with invasive fish. In contrast, spiders had a low probability of trophic overlap with native fish indicating that the traits of invaders may be important in determining their influence on ecosystem subsidies. We have added to the growing body of evidence that invaders can have cross-ecosystem impacts and demonstrated that this can be due to niche overlap.

Dietary niche constriction when invaders meet natives: evidence from freshwater decapods.

Invasive species are a key driver of global environmental change, with frequently strong negative consequences for native biodiversity and ecosystem processes. Understanding competitive interactions between invaders and functionally similar native species provides an important benchmark for predicting the consequences of invasion. However, even though having a broad dietary niche is widely considered a key factor determining invasion success, little is known about the effects of competition with functionally similar native competitors on the dietary niche breadths of invasive species. We used a combination of field experiments and field surveys to examine the impacts of competition with a functionally similar native crab species on the population densities, growth rates and diet of the globally widespread invasive red swamp crayfish in an African river ecosystem. The presence of native crabs triggered significant dietary niche constriction within the invasive crayfish population. Further, growth rates of both species were reduced significantly, and by a similar extent, in the presence of one another. In spite of this, crayfish maintained positive growth rates in the presence of crabs, whereas crabs lost mass in the presence of crayfish. Consequently, over the 3-year duration of the study, crab abundance declined at those sites invaded by the crayfish, becoming locally extinct at one. The invasive crayfish had a dramatic effect on ecosystem structure and functioning, halving benthic invertebrate densities and increasing decomposition rates fourfold compared to the crabs. This indicates that replacement of native crabs by invasive crayfish likely alters the structure and functioning of African river ecosystems significantly. This study provides a novel example of the constriction of the dietary niche of a successful invasive population in the presence of competition from a functionally similar native species. This finding highlights the importance of considering both environmental and ecological contexts in order to predict and manage the impacts of invasive species on ecosystems.

Temperature effects on fish production across a natural thermal gradient.

Global warming is widely predicted to reduce the biomass production of top predators, or even result in species loss. Several exceptions to this expectation have been identified, however, and it is vital that we understand the underlying mechanisms if we are to improve our ability to predict future trends. Here, we used a natural warming experiment in Iceland and quantitative theoretical predictions to investigate the success of brown trout as top predators across a stream temperature gradient (4-25 °C). Brown trout are at the northern limit of their geographic distribution in this system, with ambient stream temperatures below their optimum for maximal growth, and above it in the warmest streams. A five-month mark-recapture study revealed that population abundance, biomass, growth rate, and production of trout all increased with stream temperature. We identified two mechanisms that contributed to these responses: (1) trout became more selective in their diet as stream temperature increased, feeding higher in the food web and increasing in trophic position; and (2) trophic transfer through the food web was more efficient in the warmer streams. We found little evidence to support a third potential mechanism: that external subsidies would play a more important role in the diet of trout with increasing stream temperature. Resource availability was also amplified through the trophic levels with warming, as predicted by metabolic theory in nutrient-replete systems. These results highlight circumstances in which top predators can thrive in warmer environments and contribute to our knowledge of warming impacts on natural communities and ecosystem functioning.

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.

Patterns of trophic niche divergence between invasive and native fishes in wild communities are predictable from mesocosm studies.

Ecological theory attempts to predict how impacts for native species arise from biological invasions. A fundamental question centres on the feeding interactions of invasive and native species: whether invasion will result in increased interspecific competition, which would result in negative consequences for the competing species, or trophic niche divergence, which would facilitate the invader's integration into the community and their coexistence with native species. Here, the feeding interactions of a highly invasive fish, topmouth gudgeon Pseudorasbora parva, with three native and functionally similar fishes were studied to determine whether patterns of either niche overlap or divergence detected in mesocosm experiments were apparent between the species at larger spatial scales. Using stable isotope analysis, their feeding relationships were assessed initially in the mesocosms (1000 L) and then in small ponds (<400 m(2) ) and large ponds (>600 m(2) ). In the mesocosms, a consistent pattern of trophic niche divergence was evident between the sympatric fishes, with niches shifting further apart in isotopic space than suggested in allopatry, revealing that sharing of food resources was limited. Sympatric P. parva also had a smaller niche than their allopatric populations. In eight small ponds where P. parva had coexisted for several years with at least one of the fish species used in the mesocosms, strong patterns of niche differentiation were also apparent, with P. parva always at a lower trophic position than the other fishes, as also occurred in the mesocosms. Where these fishes were sympatric within more complex fish communities in the large ponds, similar patterns were also apparent, with strong evidence of trophic niche differentiation. Aspects of the ecological impacts of P. parva invasion for native communities in larger ponds were consistent with those in the mesocosm experiments. Their invasion resulted in divergence in trophic niches, partly due to their reduced niche widths when in sympatry with other species, facilitating their coexistence in invaded ecosystems. Our study highlights the utility of controlled mesocosm studies for predicting the trophic relationships that can develop from introductions of non-native species into more complex ecosystems and at larger spatial scales.

'Leaves and eats shoots': direct terrestrial feeding can supplement invasive red swamp crayfish in times of need.

We used stable isotope analyses to characterise the feeding dynamics of a population of red swamp crayfish in Lake Naivasha, Kenya, after the crash of submerged macrophytes and associated macroinvertebrates, and during a natural draw-down of the lake water level. We expected a heavy reliance upon a diet of detrital matter to sustain the population as a consequence, and indeed, for the majority of the crayfish population caught from the lake, we saw a concomitant shift in isotopic values reflecting a dietary change. However, we also caught individual crayfish that had occupied the footprints of hippopotamus and effectively extended their range beyond the lake up to 40 m into the riparian zone. Isotopic analysis confirmed limited nocturnal observations that these individuals were consuming living terrestrial plants in the vicinity of the footprints. These are the first empirical data to demonstrate direct use of terrestrial resources by an aquatic crayfish species and further highlight the traits that make red swamp crayfish such opportunistic and successful invaders.

Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology.

Biological invasions are a significant driver of human-induced global change and many ecosystems sustain sympatric invaders. Interactions occurring among these invaders have important implications for ecosystem structure and functioning, yet they are poorly understood. Here we apply newly developed metrics derived from stable isotope data to provide quantitative measures of trophic diversity within populations or species. We then use these to test the hypothesis that sympatric invaders belonging to the same functional feeding group occupy a smaller isotopic niche than their allopatric counterparts. Two introduced, globally important, benthic omnivores, Louisiana swamp crayfish (Procambarus clarkii) and carp (Cyprinus carpio), are sympatric in Lake Naivasha, Kenya. We applied our metrics to an 8-year data set encompassing the establishment of carp in the lake. We found a strong asymmetric interaction between the two invasive populations, as indicated by inverse correlations between carp abundance and measures of crayfish trophic diversity. Lack of isotopic niche overlap between carp and crayfish in the majority of years indicated a predominantly indirect interaction. We suggest that carp-induced habitat alteration reduced the diversity of crayfish prey, resulting in a reduction in the dietary niche of crayfish. Stable isotopes provide an integrated signal of diet over space and time, offering an appropriate scale for the study of population niches, but few isotope studies have retained the often insightful information revealed by variability among individuals in isotope values. Our population metrics incorporate such variation, are robust to the vagaries of sample size and are a useful additional tool to reveal subtle dietary interactions among species. Although we have demonstrated their applicability specifically using a detailed temporal dataset of species invasion in a lake, they have a wide array of potential ecological applications.