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Abstract

Multiple stressors are continuously deteriorating surface waters worldwide, posing many challenges for their conservation and restoration. Combined effect types of multiple stressors range from single-stressor dominance to complex interactions. Identifying prevalent combined effect types is critical for environmental management, as it helps to prioritise key stressors for mitigation. However, it remains unclear whether observed single and combined stressor effects reflect true ecological processes unbiased by sample size and length of stressor gradients. Therefore, we examined the role of sample size and stressor gradient lengths in 158 paired-stressor response cases with over 120,000 samples from rivers, lakes, transitional and marine ecosystems around the world. For each case, we split the overall stressor gradient into two partial gradients (lower and upper) and investigated associated changes in single and combined stressor effects. Sample size influenced the identified combined effect types, and stressor interactions were less likely for cases with fewer samples. After splitting gradients, 40 % of cases showed a change in combined effect type, 30 % no change, and 31 % showed a loss in stressor effects. These findings suggest that identified combined effect types may often be statistical artefacts rather than representing ecological processes. In 58 % of cases, we observed changes in stressor effect directions after the gradient split, suggesting unimodal stressor effects. In general, such non-linear responses were more pronounced for organisms at higher trophic levels. We conclude that observed multiple stressor effects are not solely determined by ecological processes, but also strongly depend on sampling design. Observed effects are likely to change when sample size and/or gradient length are modified. Our study highlights the need for improved monitoring programmes with sufficient sample size and stressor gradient coverage. Our findings emphasize the importance of adaptive management, as stress reduction measures or further ecosystem degradation may change multiple stressor-effect relationships, which will then require associated changes in management strategies.

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... Nonlinearity is common in nature with environmental responses to environmental stressors with there being various forms that these relationships can take (Allan, 2004;Huggett, 2005;Mack et al., 2022;Orr et al., 2024). For example, a high-sensitivity nonlinear response involves a clear threshold after which a system rapidly deteriorates while a low-sensitivity nonlinear response occurs more gradually. ...
... Our approach of examining interactions among stressor gradients further increased the realism of the model. The benefits of including interactions between variables and among stressor gradients when recreating real-world ecosystems are a growing research area with studies demonstrating their importance and effects (Mack et al., 2022;Orr et al., 2020;Simmons et al., 2021). The majority of interactive effect research has focused on aquatic ecosystems, but multiple stressorresponse research is also being done in terrestrial environments (Dieleman et al., 2012;Yue et al., 2017). ...
... Accurately modelling multiple, linear and nonlinear stressor-response relationships benefits from the increase in spatial and temporal scale. As scale increases so does the ability to comprehensively characterise individual effects over longer gradients and thus to more accurately capture the nature of the interactions and their effects, thereby improving the prediction of ecosystem responses (Feld et al., 2016;Mack et al., 2022). Field surveys and experiments allow for the inclusion of larger spatial and temporal scales and of environmental contexts and thus tend to be characterised by a higher degree of realism. ...
Article
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Stressor-response models are used to detect and predict changes within ecosystems in response to anthropogenic and naturally occurring stressors. While nonlinear stressor-response relationships and interactions between stressors are common in nature, predictive models often do not account for them due to perceived difficulties in the interpretation of results. We used Irish river monitoring data from 177 river sites to investigate if multiple stressor-response models can be improved by accounting for nonlinearity, interactions in stressor-response relationships and environmental context dependencies. Out of the six models of distinct biological responses, five models benefited from the inclusion of nonlinearity while all six benefited from the inclusion of interactions. The addition of nonlinearity means that we can better see the exponential increase in Trophic Diatom Index (TDI3) as phosphorus increases, inferring ecological conditions deteriorating at a faster rate with increasing phosphorus. Furthermore, our results show that the relationship between stressor and response has the potential to be dependent on other variables, as seen in the interaction of elevation with both siltation and nutrients in relation to Ephemeroptera, Plecoptera and Trichoptera (EPT) richness. Both relationships weakened at higher elevations, perhaps demonstrating that there is a decreased capacity for resilience to stressors at lower elevations due to greater cumulative effects. Understanding interactions such as this is vital to managing ecosystems. Our findings provide empirical support for the need to further develop and employ more complex modelling techniques in environmental assessment and management.
... Here, it is important to guarantee that there is enough stressors' variability in the study area to capture multiple stressors interaction and their associated ecological effects. This means choosing the correct study scale and sample size, as explained by Mack et al. (2022), where an increase in scale can be associated with an increase in the size of datasets or the stressor gradient length (e.g., an increase in the temperature gradient length from 15 to 22 • C to 15-31 • C). The reason for this will be explained in more detail in the next step. ...
... Second, it is important to recognize that observed multiple stressor effects are not only consequences of ecological processes, but also strongly depend on sampling design and strategy (Mack et al., 2022) as datasets not fully capturing stressor gradients or zones of influence may hinder the ability to unveil underlying effects (Segurado et al., 2022). Therefore, Feld et al. (2016), emphasised the need to cover at least 75% of the selected stressors gradient to identify the most important interactions when design a sampling strategy to capture the effects of multiple stressors. ...
... Therefore, Feld et al. (2016), emphasised the need to cover at least 75% of the selected stressors gradient to identify the most important interactions when design a sampling strategy to capture the effects of multiple stressors. In the same sense, Mack et al. (2022), demonstrated that shifts of stressors levels have an influence on multiple stressors effects. Thus, monitoring programmes need to be designed to capture the stressors gradient prevalent in the water body. ...
Article
Multiple stressors resulting from anthropogenic actions are increasingly recognized as a major threat to aquatic ecosystems. In general, ecosystems change as they respond to multiple threats that interact in complex ways, depending on the natural environment. This scenario poses complex tasks for researchers, managers, and policymakers, which require a well-defined framework to provide a clear roadmap that identify steps to apply in adaptive management decisions, monitoring designs and policy implementation. Building upon core elements of previous work, we present a Multiple Stressors Assessment Framework (MSAF) for aquatic ecosystems that provides a roadmap on the achievement of an improved integration between monitoring designs, data acquisition, evaluation processes, and management actions. The MSAF involves seven steps: 1) problem formulation and the definition of the ecosystem type and the spatial-temporal scale, 2) data compilation on the ecosystems' environmental characteristics and the definition of the type, identity and intensity of environmental stressors, 3) data compilation/collection on the biological/ecological receptors (endpoints) to stressors and selection of response variable to monitor (based on structure-based indicators and functional metrics), 4) characterization of the stressor-response relationships and their interactions, 5) construction of specific ecological conceptual models and choice of adequate statistical approaches to test the conceptual models' viability, 6) generation of hypotheses on interactive effects on biological/ecological endpoints, validation of models, hypotheses testing and, if possible, comparison of results with controlled experiments in realistic settings, and 7) recommendations to adaptive monitoring and if necessary, improvement of the study design, and eventual inclusion of other hypotheses and statistical approaches in the context of adaptive management actions. We review progress made in Europe, the USA and Canada in this field using case examples, highlight the approaches taken by the different jurisdictions that align with our framework and identify the linkages between multiple stressors assessments and decision-making for each region. We conclude that a disconnection remains between the investigation of the combined effects of multiple stressors and the implementation of management practices and policy translation. The way forward is through a collaborative effort to create standardized methodologies and appropriate programmes in this field. We hope the proposed framework can be used as a foundation to diagnose multiple stressor interactions and identify responses of ecological indicators to inform effective adaptive management of freshwater ecosystems globally
... These results demonstrate indicator-specific responses of thermal tolerance to changes in salinity. According to previous studies, the pattern of correlation between stressors depends on the gradient of individual stressors (Fischer et al., 2012;Earhart et al., 2022;Mack et al., 2022;Segurado et al., 2022) and target organisms (Corcoll et al., 2015). Freshwater species have been usually studied at increasing salinities while saline species have been often subjected to the opposite conditions. ...
... This method was selected because in most of the available studies, less than four salinity levels were included (Appendix 2). Mack et al. (2022) reported that non-linear responses were more common for organisms at high trophic levels. In other words, the highest value of the critical thermal maximum was observed at intermediate salinity. ...
Article
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Aquatic organisms are challenged by changes in their external environment, such as temperature and salinity fluctuations. If these variables interacted with each other, the response of organisms to temperature changes would be modified by salinity and vice versa. We tested for potential interaction between temperature and salinity effects on freshwater, brackish, and marine organisms, including algae, macrophytes, heterotrophic protists, parasites, invertebrates, and fish. We performed a meta-analysis that compared the thermal tolerance (characterised by the temperature optimum, lower and upper temperature limits, and thermal breadth) at various salinities. The meta-analysis was based on 90 articles (algae: 15; heterotrophic protists: 1; invertebrates: 43; and fish: 31). Studies on macrophytes and parasites were lacking. We found that decreasing salinity significantly increased and decreased the lower and upper temperature limits, respectively, in all groups. Thus, a lowered salinity increased the thermal sensitivity of organisms. These findings mainly reflect the response of brackish and marine organisms to salinity changes, which dominated our database. The few studies on freshwater species showed that their lower thermal limits increased and the upper thermal limits decreased with increasing salinity, albeit statistically nonsignificant. Although non-significant, the response of thermal tolerance to salinity changes differed between various organism groups. It generally decreased in the order of: algae > invertebrates > fish. Overall, our findings indicate adverse effects of salinity changes on the temperature tolerance of aquatic organisms. For freshwater species, studies are comparatively scarce and further studies on their thermal performance at various salinity gradients are required to obtain more robust evidence for interactions between salinity and temperature tolerance. Considering test conditions such as acclimation temperature and potential infection with parasites in future studies may decrease the variability in the relationship between salinity and thermal tolerance.
... Studies ignoring these thermal dependencies may therefore miss important, yet environmentally relevant, effects of microplastics. Ideally, future studies should include a larger gradient of temperatures as stressor interaction patterns may depend on the stressor gradient length (Mack et al., 2022). For the same reason, the interactive effects with warming should be tested along a range of concentrations of microplastics, as the toxicant concentration used may determine the interaction type with warming (Mack et al., 2022). ...
... Ideally, future studies should include a larger gradient of temperatures as stressor interaction patterns may depend on the stressor gradient length (Mack et al., 2022). For the same reason, the interactive effects with warming should be tested along a range of concentrations of microplastics, as the toxicant concentration used may determine the interaction type with warming (Mack et al., 2022). Second, we demonstrated for the first time that, in contrast to the widespread pattern among traditional toxicants such as pesticides and metals, microplastics can increase the heat tolerance. ...
Article
The ecological risk assessment of microplastics under global warming receives increasing attention. Yet, such studies mostly focused on increased mean temperatures (MT), ignoring another key component of global warming, namely daily temperature fluctuations (DTF). Moreover, we know next to nothing about the combined effects of multigenerational exposure to microplastics and warming. In this study, Daphnia magna was exposed to an environmentally relevant concentration of polystyrene microplastics (5 μg L⁻¹) under six thermal conditions (MT: 20 ℃, 24 ℃; DTF: 0 ℃, 5 ℃, 10 ℃) over two generations to investigate the interactive effects of microplastics and global warming. Results showed that microplastics had no effects on Daphnia at standard thermal conditions (constant 20 °C). Yet, microplastics increased the fecundity, heat tolerance, amount of energy storage, net energy budget and cytochrome P450 activity, and decreased the energy consumption when tested under an increased MT or DTF, indicating a hormesis effect induced by microplastics under warming. The unexpected increase in heat tolerance upon exposure to microplastics could be partly explained by the reduced energy consumption and/or increased energy availability. Overall, the present study highlighted the importance of including DTF and multigenerational exposure to improve the ecological risk assessment of microplastics under global warming.
... Limited stressor gradients may also prevent the identification of non-linear responses and potential thresholds beyond which interacting stressors have dramatic ecological effects (Mack et al., 2022). ...
Article
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Drought is an increasing risk to the biodiversity within rivers—ecosystems which are already impacted by human activities. However, the long‐term spatially replicated studies needed to generate understanding of how anthropogenic stressors alter ecological responses to drought are lacking. We studied aquatic invertebrate communities in 2500 samples collected from 179 sites on rivers emerging from England's chalk aquifer over three decades. We tested two sets of alternative hypotheses describing responses to and recovery from drought in interaction with human impacts affecting water quality, fine sediment, water temperature, channel morphology, flow and temporal change in land use. We summarized communities using taxa richness, an index indicating tolerance of anthropogenic degradation (average score per taxon, ASPT) and deviation from the average composition. Responses to drought were altered by interactions with human impacts. Poor water quality exacerbated drought‐driven reductions in taxa richness. Drought‐driven deviations from the average community composition were reduced and enhanced at sites impacted by flow augmentation (e.g. effluent releases) and flow reduction (e.g. abstraction), respectively. Human impacts altered post‐drought recovery. Increases in richness were lower at sites impacted by water abstraction and higher at sites with augmented flows, in particular as recovery trajectories extended beyond 3 years. ASPT recovered faster at sites that gained woodland compared to urban land, due to their greater recovery potential, that is, their lower drought‐driven minimum values and higher post‐drought maximum values. Synthesis and applications. We show that communities in river ecosystems exposed to human impacts—in particular poor water quality, altered flow volumes and land use change—are particularly vulnerable to drought. These results provide evidence that management actions taken to enhance water quality, regulate abstraction and restore riparian land use could promote ecological resilience to drought in groundwater‐dominated rivers such as globally rare chalk streams and other rivers of the Anthropocene, as they adapt to a future characterized by increasing climatic extremity.
... The statistical interactions ultimately detected by a multiple-stressor experiment do not only depend on the intrinsic interactions between stressors and the nonlinearity of biological responses, but also on methodological decisions made throughout the scientific process ( Figure 6c). Firstly, during data collection, researchers should be aware that the choice of biological response variable used to quantify stressor effects, the range of stressor intensities observed or tested, and the measurement of potentially confounding variables can all affect the magnitude and direction of detected statistical interactions (Duncan & Kefford, 2021;Mack et al., 2022;Turschwell et al., 2022). Secondly, during data analysis, researchers must ensure that they use appropriate null models that are mechanistically informed by stressorresponse relationships (Schäfer & Piggott, 2018;Tekin et al., 2020). ...
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Understanding the interactions among anthropogenic stressors is critical for effective conservation and management of ecosystems. Freshwater scientists have invested considerable resources in conducting factorial experiments to disentangle stressor interactions by testing their individual and combined effects. However, the diversity of stressors and systems studied has hindered previous syntheses of this body of research. To overcome this challenge, we used a novel machine learning framework to identify relevant studies from over 235,000 publications. Our synthesis resulted in a new dataset of 2396 multiple‐stressor experiments in freshwater systems. By summarizing the methods used in these studies, quantifying trends in the popularity of the investigated stressors, and performing co‐occurrence analysis, we produce the most comprehensive overview of this diverse field of research to date. We provide both a taxonomy grouping the 909 investigated stressors into 31 classes and an open‐source and interactive version of the dataset (https://jamesaorr.shinyapps.io/freshwater‐multiple‐stressors/). Inspired by our results, we provide a framework to help clarify whether statistical interactions detected by factorial experiments align with stressor interactions of interest, and we outline general guidelines for the design of multiple‐stressor experiments relevant to any system. We conclude by highlighting the research directions required to better understand freshwater ecosystems facing multiple stressors.
... Rigby and Stasinopoulos, 2005). The GLMMs were set up with a zero-one inflated beta regression (BEINF) and a logit link to decrease the dependency of the effect sizes on the gradient length (compare Mack et al., 2022). Prior to model fitting, we assessed collinearity with the variance inflation factor (VIF). ...
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While the general effects of agricultural land use on riverine biota are well documented, the differential effects of specific crop types on different riverine organism groups, remain largely unexplored. Here we used recently published land use data distinguishing between specific crop types and a Germany-wide dataset of 7748 sites on the ecological status of macroinvertebrates, macrophytes and diatoms and applied generalized linear mixed models to unravel the associations between land use types, crop types, and the ecological status. For all organism groups, associations of specific crop types with biota were stronger than those of urban land use. For macroinvertebrates and macrophytes, strong negative associations were found for pesticide intensive permanent crops, while intensively fertilized crops (maize, intensive cereals) affected diatoms most. These differential associations highlight the importance of distinguishing between crop types and organism groups and the urgency to buffer rivers against agricultural stressors at the catchment scales and to expand sustainably managed agriculture.
... Systematic reviews on the combined effects of multiple stressors on aquatic organisms demonstrated diverse patterns in the responses, influenced by various factors such as stressor identity, level of biological organizations, and evolutionary history of animals (Crain et al., 2008;Dinh et al., 2022;Morris et al., 2022). Mack et al. (2022) suggested that the detection of interactive effects is influenced by research design rather than reflecting actual ecological processes. ...
Article
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Sediment contamination and seawater warming are two major stressors to macrobenthos in estuaries. However, little is known about their combined effects on infaunal organisms. Here we investigated the responses of an estuarine polychaete Hediste diversicolor to metal-contaminated sediment and increased temperature. Ragworms were exposed to sediments spiked with 10 and 20 mg kg-1 of copper at 12 and 20 °C for three weeks. No considerable changes were observed in the expression of genes related to copper homeostasis and in the accumulation of oxidative stress damage. Dicarbonyl stress was attenuated by warming exposure. Whole-body energy reserves in the form of carbohydrates, lipids and proteins were little affected, but the energy consumption rate increased with copper exposure and elevated temperature indicating higher basal maintenance costs of ragworms. The combined effects of copper and warming exposures were mostly additive, with copper being a weak stressor and warming a more potent stressor. These results were replicable, as confirmed by two independent experiments of similar settings conducted at two different months of the year. This study suggests the higher sensitivity of energy-related biomarkers and the need to search for more conserved molecular markers of metal exposure in H. diversicolor.
... For example, data analyses demonstrated that the relative importance of chemical mixtures and nonchemical stressors but also of stressor interactions varies spatially and temporally at a given scale (Grizzetti et al., 2017;Kefford et al., 2023;Lemm et al., 2021;. Considering this scale is important when interpreting the results of such studies because the temporal and spatial scale can determine the shape and importance of stressors and their interactions (Fraker et al., 2022;Mack et al., 2022;Pirotta et al., 2022). Moreover, to conduct large-scale analyses often requires simplifying assumptions and data aggregation, and this may result in biased estimates of individual stressor effects and interactions (Jähnig et al., 2020). ...
Article
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Ecosystems are strongly influenced by multiple anthropogenic stressors, including a wide range of chemicals and their mixtures. Studies on the effects of multiple stressors have largely focussed on non-chemical stressors, whereas studies on chemical mixtures have largely ignored other stressors. However, both research areas face similar challenges and require similar tools and methods to predict the joint effects of chemicals or non-chemical stressors, and frameworks to integrate multiple chemical and non-chemical stressors are missing. We provide an overview of the research paradigms, tools and methods commonly used in multiple stressor and chemical mixture research and discuss potential domains of cross-fertilization and joint challenges. First, we compare the general paradigms of ecotoxicology and (applied) ecology to explain the historical divide. Subsequently, we compare methods and approaches for the identification of interactions, stressor characterization and designing experiments. We suggest that both multiple stressor and chemical mixture research are too focused on interactions and would benefit from integration regarding null model selection. Stressor characterization is typically more costly for chemical mixtures. While for chemical mixtures comprehensive classification systems at suborganismal level have been developed, recent classification systems for multiple stressors account for environmental context. Both research areas suffer from rather simplified experimental designs that focus on only a limited number of stressors, chemicals and treatments. We discuss concepts that can guide more realistic designs capturing spatiotemporal stressor dynamics. We suggest that process-based and data-driven models are particularly promising to tackle the challenge of prediction of effects of chemical mixtures and non-chemical stressors on (meta-)communities and (meta-)food webs. We propose a framework to integrate the assessment of effects for multiple stressors and chemical mixtures. This article is protected by copyright. All rights reserved. Environ Toxicol Chem 2023;00:0-0. © 2023 SETAC.
... Long-term analyses of ecosystems under multiple stress are therefore necessary for a better understanding of the potential synergistic interactions of abiotic and biotic (invasion) impacts on river communities (Reid et al., 2019;Ricciardi et al., 2021). In particular, they facilitate covering the long stressor gradients and large sample sizes that are necessary to detect stressor effects correctly (Mack et al., 2022). ...
Article
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Most river ecosystems are exposed to multiple anthropogenic stressors affecting the composition and functionality of benthic communities. Identifying main causes and detecting potentially alarming trends in time depends on the availability of long-term monitoring data sets. Our study aimed to improve the knowledge about community effects of multiple stressors that is needed for effective, sustainable management and conservation. We conducted a causal analysis to detect the dominant stressors and hypothesised that multiple stressors, such as climate change and multiple biological invasions, reduce biodiversity and thus endanger ecosystem stability. Using a data set from 1992 to 2019 for the benthic macroinvertebrate community of a 65-km stretch of the upper Elbe river in Germany, we evaluated the effects of alien species, temperature, discharge, phosphorus, pH and abiotic conditional variables on the taxonomic and functional composition of the benthic community and analysed the temporal behaviour of biodiversity metrics. We observed fundamental taxonomic and functional changes in the community, with a shift from collectors/gatherers to filter feeders and feeding opportunists preferring warm temperatures. A partial dbRDA revealed significant effects of temperature and alien species abundance and richness. The occurrence of distinct phases in the development of community metrics suggests a temporally varying impact of different stressors. Taxonomic and functional richness responded more sensitively than the diversity metrics whereas the functional redundancy metric remained unchanged. Especially the last 10-year phase, however, showed a decline in richness metrics and an unsaturated, linear relationship between taxonomic and functional richness, which rather indicates reduced functional redundancy. We conclude that the varying anthropogenic stressors over three decades, mainly biological invasions and climate change, affected the community severely enough to increase its vulnerability to future stressors. Our study highlights the importance of long-term monitoring data and emphasises a careful use of biodiversity metrics, preferably considering also community composition.
Preprint
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Unprecedented rates of urbanisation cause detrimental impacts on the natural environment. Two of the most prominent and ubiquitous urban stressors are artificial light at night (ALAN) and the urban heat island (UHI) effect. Individually, these two stressors have a wide array of effects on physiological, behavioural, and life-history traits of organisms. However, stressors rarely work in isolation, and the potential interactions of ALAN and elevated temperatures on organismal life-history traits, particularly with respect to sexual signalling and reproduction, are not well understood. Here, in a fully factorial design, we manipulated intensities of ALAN exposure (simulating urban light pollution) and/or developmental rearing temperatures (simulating UHI effects) to explore the consequences for juvenile development, survival, sexual signalling, and mating behaviour of the Pacific field cricket, Teleogryllus oceanicus. Our data revealed significant effects of temperature on key life-history traits. Crickets reared under elevated temperatures had higher mortality; reduced adult longevity, altered sexual signalling and male attractiveness. In isolation, ALAN had very limited impacts, reducing male juvenile development time. Similarly, both stressors acting in concert also had little impact; ALAN reduced female developmental duration when reared at control temperatures, but not elevated temperatures. These data suggest very limited effects of combined stressors in this species, while elevated temperatures, consistent with urban heat island effects, had equivocal effects on life-history traits, reducing survival, but potentially increasing male fitness. Our data highlight the complexity of urban stressors on wildlife behaviour and fitness. Understanding these processes is essential as both ALAN and temperature are predicted to intensify.
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Aquatic organisms are challenged by changes in the external environment, such as temperature and salinity fluctuations. The response of an organism to temperature changes can be modified by salinity, thus pointing at the potential interaction of both variables. In the present study, we tested this assumption for freshwater, brackish, and marine organisms, including algae, macrophytes, heterotrophic protists, parasites, invertebrates, and fish. We reviewed the existing body of literature on potential interactions between temperature and salinity and performed a meta-analysis that compared the thermal tolerance (characterized by the temperature optima, lower and upper temperature limits, and thermal breadths). The final database includes 90 relevant publications (algae: 15; heterotrophic protists: 1; invertebrates: 43; and fish: 31). Relevant publications for microphytes and parasites were not available. Overall, our results show that decreasing salinity significantly increased the lower temperature limits and decreased the upper temperature limits irrespective of the organism groups. These findings mainly reflect the response to salinity changes in brackish and marine systems that dominate our database. Although the number of studies on freshwater species was limited, they showed negative, although statistically nonsignificant, effects of an increased salinity on the thermal tolerance of these species (i.e. increased lower limits and decreased upper limits). In addition, our meta-analysis shows nonsignificant differences in the responsiveness of thermal tolerance to salinity changes among different groups of organisms, but the sensitivity of thermal tolerance to salinity changes generally followed the order: algae > invertebrates > fish. Facing the impact of climate change, our findings point at adverse effects of salinity changes on the temperature tolerance of aquatic organisms. Further studies that investigate the thermal performance of freshwater species at various salinity gradients are required to broaden the evidence for interactions between salinity and temperature tolerance. This also applies to the influence of parasitic infections, which have been found to modulate the temperature tolerance of aquatic invertebrates and fish.
Thesis
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Biodiversity and the health of freshwater ecosystems is strongly impaired by human activities, compromising the stability of these ecosystems and the ecosystem services they provide. Global and European efforts to halt the biodiversity decline and protect ecosystem health were not very successful, especially for rivers, so that for less than ten percent of the German rivers good ecological status was reached in 2021. Present-day agriculture has been identified as the main driver for this deterioration, as evident from a multitude of studies. However, the agricultural effects differ between the organism groups and depending on environmental conditions like soil and climatic conditions. Moreover, and most importantly, agriculture is not uniform. The specific agricultural types and practices differ between regions, which in turn leads to differences in the intensity of agrochemical usage as suggested by many small-scale studies. Consequently, the magnitude of agricultural effects on biodiversity and health of river ecosystems most probably depends on agricultural types and practices and differs between regions. For the effective mitigation of these negative effects, several knowledge gaps need to be closed, which were addressed in six chapters, shortly described in the following. First, the current knowledge on the effect of agriculture on river biota was summarized and analysed in a meta-analysis (Schürings et al., 2022). According to this meta-analysis described in the first chapter, agriculture has an overall medium to high negative effect on river biota, and results indicate that the effects of agriculture differ between agricultural types, practices, the organism groups, and biological metrics considered. Second, a pan-European dataset was used to establish an agricultural typology, based on agricultural production and agriculture-related freshwater pressure by nutrients, pesticides, water abstraction and hydromorphological alterations (Schürings et al., 2023). This chapter identified how agricultural types differ in their pressures exerted on freshwaters and shows that accounting for agricultural pressure intensity nearly doubles the correlation with the ecological status. Third, the effects of different agricultural types on the ecological status according to the EU Water Framework Directive (WFD) were investigated, using high resolution German-wide land use data, distinguishing between different crop types (Schürings et al., 2024a). The effects on the ecological status clearly differed between crop types, which typically are associated with different agrochemical application rates. Macroinvertebrates and macrophytes were most strongly affected by pesticide application intensive crops and diatoms were most affected by nutrient intensive crops. Fourth, the results presented in Markert et al. (2023) provided evidence that urban areas and different 5 agricultural crop types with typical agrochemical application rates are indeed related to the micropollutant concentrations monitored in rivers, which often exceeded Environmental Quality Standards. Fifth, crop type-specific differences in agrochemical application rates reported in literature were used to generate an agricultural intensity index (Schürings et al., 2024b). This index improved the correlative strength between present-day agriculture and the ecological status with most pronounced relations for macroinvertebrates in small mountain streams. Sixth, experiences from implementing environmental legislations like the WFD were used to advice for a successful implementation of the EU Nature Restoration Law (Hering et al., 2023). This final chapter highlights that joining restoration efforts with a shift to more sustainable agriculture, whose importance is reasoned in the previous chapters, would offer unprecedented opportunities for successful protection of ecosystem health. In conclusion, this thesis provides overwhelming evidence for the negative effects of present- day agriculture on river biota, portraying influencing factors and highlighting strong relationships between agricultural effects on river biota and agrochemical application, particularly of pesticides. Therefore, to mitigate these effects, a transition of present-day agriculture to more sustainable practices, such as organic farming or agroecology is of vital importance. Such a transition would be beneficial both for the future viability of agriculture itself but also for the protection and restoration of healthy ecosystems, including the successful implementation of the European environmental legislation such as the Nature Restoration Law.
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Agriculture has been identified as a main cause for more than 90% of Germany´s rivers still not meeting good ecological status in 2021. While many large-scale studies observed a negative effect of catchment agricultural land use on river biota, they rarely considered differences in cultivation intensities, although small-scale studies highlight clear differences between the effects of agricultural crops. Here we used Germany-wide and spatially explicit information on crop types to calculate agricultural intensity indices for nutrients and pesticides, weighting different crop types based on average pesticide treatment and nutrient application rates. These indices were then used as explanatory variables for the ecological status of n = 7677 biological sampling sites. Pesticides were more important than nutrient pollution for macroinvertebrates and macrophytes, while diatoms were more sensitive to nutrients. Considering the most relevant intensity index (pesticide or nutrient) slightly increased the correlative strength with ecological status, as compared to the correlation with agricultural land or cropland cover by up to R² = 0.14 for diatoms. Correlative strength of agricultural intensity indices was substantially larger in small mountain and (pre)-alpine streams compared to lowland streams, with an R² up to 0.43 for macroinvertebrates. These results not only confirm previous large-scale studies by demonstrating the detrimental effects of present-day agriculture on river biota, but also shed light on the main pathways involved, particularly highlighting the adverse impacts of agrochemicals. Consequently, to protect river biota, a shift to more sustainable agricultural practices, like reducing pesticide application, is urgently required.
Article
Ecotoxicological studies considerably improved realism by assessing the toxicity of pollutants at different temperatures. Nevertheless, they may miss key interaction patterns between pollutants and temperature by typically considering only part of the natural thermal gradient experienced by species and ignoring daily temperature fluctuations (DTF). We therefore tested in a common garden laboratory experiment the effects of the pesticide chlorpyrifos across a range of mean temperatures and DTF on physiological traits (related to oxidative stress and bioenergetics) in low- and high-latitude populations of Ischnura elegans damselfly larvae. As expected, the impact of chlorpyrifos varied along the wide range of mean temperatures (12-34 °C). None of the physiological traits (except the superoxide anion levels) were affected by chlorpyrifos at the intermediate mean temperatures (20-24 °C). Instead, most of them were negatively affected by chlorpyrifos (reduced activity levels of the antioxidant defense enzymes superoxide dismutase [SOD], catalase [CAT] and peroxidase [PER], and a reduced energy budget) at the very high (≥28 °C) or extreme high temperatures (≥32 °C), and to lesser extent at the lower mean temperatures (≤16 °C). Notably, at the lower mean temperatures the negative impact of chlorpyrifos was often only present or stronger under DTF. Although the chlorpyrifos effects on the physiological traits greatly depended on the experimentally imposed thermal gradient, patterns were mainly consistent across the natural latitude-associated thermal gradient, indicating the generality of our results. The thermal patterns in chlorpyrifos-induced physiological responses contributed to the observed toxicity patterns in life history (reduced survival and growth at low and high mean temperatures). Taken together, our results underscore the importance of evaluating pesticide toxicity along a temperature gradient and of taking a mechanistic approach with a focus on physiology, to improve our understanding of the combined effects of pollutants and temperature in natural populations.
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The feasibility assessment (FA) presents a systematic framework to assess adaptation and mitigation options organised by system transitions. This Cross-Chapter Box assessed the feasibility of 23 adaptation options across six dimensions: economic, technological, institutional, socio-cultural, environmental-ecological, and geophysical to identify factors within each dimension that present barriers to the achievement of the option. The results are presented below.
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This study aims at understanding how observed inconsistencies in the response of biotic indicators to multiple stressors may result from different stressor gradient lengths being represented at different areas or temporal windows, either as the result of intrinsic natural causes or as the result of sampling bias. We simulated a pool of sites showing five types of interactive responses of indicators to two co-occurring virtual stressors, as well as several sampling constraints, resulting in different portions of each stressor's gradient being covered. The sampled gradient length showed a strong influence on the detection of single stressor effects, both in terms of statistical significance and goodness-of-fit. Increasing constraints on gradient coverage also led to an increasingly deficient identification of stressor interactions. The fail in detecting significant interactions largely dominated over switches between interaction types. The simulations indicated that datasets not fully capturing stressor gradients may hinder the ability to unveil underlying multiple stressor effects. As distinct portions of stressor gradients may be present at different contexts and may change over time, our simulations stress the importance of adaptive management strategies based on robust sampling designs to minimize potential statistical artefacts and uncertainties.
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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.
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Climate and land-use change drive a suite of stressors that shape ecosystems and interact to yield complex ecological responses, i.e. additive, antagonistic and synergistic effects. Currently we know little about the spatial scale relevant for the outcome of such interactions and about effect sizes. This knowledge gap needs to be filled to underpin future land management decisions or climate mitigation interventions, for protecting and restoring freshwater ecosystems. The study combines data across scales from 33 mesocosm experiments with those from 14 river basins and 22 cross-basin studies in Europe producing 174 combinations of paired-stressor effects on a biological response variable. Generalised linear models showed that only one of the two stressors had a significant effect in 39% of the analysed cases, 28% of the paired-stressor combinations resulted in additive and 33% in interactive (antagonistic, synergistic, opposing or reversal) effects. For lakes the frequency of additive and interactive effects was similar for all spatial scales addressed, while for rivers this frequency increased with scale. Nutrient enrichment was the overriding stressor for lakes, generally exceeding those of secondary stressors. For rivers, the effects of nutrient enrichment were dependent on the specific stressor combination and biological response variable. These results vindicate the traditional focus of lake restoration and management on nutrient stress, while highlighting that river management requires more bespoke management solutions.
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In this paper, we discuss an extension to two popular approaches to modeling complex structures in ecological data: the generalized additive model (GAM) and the hierarchical model (HGLM). The hierarchical GAM (HGAM), allows modeling of nonlinear functional relationships between covariates and outcomes where the shape of the function itself varies between different grouping levels. We describe the theoretical connection between HGAMs, HGLMs, and GAMs, explain how to model different assumptions about the degree of intergroup variability in functional response, and show how HGAMs can be readily fitted using existing GAM software, the mgcv package in R. We also discuss computational and statistical issues with fitting these models, and demonstrate how to fit HGAMs on example data. All code and data used to generate this paper are available at: github.com/eric-pedersen/mixed-effect-gams.
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Multiple stressors are increasingly affecting organisms and communities, thereby modifying ecosystems' state and functioning. Raising awareness about the threat from multiple stressors has increased the number of experimental and observational studies specifically addressing consequences of stressor interactions on biota. Most studies measure the direct effects of multiple stressors and their interactions on biological endpoints such as abundance, biomass, or diversity of target organisms. This yields invaluable information for the management and restoration of stressed ecosystems. However, as we argue in our perspective paper, this common approach ignores a fundamental characteristic of communities and ecosystems, i.e., that organisms in ecosystems are interlinked by biotic interactions in ecological networks. Examples from the literature show that biotic interactions can modify stressor effects, transfer stressor effects to distant groups of organisms, and create new stressor interactions. These examples also suggest that changes in biotic interactions can have effects of similar or greater magnitude than direct stressor effects. We provide a perspective on how to include network characteristics and biotic interactions into analyses of multiple-stressor effects on ecosystems. Our approach can also make use of biomonitoring data produced with established and intercalibrated methods, and can combine it with novel metrics used to describe the functioning of ecosystems, such as trait information or stable-isotope measurements. The insights on network-mediated effects gained via the approach we propose can substantially increase mechanistic understanding of multiple-stressor effects, and in turn, the efficiency of ecosystem management and restoration.
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Eutrophication and climate change are two of the most pressing environmental issues affecting up to 50% of aquatic ecosystems worldwide. Mitigation strategies to reduce the impact of environmental change are complicated by inherent difficulties of predicting the long-term impact of multiple stressors on natural populations. Here, we investigated the impact of temperature, food levels and carbamate insecticides, in isolation and in combination, on current and historical populations of the freshwater grazer Daphnia. We used common garden and competition experiments on historical and modern populations of D. magna ‘resurrected’ from a lake with known history of anthropogenic eutrophication and documented increase in ambient temperature over time. We found that these populations response dramatically differed between single and multiple stressors. Whereas warming alone induced similar responses among populations, warming combined with insecticides or food limitation resulted in significantly lower fitness in the population historically exposed to pesticides. These results suggest that the negative effect of historical pesticide exposure is magnified in the presence of warming, supporting the hypothesis of synergism between chemical pollution and other stressors.
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Cumulative ecological impacts of chronic, extreme, and often novel, anthropogenic environmental changes (i.e., stressors) often differ from the sum of their individual effects. Uncertainty over the causes of such non‐additivity among multiple stressors confounds forecasts of their net ecological impact. Although stressors can interact directly within the environment to mediate their combined effects on communities, species interactions likely also play key roles. Here, we use a simulation model to explore how species interactions cause community responses (changes in species richness and total biomass) to paired stressors to differ from what we would expect based on the individual effects of each stressor (the additive effect). We demonstrate how interspecific interactions cause communities to respond non‐additively to stressors, and how this depends on whether these interactions are negative or positive and whether the stressors have positive or negative impacts on the community property of interest. When pairwise species interactions involve at least one negative interaction (i.e., competition or predation), stressors combine to have greater than expected negative impacts (e.g., species or biomass loss) and less than expected positive impacts (e.g., biomass increases). In contrast, reciprocally positive interactions between species (i.e., facilitation) generally cause stressors to have additive, or slightly less than additive, net effects on species richness and community biomass. While species interactions determine the nature of the combined impact of multiple stressors (i.e., greater than or less than expected), species co‐tolerance and stressor timing (i.e., sequential vs simultaneous application) only modify the magnitude of this effect. These findings highlight how interactions among species can contribute to non‐additive responses by communities to environmental change, in addition to those caused by interactions among stressors themselves.
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A fundamental challenge in experimental ecology is to capture nonlinearities of ecological responses to interacting environmental drivers. Here, we demonstrate that gradient designs outperform replicated designs for detecting and quantifying nonlinear responses. We report the results of (1) multiple computer simulations and (2) two purpose‐designed empirical experiments. The findings consistently revealed that unreplicated sampling at a maximum number of sampling locations maximised prediction success (i.e. the R² to the known truth) irrespective of the amount of stochasticity and the underlying response surfaces, including combinations of two linear, unimodal or saturating drivers. For the two empirical experiments, the same pattern was found, with gradient designs outperforming replicated designs in revealing the response surfaces of underlying drivers. Our findings suggest that a move to gradient designs in ecological experiments could be a major step towards unravelling underlying response patterns to continuous and interacting environmental drivers in a feasible and statistically powerful way.
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Synergistic interactions between temperature and contaminants are a major challenge for ecological risk assessment, especially under global warming. While thermal evolution may increase the ability to deal with warming, it is unknown whether it may also affect the ability to deal with the many contaminants that are more toxic at higher temperatures. We investigated how evolution of genetic adaptation to warming affected the interactions between warming and a novel stressor: zinc oxide nanoparticles (nZnO) in a natural population of Daphnia magna using resurrection ecology. We hatched resting eggs from two D. magna subpopulations (old: 1955‐1965, recent: 1995‐2005) from the sediment of a lake that experienced an increase in average temperature and in recurrence of heat waves but was never exposed to industrial waste. In the old ‘ancestral’ subpopulation, exposure to a sublethal concentration of nZnO decreased the intrinsic growth rate, metabolic activity and energy reserves at 24°C but not at 20°C, indicating a synergism between warming and nZnO. In contrast, these synergistic effects disappeared in the recent ‘derived’ subpopulation that evolved a lower sensitivity to nZnO at 24°C, which indicates that thermal evolution could offset the elevated toxicity of nZnO under warming. This evolution of reduced sensitivity to nZnO under warming could not be explained by changes in the total internal zinc accumulation but was partially associated with the evolution of the expression of a key metal detoxification gene under warming. Our results suggest that the increased sensitivity to the sublethal concentration of nZnO under the predicted 4°C warming by the end of this century may be counteracted by thermal evolution in this D. magna population. Our results illustrate the importance of evolution to warming in shaping the responses to another anthropogenic stressor, here a contaminant. More general, genetic adaptation to an environmental stressor may ensure that synergistic effects between contaminants and this environmental stressor will not be present anymore. This article is protected by copyright. All rights reserved.
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Sedimentation, nutrients and metal loading to coastal environments are increasing, associated with urbanization and global warming, hence there is a growing need to predict ecological responses to such change. Using a regression technique we predicted how maximum abundance of 20 macrobenthic taxa and 22 functional traits separately and interactively responded to these key stressors. The abundance of most taxa declined in response to sedimentation and metal loading while a unimodal response was often associated with nutrient loading. Optimum abundances for both taxa and traits occurred at relatively low stressor levels, highlighting the vulnerability of estuaries to increasing stressor loads. Individual taxa were more susceptible to stress than traits, suggesting that functional traits may be less sensitive for detecting changes in ecosystem health. Multiplicative effects were more common than additive interactions. The observed sensitivity of most taxa to increasing sedimentation and metal loading and the documented interaction effects between multiple stressors have important implications for understanding and managing the ecological consequences of eutrophication, sedimentation and contaminants on coastal ecosystems.
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Connecting the nonlinear and often counterintuitive physiological effects of multiple environmental drivers to the emergent impacts on ecosystems is a fundamental challenge. Unfortunately, the disconnect between the way "stressors" (e.g., warming) is considered in organismal (physiological) and ecological (community) contexts continues to hamper progress. Environmental drivers typically elicit biphasic physiological responses, where performance declines at levels above and below some optimum. It is also well understood that species exhibit highly variable response surfaces to these changes so that the optimum level of any environmental driver can vary among interacting species. Thus, species interactions are unlikely to go unaltered under environmental change. However, while these nonlinear, species-specific physiological relationships between environment and performance appear to be general, rarely are they incorporated into predictions of ecological tipping points. Instead, most ecosystem-level studies focus on varying levels of "stress" and frequently assume that any deviation from "normal" environmental conditions has similar effects, albeit with different magnitudes, on all of the species within a community. We consider a framework that realigns the positive and negative physiological effects of changes in climatic and nonclimatic drivers with indirect ecological responses. Using a series of simple models based on direct physiological responses to temperature and ocean pCO2, we explore how variation in environment-performance relationships among primary producers and consumers translates into community-level effects via trophic interactions. These models show that even in the absence of direct mortality, mismatched responses resulting from often subtle changes in the physical environment can lead to substantial ecosystem-level change.
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Changes in the Earth's environment are now sufficiently complex that our ability to forecast the emergent ecological consequences of ocean acidification (OA) is limited. Such projections are challenging because the effects of OA may be enhanced, reduced or even reversed by other environmental stressors or interactions among species. Despite an increasing emphasis on multifactor and multispecies studies in global change biology, our ability to forecast outcomes at higher levels of organization remains low. Much of our failure lies in a poor mechanistic understanding of nonlinear responses, a lack of specificity regarding the levels of organization at which interactions can arise, and an incomplete appreciation for linkages across these levels. To move forward, we need to fully embrace interactions. Mechanistic studies on physiological processes and individual performance in response to OA must be complemented by work on population and community dynamics. We must also increase our understanding of how linkages and feedback among multiple environmental stressors and levels of organization can generate nonlinear responses to OA. This will not be a simple undertaking, but advances are of the utmost importance as we attempt to mitigate the effects of ongoing global change.
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Humans have increased the discharge of pollution, altered water flow regime and modified the morphology of rivers. All these actions have resulted in multiple pressures on freshwater ecosystems, undermining their biodiversity and ecological functioning. The European Union has adopted an ambitious water policy to reduce pressures and achieve a good ecological status for all water bodies. However, assessing multiple pressures on aquatic ecosystems and understanding their combined impact on the ecological status is challenging, especially at the large scale, though crucial to the planning of effective policies. Here, for the first time, we quantify multiple human pressures and their relationship with the ecological status for all European rivers. We considered ecological data collected across Europe and pressures assessed by pan-European models, including pollution, hydrological and hydromorphological alterations. We estimated that in one third of EU’s territory rivers are in good ecological status. We found that better ecological status is associated with the presence of natural areas in floodplains, while urbanisation and nutrient pollution are important predictors of ecological degradation. We explored scenarios of improvement of rivers ecological status for Europe. Our results strengthen the need to halt urban land take, curb nitrogen pollution and maintain and restore nature along rivers.
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Meta‐analysis and meta‐regression are statistical methods for synthesizing and modelling the results of different studies, and are critical research synthesis tools in ecology and evolutionary biology (E&E). However, many E&E researchers carry out meta‐analyses using software that is limited in its statistical functionality and is not easily updatable. It is likely that these software limitations have slowed the uptake of new methods in E&E and limited the scope and quality of inferences from research syntheses. We developed OpenMEE: Open Meta‐analyst for Ecology and Evolution to address the need for advanced, easy‐to‐use software for meta‐analysis and meta‐regression. OpenMEE has a cross‐platform, easy‐to‐use graphical user interface (GUI) that gives E&E researchers access to the diverse and advanced statistical functionalities offered in R , without requiring knowledge of R programming. OpenMEE offers a suite of advanced meta‐analysis and meta‐regression methods for synthesizing continuous and categorical data, including meta‐regression with multiple covariates and their interactions, phylogenetic analyses, and simple missing data imputation. OpenMEE also supports data importing and exporting, exploratory data analysis, graphing of data, and summary table generation. As intuitive, open‐source, free software for advanced methods in meta‐analysis, OpenMEE meets the current and pressing needs of the E&E community for teaching meta‐analysis and conducting high‐quality syntheses. Because OpenMEE 's statistical components are written in R , new methods and packages can be rapidly incorporated into the software. To fully realize the potential of OpenMEE , we encourage community development with an aim to advance the capabilities of meta‐analyses in E&E.
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Abstract This work addresses human stressors and their impacts on fish assemblages at pan-European scale by analysing single and multiple stressors and their interactions. Based on an extensive dataset with 3105 fish sampling sites, patterns of stressors, their combination and nature of interactions, i.e. synergistic, antagonistic and additive were investigated. Geographical distribution and patterns of seven human stressor variables, belonging to four stressor groups (hydrological-, morphological-, water quality- and connectivity stressors), were examined, considering both single and multiple stressor combinations. To quantify the stressors' ecological impact, a set of 22 fish metrics for various fish assemblage types (headwaters, medium gradient rivers, lowland rivers and Mediterranean streams) was analysed by comparing their observed and expected response to different stressors, both acting individually and in combination. Overall, investigated fish sampling sites are affected by 15 different stressor combinations, including 4 stressors acting individually and 11 combinations of two or more stressors; up to 4 stressor groups per fish sampling site occur. Stressor-response analysis shows divergent results among different stressor categories, even though a general trend of decreasing ecological integrity with increasing stressor quantity can be observed. Fish metrics based on density of species ‘intolerant to water quality degradation’ and ‘intolerant to oxygen depletion” responded best to single and multiple stressors and their interactions. Interactions of stressors were additive (40%), synergistic (30%) or antagonistic (30%), emphasizing the importance to consider interactions in multi-stressor analyses. While antagonistic effects are only observed in headwaters and medium-gradient rivers, synergistic effects increase from headwaters over medium gradient rivers and Mediterranean streams to large lowland rivers. The knowledge gained in this work provides a basis for advanced investigations in European river basins and helps prioritizing further restoration and management actions.
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Misinterpretation and abuse of statistical tests, confidence intervals, and statistical power have been decried for decades, yet remain rampant. A key problem is that there are no interpretations of these concepts that are at once simple, intuitive, correct, and foolproof. Instead, correct use and interpretation of these statistics requires an attention to detail which seems to tax the patience of working scientists. This high cognitive demand has led to an epidemic of shortcut definitions and interpretations that are simply wrong, sometimes disastrously so-and yet these misinterpretations dominate much of the scientific literature. In light of this problem, we provide definitions and a discussion of basic statistics that are more general and critical than typically found in traditional introductory expositions. Our goal is to provide a resource for instructors, researchers, and consumers of statistics whose knowledge of statistical theory and technique may be limited but who wish to avoid and spot misinterpretations. We emphasize how violation of often unstated analysis protocols (such as selecting analyses for presentation based on the P values they produce) can lead to small P values even if the declared test hypothesis is correct, and can lead to large P values even if that hypothesis is incorrect. We then provide an explanatory list of 25 misinterpretations of P values, confidence intervals, and power. We conclude with guidelines for improving statistical interpretation and reporting.
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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. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
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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.
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We live amid a global wave of anthropogenically driven biodiversity loss: species and population extirpations and, critically, declines in local species abundance. Particularly, human impacts on animal biodiversity are an under-recognized form of global environmental change. Among terrestrial vertebrates, 322 species have become extinct since 1500, and populations of the remaining species show 25% average decline in abundance. Invertebrate patterns are equally dire: 67% of monitored populations show 45% mean abundance decline. Such animal declines will cascade onto ecosystem functioning and human well-being. Much remains unknown about this “Anthropocene defaunation”; these knowledge gaps hinder our capacity to predict and limit defaunation impacts. Clearly, however, defaunation is both a pervasive component of the planet’s sixth mass extinction and also a major driver of global ecological change.
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This study was designed to test for synergism (increased stress) or antagonism (decreased stress) among multiple environmental stressors using additive, multiplicative, and simple comparative effects models. Model predictions were compared to empirical results of laboratory experiments measuring interactions among thermal stress, toxin exposure, and low food on reproduction and survival of two species of cladoceran zooplankton. Stress was defined operationally as a reduction in reproduction or survival relative to optimal conditions over a 7-d period. These experiments are particularly applicable to episodic stresses such as those associated with short-term heat waves. Toxin or low food in combination with 30°C temperatures were generally more harmful than high temperature alone. However, most multiple stress effects were antagonistic, in that effects in combination were not as severe as predicted based on the sum or the product of their individual effects. In rare cases, interaction among stressors even diminished effects of the worst single stressor. Optimal conditions for reproduction and survival occurred at 25°C, high food and 0 mg liter-1 toxin (a surfactant, sodium dodecyl sulfate). Suppressive effects of stressors examined individually ranked: high temperature (30°C) > SDS (10 mg liter-1 ≥ low food (~100 μg C liter-1) > low temperature (20°C). Daphnia pulex isolated from a pond which experiences high summer temperatures throughout was more tolerant of 30°C conditions than Daphnia pulicaria isolated from a lake with a cold-water refuge. Differences were observed in individuals exposed as either adults or as 24-h neonates.
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1. The fundamental importance of freshwater resources, the rapid extinction rate among freshwater species and the pronounced sensitivity of freshwater ecosystems to climate change together signal a pre-eminent need for renewed scientific focus and greater resources. Against this background, the Freshwater Biological Association in 2008 launched a new series of ‘summit’ Conferences in Aquatic Biology intended to develop and showcase the application of ecological science to major issues in freshwater management. 2. This collection of studies arose from the first summit entitled ‘Multiple Stressors in Freshwater Ecosystems’. Although freshwater science and management are replete with mutiple-stressor problems, few studies have been designed explicitly to untangle their effects. 3. The individual case studies that follow reveal the wide array of freshwaters affected by multiple stressors, the spatial and temporal scales involved, the species and ecosystem processes affected, the complex interactions between ecology and socioeconomics that engender such effects, the approaches advocated to address the problems and the challenges of restoring affected systems. The studies also illustrate the extent to which new challenges are emerging (e.g. through climate change), but also they develop a vision of how freshwaters might be managed sustainably to offset multiple stressors in future. 4. More generically, these case studies illustrate (i) how freshwaters might be at particular risk of multiple-stressor effects because of conflicts in water use, and because the hydrological cycle vectors stressor effects so effectively and so extensively; (ii) that dramatic, nonlinear, ‘ecological surprises’ sometimes emerge as multiple-stressor effects develop and (iii) that good ecology and good ecologists add considerable value to other freshwater disciplines in understanding multiple stressors and managing their effects.
Article
Interactions between stressors in freshwater ecosystems, including those associated with climate change and nutrient enrichment, are currently difficult to detect and manage. Our understanding of the forms and frequency of occurrence of such interactions is limited; assessments using field data have been constrained as a result of varying data forms and quality. To address this issue, we demonstrate a statistical approach capable of assessing multiple stressor interactions using contrasting data forms in 3 European catchments (Loch Leven Catchment, UK: assessment of phytoplankton response in a single lake with time series data; Pinios Catchment, Greece: macroinvertebrate response across multiple rivers using spatial data; and Lepsämänjoki Catchment, Finland: phytoplankton response across multiple rivers using spatiotemporal data). Statistical models were developed to predict the relative and interactive effects of climate change and nutrient enrichment sensitive indicators (stressors) on indicators of ecological quality (ecological responses) within the framework of linear mixed effects models. In all catchments, indicators of nutrient enrichment were identified as the primary stressor, with climate change-sensitive indicators causing secondary effects (Loch Leven: additive, total phosphorus [TP] × precipitation; Pinios: additive, nitrate × dissolved oxygen; Lepsämänjoki: synergistic, TP × summer water temperature), the intensity of which varied between catchments and along the nutrient stressor gradient. Simple stressor change scenarios were constructed for each catchment and used in combination with mechanistic models to explore potential management responses. This approach can be used to explore the need for multiple stressor management in freshwaters, helping practitioners navigate a complex world of environmental change.
Article
In the 12 years since Dudgeon et al. (2006) reviewed major pressures on freshwater ecosystems, the biodiversity crisis in the world's lakes, reservoirs, rivers, streams and wetlands has deepened. While lakes, reservoirs and rivers cover only 2.3% of the Earth's surface, these ecosystems host at least 9.5% of the Earth's described animal species. Furthermore, using the World Wide Fund for Nature's Living Planet Index, freshwater population declines (83% between 1970 and 2014) continue to outpace contemporaneous declines in marine or terrestrial systems. The Anthropocene has brought multiple new and varied threats that disproportionately impact freshwater systems. We document 12 emerging threats to freshwater biodiversity that are either entirely new since 2006 or have since intensified: (i) changing climates; (ii) e‐commerce and invasions; (iii) infectious diseases; (iv) harmful algal blooms; (v) expanding hydropower; (vi) emerging contaminants; (vii) engineered nanomaterials; (viii) microplastic pollution; (ix) light and noise; (x) freshwater salinisation; (xi) declining calcium; and (xii) cumulative stressors. Effects are evidenced for amphibians, fishes, invertebrates, microbes, plants, turtles and waterbirds, with potential for ecosystem‐level changes through bottom‐up and top‐down processes. In our highly uncertain future, the net effects of these threats raise serious concerns for freshwater ecosystems. However, we also highlight opportunities for conservation gains as a result of novel management tools (e.g. environmental flows, environmental DNA) and specific conservation‐oriented actions (e.g. dam removal, habitat protection policies, managed relocation of species) that have been met with varying levels of success. Moving forward, we advocate hybrid approaches that manage fresh waters as crucial ecosystems for human life support as well as essential hotspots of biodiversity and ecological function. Efforts to reverse global trends in freshwater degradation now depend on bridging an immense gap between the aspirations of conservation biologists and the accelerating rate of species endangerment.
Article
Interactions among multiple anthropogenic stressors threaten freshwater fish and pose challenges for fisheries management and conservation. Previous studies of multiple‐stressor effects on freshwater fish suggest a prevalence of antagonistic interactions. However, taxonomy, life stage and/or environmental context likely modify the magnitude and direction of fish responses to multiple stressors. Stressor intensity, impact mechanism, exposure time and ecosystem size may further affect interaction outcomes. Large‐scale studies quantifying how these variables moderate stressor interactions are lacking. To address this knowledge gap, we performed a meta‐analysis of 29 factorial multiple‐stressor experiments to examine the influence of seven potential moderator variables on the magnitude and direction of stressor interactions. Using weighted random‐effects meta‐analytic models, we demonstrate the importance of taxonomic identity and life stage for interaction outcomes. In particular, Cypriniformes showed stronger antagonisms than Salmoniformes, as did larval fish compared to juveniles. Interaction outcomes also varied among the measured fish responses with survival yielding stronger antagonisms than biomass. Increasing experimental duration and volume of the experimental units both drove interactions towards synergisms, supporting findings from previous studies that synergisms take time and space to develop. In an era when the number of stressors affecting freshwater systems is increasing rapidly, our study provides a vital step towards identifying generalities in multiple‐stressor outcomes and thus improved predictions of multiple‐stressor impacts. Furthermore, our meta‐analysis complements studies in real streams, rivers and lakes by providing an experimentally derived context for the growing number of multiple‐stressor assessments in research, management and conservation of freshwater fish.
Article
While there is a lot of data on interactive effects of eutrophication and warming, to date, we lack data to generate reliable predictions concerning possible effects of nutrient decrease and temperature increase on community composition and functional responses. In recent years, a wide‐ranging trend of nutrient decrease (re‐oligotrophication) was reported for freshwater systems. Small lakes and ponds, in particular, show rapid responses to anthropogenic pressures and became model systems to investigate single as well as synergistic effects of warming and fertilization in situ and in experiments. Therefore, we set up an experiment to investigate the single as well as the interactive effects of nutrient reduction and gradual temperature increase on a natural freshwater phytoplankton community, using an experimental indoor mesocosm setup. Biomass production initially increased with warming but decreased with nutrient depletion. If nutrient supply was constant, biomass increased further, especially under warming conditions. Under low nutrient supply, we found a sharp transition from initially positive effects of warming to negative effects when resources became scarce. Warming reduced phytoplankton richness and evenness, whereas nutrient reduction at ambient temperature had positive effects on diversity. Our results indicate that temperature effects on freshwater systems will be altered by nutrient availability. These interactive effects of energy increase and resource decrease have major impacts on biodiversity and ecosystem function and thus need to be considered in environmental management plans. This article is protected by copyright. All rights reserved.
Article
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.
Article
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. This article is protected by copyright. All rights reserved.
Article
As contaminants are often more toxic at higher temperatures, predicting their impact under global warming remains a key challenge for ecological risk assessment. Ignoring delayed effects, synergistic interactions between contaminants and warming, and differences in sensitivity across species' ranges could lead to an important underestimation of the risks. We addressed all three mechanisms by studying effects of larval exposure to zinc and warming before, during and after metamorphosis in Ischnura elegans damselflies from high- and low-latitude populations. By integrating these mechanisms into a single study we could identify two novel patterns. Firstly, during exposure zinc did not affect survival, whereas it induced mild to moderate post-exposure mortality in the larval stage and at metamorphosis, and very strongly reduced adult lifespan. This severe delayed effect across metamorphosis was especially remarkable in high-latitude animals, as they appeared almost insensitive to zinc during the larval stage. Secondly, the well-known synergism between metals and warming was manifested not only during the larval stage but also after metamorphosis, yet notably only in low-latitude damselflies. These results highlight that a more complete life-cycle approach that incorporates the possibility of delayed interactions between contaminants and warming in a geographical context is crucial for a more realistic risk assessment in a warming world.
Code
Tools for performing model selection and model averaging. Automated model selection through subsetting the maximum model, with optional constraints for model inclusion. Model parameter and prediction averaging based on model weights derived from information criteria (AICc and alike) or custom model weighting schemes. [Please do not request the full text - it is an R package. The up-to-date manual is available from CRAN].
Article
Using a long-term (1995–2014) monitoring network, from 51 sampling stations in estuaries and coasts of the Basque Country (Bay of Biscay), the objective of this investigation was to assess the responsiveness of 83 variables in water (18), sediments (27), biota (26), phytoplankton (2), macroinvertebrates (5) and fishes (5) to different human pressures and management actions. We used a total of 3247 series of data to analyse trends of improvement and worsening in quality. In a high percentage of the cases, the management actions taken have resulted in positive effects in the environment, as shown by the trend analysis in this investigation. Overall, much more trends of improvement than of worsening have been observed; this is true for almost all the media and biological components studied, with the exception of phytoplankton; and it applies as well to almost all the stations and water bodies, with the exception of those corresponding to areas with water treatment pending of accomplishment. In estuaries with decreasing human pressures during the period, the percentage of series showing quality improvement was higher (approx. 30%) than those showing worsening of quality (12%). Moreover, in those water bodies showing an increase of pressure, variables which can be considered indicators of anthropogenic effects showed negative trends (quality worsening). On the other hand, some of the variables analysed were more affected by natural variability than by changes in pressures. That was the case of silicate, nitrate and suspended solids, which followed trends correlated to salinity, which, in turn, was related to the rainfall regime during the study period.
Chapter
Eutrophication is the natural aging process of aquatic ecosystems, historically used in reference to the natural aging of lakes. It is sometimes defined as an increase in the rate of organic production or an increase in the total organic carbon. More recently, it has been used to mean “cultural” eutrophication wherein the natural aging process is greatly accelerated by human activities that add nutrients to the water, especially nitrogen and phosphorus, which promote excessive algal growth and biomass accumulation, lower biodiversity at all trophic levels, and other adverse impacts. Oligotrophication is a partial reversal of the eutrophication process, in which water becomes less nutrient-enriched and supports less plant and animal production.
Article
Global climate change will undoubtedly be a pressure on coastal marine ecosystems, not only affecting species distributions and physiology but also ecosystem functioning. In the coastal zone, the environmental variables that may drive ecological responses to climate change include temperature, wave energy, upwelling events and freshwater inputs, and all act and interact at a variety of spatial and temporal scales). To date we have a poor understanding of how climate-related environmental changes may affect coastal marine ecosystems or which environmental variables are likely to produce priority effects. Here we use time series data (17 years) of coastal benthic macrofauna to investigate responses to a range of climate influenced variables including sea surface temperature, southern oscillation indices (SOI, Z4), wind-wave exposure, freshwater inputs and rainfall. We investigate responses from the abundances of individual species to abundances of functional traits and test whether species that are near the edge of their tolerance to another stressor (in this case sedimentation) may exhibit stronger responses. The responses we observed were all nonlinear and exhibited thresholds. While temperature was most frequently an important predictor, wave exposure and ENSO-related variables were also frequently important and most ecological variables responded to interactions between environmental variables. There were also indications that species sensitive to another stressor responded more strongly to weaker climate-related environmental change at the stressed site than the unstressed site. The observed interactions between climate variables, effects on key species or functional traits, and synergistic effects of additional anthropogenic stressors have important implications for understanding and predicting the ecological consequences of climate change to coastal ecosystems. This article is protected by copyright. All rights reserved.
Article
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. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Article
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 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 co-stressors than any other stressor, with ~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. This article is protected by copyright. All rights reserved.
Article
The interdisciplinary area of stress ecology provides education, government, and industry with an integrative area in which to apply jointly a quantitative, problem-solving approach to many of society's environmental problems. Ten guidelines are suggested for establishing programs in stress ecology, which would provide on-the-job training opportunities for students and personnel with diverse liberal arts and applied backgrounds. Evaluating stress response on ecosystems could serve as an integrative focal point for these programs.