Multiple-stressor effects on freshwater fish: Importance of taxonomy and life stage

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.

[1]  J. Olden,et al.  Declining streamflow induces collapse and replacement of native fish in the American Southwest , 2016 .

[2]  W. Darwall,et al.  Conservation of Freshwater Fishes: Lost fishes, who is counting? The extent of the threat to freshwater fish biodiversity , 2015 .

[3]  F. D. Shields,et al.  Use of the index of biotic integrity to assess physical habitat degradation in warmwater streams , 1995, Hydrobiologia.

[4]  E. R. Keeley,et al.  Temperature-Related Changes in Habitat Quality and Use by Bonneville Cutthroat Trout in Regulated and Unregulated River Segments , 2012 .

[5]  Charlie J. G. Loewen,et al.  Net effects of multiple stressors in freshwater ecosystems: a meta‐analysis , 2016, Global change biology.

[6]  David A. Bohan,et al.  Mesocosm Experiments as a Tool for Ecological Climate-Change Research , 2013 .

[7]  W. Darwall,et al.  Why are freshwater fish so threatened , 2015 .

[8]  C. Matthaei,et al.  Multiple stressor effects on freshwater fish: a review and meta-analysis , 2015 .

[9]  H. Segner,et al.  Assessing the impact of multiple stressors on aquatic biota: the receptor's side matters. , 2014, Environmental science & technology.

[10]  M. Rosenberg,et al.  THE FILE‐DRAWER PROBLEM REVISITED: A GENERAL WEIGHTED METHOD FOR CALCULATING FAIL‐SAFE NUMBERS IN META‐ANALYSIS , 2005, Evolution; international journal of organic evolution.

[11]  Jonathan A C Sterne,et al.  The Funnel Plot , 2006 .

[12]  A Whitehead,et al.  Meta‐analysis of continuous outcome data from individual patients , 2001, Statistics in medicine.

[13]  M. Lemus,et al.  Paraquat and temperature affect nonspecific immune response of Colossoma macropomum. , 2009, Environmental toxicology and pharmacology.

[14]  Á. Borja,et al.  Quantified biotic and abiotic responses to multiple stress in freshwater, marine and ground waters. , 2016, The Science of the total environment.

[15]  Shinichi Nakagawa,et al.  Methodological issues and advances in biological meta-analysis , 2012, Evolutionary Ecology.

[16]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[17]  B. Barton Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in Circulating Corticosteroids1 , 2002, Integrative and comparative biology.

[18]  C. Townsend,et al.  Individual and combined responses of stream ecosystems to multiple stressors , 2008 .

[19]  A. Gelman Scaling regression inputs by dividing by two standard deviations , 2008, Statistics in medicine.

[20]  C. Brown,et al.  Interactions among ecosystem stressors and their importance in conservation , 2016, Proceedings of the Royal Society B: Biological Sciences.

[21]  J. Armstrong,et al.  Fishes in a changing world: learning from the past to promote sustainability of fish populations. , 2018, Journal of fish biology.

[22]  C. Townsend,et al.  Reconceptualizing synergism and antagonism among multiple stressors , 2015, Ecology and evolution.

[23]  I. Cuthill,et al.  Effect size, confidence interval and statistical significance: a practical guide for biologists , 2007, Biological reviews of the Cambridge Philosophical Society.

[24]  Effects of chronic environmental acidification and a summer global warming scenario : protein synthesis in juvenile rainbow trout ( Oncorhynchus mykiss ) , 1997 .

[25]  Jessica Gurevitch,et al.  The Interaction between Competition and Predation: A Meta‐analysis of Field Experiments , 2000, The American Naturalist.

[26]  M. Scheffer,et al.  Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co‐tolerance , 2004 .

[27]  S. Hurlbert Pseudoreplication and the Design of Ecological Field Experiments , 1984 .

[28]  Benjamin S Halpern,et al.  Interactive and cumulative effects of multiple human stressors in marine systems. , 2008, Ecology letters.

[29]  M. J. Hatcher,et al.  Predator cue studies reveal strong trait-mediated effects in communities despite variation in experimental designs , 2013, Animal Behaviour.

[30]  M. Moore,et al.  Synergism and antagonism among multiple stressors , 1999 .

[31]  J. S. Alabaster,et al.  Water Quality Criteria for Freshwater Fish , 1982 .

[32]  Michael A. Turner,et al.  Multiple anthropogenic stressors cause ecological surprises in boreal lakes , 2006 .

[33]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[34]  D. Goffaux,et al.  Assessing river biotic condition at a continental scale: a European approach using functional metrics and fish assemblages , 2006 .

[35]  T. Linton,et al.  Effects of chronic environmental acidification and a summer global warming scenario: protein synthesis in juvenile rainbow trout (Oncorhynchus mykiss) , 1997 .

[36]  María González,et al.  Effects of agricultural subsidies of nutrients and detritus on fish and plankton of shallow-reservoir ecosystems. , 2009, Ecological applications : a publication of the Ecological Society of America.

[37]  I. Côté,et al.  Quantifying the evidence for ecological synergies. , 2008, Ecology letters.

[38]  S. Schmutz,et al.  Untangling the effects of multiple human stressors and their impacts on fish assemblages in European running waters. , 2016, The Science of the total environment.

[39]  G. Woodward,et al.  Climate change and freshwater ecosystems: impacts across multiple levels of organization , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  Peter E. Jones,et al.  Biotic interactions modify multiple‐stressor effects on juvenile brown trout in an experimental stream food web , 2017, Global change biology.

[41]  J. Mckim Evaluation of Tests with Early Life Stages of Fish for Predicting Long-Term Toxicity , 1977 .

[42]  Corey J A Bradshaw,et al.  Synergies among extinction drivers under global change. , 2008, Trends in ecology & evolution.

[43]  J. M. Elliott,et al.  Pools as refugia for brown trout during two summer droughts: trout responses to thermal and oxygen stress , 2000 .

[44]  M. Power Assessing the effects of environmental stressors on fish populations , 1997 .