Combined effects of climate warming and pharmaceuticals on a tri-trophic freshwater food web

Multiple anthropogenic stressors influence the functioning of ponds and lakes, but their combined effects are often little understood. We ran two mesocosm experiments to evaluate the effects of warming (+4°C above ambient) and environmentally relevant concentrations of a mixture of commonly used pharmaceuticals, an emerging class of chemical contaminants, on tri-trophic food webs representative of pelagic communities in ponds and other small standing waters. We quantified the main and interactive effects of warming and pharmaceuticals on each trophic level and attributed them to the direct effects of both stressors and the indirect effects arising through biotic interactions. Warming and pharmaceuticals had stronger effects in the summer experiment, altering zooplankton community composition and causing delayed or accelerated emergence of top insect predators. In summer, both stressors and top predators reduced filter-feeding zooplankton biomass, while warming and pharmaceuticals had opposing effects on phytoplankton. In the winter experiment, the effects were much weaker and primarily limited to a positive effect of warming on phytoplankton biomass. Overall, we show that pharmaceuticals can exacerbate the effects of climate warming in freshwater ecosystems, especially during the warm season. Our results demonstrate the utility of community-level studies across different seasons for the risk assessment of multiple emerging stressors in freshwater ecosystems.

[1]  K. V. Dinh,et al.  Winter is coming: Interactions of multiple stressors in winter and implications for the natural world , 2023, Global change biology.

[2]  Charlie J. G. Loewen,et al.  Local stressors mask the effects of warming in freshwater ecosystems , 2022, Ecology letters.

[3]  Salem S. Gharbia,et al.  Pharmaceutical pollution of the world’s rivers , 2022, Proceedings of the National Academy of Sciences.

[4]  M. Jackson,et al.  Combined effects of heatwaves and micropollutants on freshwater ecosystems: Towards an integrated assessment of extreme events in multiple stressors research , 2021, Global change biology.

[5]  F. Sánchez-Bayo,et al.  Indirect Effect of Pesticides on Insects and Other Arthropods , 2021, Toxics.

[6]  B. Brooks,et al.  Water reuse for aquaculture: Comparative removal efficacy and aquatic hazard reduction of pharmaceuticals by a pond treatment system during a one year study. , 2021, Journal of hazardous materials.

[7]  N. Fohrer,et al.  Influences of pesticides, nutrients, and local environmental variables on phytoplankton communities in lentic small water bodies in a German lowland agricultural area. , 2021, The Science of the total environment.

[8]  B. Brooks,et al.  De facto reuse at the watershed scale: Seasonal changes, population contributions, instream flows and water quality hazards of human pharmaceuticals. , 2020, Environmental pollution.

[9]  J. Porcher,et al.  Effects of chronic exposure to a pharmaceutical mixture on the three-spined stickleback (gasterosteus aculeatus) population dynamics in lotic mesocosms. , 2020, Aquatic toxicology.

[10]  L. Hansson,et al.  Different climate scenarios alter dominance patterns among aquatic primary producers in temperate systems , 2020, Limnology and Oceanography.

[11]  T. Crowe,et al.  Combined Effects of Multiple Stressors: New Insights Into the Influence of Timing and Sequence , 2019, Front. Ecol. Evol..

[12]  D. Boukal,et al.  Species interactions under climate change: connecting kinetic effects of temperature on individuals to community dynamics. , 2019, Current opinion in insect science.

[13]  J. Oehlmann,et al.  Interactive effects of biotic and abiotic environmental stressors on carbamazepine toxicity in the non-biting midge Chironomus riparius. , 2019, Water research.

[14]  J. Reiss,et al.  Antibiotic pollution in surface fresh waters: Occurrence and effects. , 2019, The Science of the total environment.

[15]  V. Žlábek,et al.  Foraging behaviour of top predators mediated by pollution of psychoactive pharmaceuticals and effects on ecosystem stability. , 2019, The Science of the total environment.

[16]  J. Fick,et al.  Behavioural effects of psychoactive pharmaceutical exposure on European perch (Perca fluviatilis) in a multi-stressor environment. , 2019, The Science of the total environment.

[17]  R. Dewil,et al.  Pharmaceuticals in freshwater aquatic environments: A comparison of the African and European challenge. , 2019, The Science of the total environment.

[18]  Topi K. Lehtonen,et al.  The pharmaceutical pollutant fluoxetine alters reproductive behaviour in a fish independent of predation risk. , 2019, The Science of the total environment.

[19]  K. Yeager,et al.  Phytoplankton response to climate changes and anthropogenic activities recorded by sedimentary pigments in a shallow eutrophied lake. , 2019, The Science of the total environment.

[20]  E. Jeppesen,et al.  Fish-mediated plankton responses to increased temperature in subtropical aquatic mesocosm ecosystems: Implications for lake management. , 2018, Water research.

[21]  E. Jongejans,et al.  Population‐level responses to temperature, density and clonal differences in Daphnia magna as revealed by integral projection modelling , 2018, Functional Ecology.

[22]  H. Paerl,et al.  Cyanobacterial blooms , 2018, Nature Reviews Microbiology.

[23]  L. Blaustein,et al.  Pesticide-mediated trophic cascade and an ecological trap for mosquitoes , 2018 .

[24]  A. Soares,et al.  Invasive Species Mediate Insecticide Effects on Community and Ecosystem Functioning. , 2018, Environmental science & technology.

[25]  R. Stoks,et al.  Negative effects of pesticides under global warming can be counteracted by a higher degradation rate and thermal adaptation , 2017 .

[26]  J. Fick,et al.  Bioaccumulation of psychoactive pharmaceuticals in fish in an effluent dominated stream. , 2017, Water research.

[27]  D. Baird,et al.  Shifts of community composition and population density substantially affect ecosystem function despite invariant richness. , 2017, Ecology letters.

[28]  L. Hansson,et al.  Phytoplankton diversity loss along a gradient of future warming and brownification in freshwater mesocosms , 2017 .

[29]  Peifang Wang,et al.  Bioaccumulation and trophic transfer of pharmaceuticals in food webs from a large freshwater lake. , 2017, Environmental pollution.

[30]  E. Jeppesen,et al.  Warming and nutrient enrichment in combination increase stochasticity and beta diversity of bacterioplankton assemblages across freshwater mesocosms , 2016, The ISME Journal.

[31]  J. Fick,et al.  Bioaccumulation of five pharmaceuticals at multiple trophic levels in an aquatic food web - Insights from a field experiment. , 2016, The Science of the total environment.

[32]  P. Cadmus,et al.  Low-cost floating emergence net and bottle trap: comparison of two designs , 2016 .

[33]  Colin R. Janssen,et al.  Per capita interactions and stress tolerance drive stress-induced changes in biodiversity effects on ecosystem functions , 2016, Nature Communications.

[34]  J. Ellis,et al.  Multiple stressors, nonlinear effects and the implications of climate change impacts on marine coastal ecosystems , 2016, Global change biology.

[35]  Akihiko Hirose,et al.  Chronic toxicity of an environmentally relevant mixture of pharmaceuticals to three aquatic organisms (alga, daphnid, and fish) , 2016, Environmental toxicology and chemistry.

[36]  I. Lopes,et al.  Multiple Stressor Differential Tolerances: Possible Implications at the Population Level , 2016, PloS one.

[37]  J. Stark,et al.  Pesticide-Induced Stress in Arthropod Pests for Optimized Integrated Pest Management Programs. , 2016, Annual review of entomology.

[38]  Kevin J. Gaston,et al.  Five Years of Experimental Warming Increases the Biodiversity and Productivity of Phytoplankton , 2015, PLoS biology.

[39]  Ç. Tavşanoğlu.  Ecology of climate change — the importance of biotic interactions , 2015, Folia Zoologica.

[40]  D. Boukal,et al.  Thermal acclimation modulates the impacts of temperature and enrichment on trophic interaction strengths and population dynamics , 2015, Global change biology.

[41]  R. Relyea,et al.  Submerged Macrophytes Mitigate Direct and Indirect Insecticide Effects in Freshwater Communities , 2015, PloS one.

[42]  Vimal Kumar,et al.  Presence of pharmaceuticals in benthic fauna living in a small stream affected by effluent from a municipal sewage treatment plant. , 2015, Water research.

[43]  O. Richter,et al.  Temperature response of growth of larval dragonflies – an overview , 2015 .

[44]  Tomas Brodin,et al.  Ecological effects of pharmaceuticals in aquatic systems—impacts through behavioural alterations , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  T. Backhaus.  Medicines, shaken and stirred: a critical review on the ecotoxicology of pharmaceutical mixtures , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  C. Chambliss,et al.  Bioaccumulation and trophic dilution of human pharmaceuticals across trophic positions of an effluent-dependent wadeable stream , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[47]  E. Jeppesen,et al.  Zooplankton response to climate warming: a mesocosm experiment at contrasting temperatures and nutrient levels , 2014, Hydrobiologia.

[48]  J. Fick,et al.  EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents. , 2013, Water research.

[49]  M. Solan,et al.  Long-term effects of warming and ocean acidification are modified by seasonal variation in species responses and environmental conditions , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  C. Beierkuhnlein,et al.  Ecological stress memory and cross stress tolerance in plants in the face of climate extremes , 2013 .

[51]  R. Kotter,et al.  Ecology of climate change: the importance of biotic interactions , 2013 .

[52]  D. Barceló,et al.  Response of biofilm bacterial communities to antibiotic pollutants in a Mediterranean river. , 2013, Chemosphere.

[53]  T. Royer,et al.  Pharmaceuticals suppress algal growth and microbial respiration and alter bacterial communities in stream biofilms. , 2013, Ecological applications : a publication of the Ecological Society of America.

[54]  C. Brönmark,et al.  Food-chain length alters community responses to global change in aquatic systems , 2013 .

[55]  G. Woodward,et al.  Warming alters community size structure and ecosystem functioning , 2012, Proceedings of the Royal Society B: Biological Sciences.

[56]  Patrick L. Thompson,et al.  Warming modifies trophic cascades and eutrophication in experimental freshwater communities. , 2012, Ecology.

[57]  Marco A. Lara,et al.  Climate extremes initiate ecosystem‐regulating functions while maintaining productivity , 2011 .

[58]  G. Woodward,et al.  Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems , 2011 .

[59]  P. McIntyre,et al.  Global threats to human water security and river biodiversity , 2010, Nature.

[60]  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.

[61]  S. Collins,et al.  A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. , 2009, Ecology.

[62]  E. Levin,et al.  The toxicology of climate change: environmental contaminants in a warming world. , 2009, Environment international.

[63]  R. Relyea.  A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities , 2009, Oecologia.

[64]  R. Macdonald,et al.  Interactions between climate change and contaminants. , 2007, Marine pollution bulletin.

[65]  C. Beierkuhnlein,et al.  A new generation of climate‐change experiments: events, not trends , 2007 .

[66]  J. Belden,et al.  How Well Can We Predict the Toxicity of Pesticide Mixtures to Aquatic Life? , 2007, Integrated environmental assessment and management.

[67]  A. F. Bennett,et al.  An experimental test of evolutionary trade-offs during temperature adaptation , 2007, Proceedings of the National Academy of Sciences.

[68]  J. Stachowicz,et al.  Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammonium. , 2006, Ecology.

[69]  R. Naiman,et al.  Freshwater biodiversity: importance, threats, status and conservation challenges , 2006, Biological reviews of the Cambridge Philosophical Society.

[70]  S. Mabury,et al.  Effects of pharmaceutical mixtures in aquatic microcosms , 2004, Environmental toxicology and chemistry.

[71]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[72]  A. Dauta,et al.  Light and temperature effects on the growth rate of three freshwater [2pt] algae isolated from a eutrophic lake , 2002, Hydrobiologia.

[73]  G. Meehl,et al.  Climate extremes: observations, modeling, and impacts. , 2000, Science.

[74]  Peter M. Vitousek,et al.  Effects of plant composition and diversity on nutrient cycling , 1998 .

[75]  Michael H. Depledge,et al.  Community and population indicators of ecosystem health: targeting links between levels of biological organisation , 1997 .

[76]  P. Hamilton,et al.  Spatial Distribution of Plankton in Enclosures of Three Sizes , 1984 .

[77]  E. Barrett.  Impact of climate , 1974, Nature.

[78]  C. Braak,et al.  Canoco reference manual and user's guide , 2018 .

[79]  E. Donk,et al.  Warming advances top-down control and reduces producer biomass in a freshwater plankton community , 2017 .

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

[81]  U. Sommer,et al.  Temperature effects on phytoplankton diversity - The zooplankton link , 2014 .

[82]  E. Jeppesen,et al.  Zooplankton response to climate warming: a mesocosm experiment at contrasting temperatures and nutrient levels , 2014, Hydrobiologia.

[83]  C.J.F. ter Braak,et al.  Canoco Reference Manual and User’s Guide: Software for Ordination (version 5.0) , 2012 .

[84]  G. Woodward.  Integrative ecology : from molecules to ecosystems , 2010 .

[85]  H. Hillebrand,et al.  Chapter 1 - Hutchinson Reversed, or Why There Need to Be So Many Species , 2010 .

[86]  Wolf M. Mooij,et al.  The impact of climate warming on water temperature, timing of hatching and young-of-the-year growth of fish in shallow lakes in the Netherlands , 2008 .

[87]  S. Adams.  Assessing cause and effect of multiple stressors on marine systems. , 2005, Marine pollution bulletin.

[88]  Jonathan M. Chase,et al.  Trade‐offs in community ecology: linking spatial scales and species coexistence , 2004 .

[89]  I. Joint,et al.  Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms , 2002 .

[90]  C. Amoros.  Introduction pratique à la systématique des organismes des eaux continentales françaises - 5. Crustacés Cladocères , 1984 .