Energy limitation or sensitive predators? Trophic and non-trophic impacts of wastewater pollution on stream food webs.

community size spectra energy transfer food webs stable isotopes water quality

Journal

Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541

Informations de publication

Date de publication:
02 2022
Historique:
received: 30 05 2021
accepted: 20 08 2021
pubmed: 19 11 2021
medline: 1 4 2022
entrez: 18 11 2021
Statut: ppublish

Résumé

Impacts of environmental stressors on food webs are often difficult to predict because trophic levels can respond in divergent ways, and biotic interactions may dampen or amplify responses. Here we studied food-web-level impacts of urban wastewater pollution, a widespread source of degradation that can alter stream food webs via top-down and bottom-up processes. Wastewater may (1) subsidize primary producers by decreasing nutrient limitation, inducing a wide-bottomed trophic pyramid. However, (2) wastewater may also reduce the quality and diversity of resources, which could decrease energy transfer efficiency by reducing consumer fitness, leading to predator starvation. Additionally, (3) if higher trophic levels are particularly sensitive to pollution, primary consumers could be released from predation pressure. We tested these hypotheses in 10 pairs of stream sites located upstream and downstream of urban wastewater effluents with different pollutant levels. We found that wastewater pollution reduced predator richness by ∼34%. Community size spectra (CSS) slopes were steeper downstream than upstream of wastewater effluents in all except one impact site where predators became locally extinct. Further, variation in downstream CSS slopes were correlated with pollution loads: the more polluted the stream, the steeper the CSS. We estimate that wastewater pollution decreased energy transfer efficiencies to primary consumers by ∼70%, limiting energy supply to predators. Additionally, traits increasing vulnerability to chemical pollution were overrepresented among predators, which presented compressed trophic niches (δ

Identifiants

pubmed: 34792187
doi: 10.1002/ecy.3587
doi:

Substances chimiques

Waste Water 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e03587

Informations de copyright

© 2021 The Authors. Ecology published by Wiley Periodicals LLC on behalf of Ecological Society of America.

Références

Acuña, V., I. Muñoz, A. Giorgi, M. Omella, F. Sabater, and S. Sabater. 2005. Drought and postdrought recovery cycles in an intermittent Mediterranean stream: structural and functional aspects. Journal of the North American Benthological Society 24:919-933.
Arim, M., S. R. Abades, G. Laufer, M. Loureiro, and P. A. Marquet. 2010. Food web structure and body size: trophic position and resource acquisition. Oikos 119:147-153.
Baselga, A., D. Orme, S. Villeger, J. de Bortoli, and F. Leprieur. 2017. betapart: partitioning beta diversity into turnover and nestedness components. R package version 1.4-1. https://cran.r-project.org/package=betapart
Benke, A. C., A. D. Huryn, and G. M. Ward. 1998. Use of empirical models of stream invertebrate secondary production as applied to a functional feeding group. Internationale Vereinigung Für Theoretische Und Angewandte Limnologie: Verhandlungen 26:2024-2029.
Birk, S., et al. 2020. Impacts of multiple stressors on freshwater biota across spatial scales and ecosystems. Nature Ecology & Evolution 4:1-8.
Bonada, N. and S. Dolédec. 2011. Do Mediterranean genera not included in Tachet et al. 2002 have Mediterranean trait characteristics? Limnetica 30:129-142.
Brose, U., et al. 2017. Predicting the consequences of species loss using size-structured biodiversity approaches. Biological Reviews 92:684-697.
Bruno, J. F., and B. J. Cardinale. 2008. Cascading effects of predator richness. Frontiers in Ecology and the Environment 6:539-546.
Burgherr, P., and E. I. Meyer. 1997. Regression analysis of linear body dimensions vs. dry mass in stream macroinvertebrates. Archiv Für Hydrobiologie 139:101-112.
Cardinale, B. J., D. S. Srivastava, J. E. Duffy, J. P. Wright, A. L. Downing, M. Sankaran, and C. Jouseau. 2006. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989-992.
Carey, R. O., and K. W. Migliaccio. 2009. Contribution of wastewater treatment plant effluents to nutrient dynamics in aquatic systems: a review. Environmental Management 44:205-217.
Clement, T. A., B. A. Murry, and D. G. Uzarski. 2015. Fish community size structure of small lakes: the role of lake size, biodiversity and disturbance. Journal of Freshwater Ecology 30:557-568.
Cross, W. F., C. V. Baxter, E. J. Rosi-Marshall, R. O. Hall, T. A. Kennedy, K. C. Donner, H. A. Wellard Kelly, S. E. Z. Seegert, K. E. Behn, and M. D. Yard. 2013. Food-web dynamics in a large river discontinuum. Ecological Monographs 83:311-337.
Cucherousset, J., and S. Villéger. 2015. Quantifying the multiple facets of isotopic diversity: New metrics for stable isotope ecology. Ecological Indicators 56:152-160.
Daan, N., H. G. Gislason, J. Pope, and J. C. Rice. 2005. Changes in the North Sea fish community: evidence of indirect effects of fishing? ICES Journal of Marine Science 62:177-188.
Davis, J. M., A. D. Rosemond, S. L. Eggert, W. F. Cross, and J. B. Wallace. 2010. Long-term nutrient enrichment decouples predator and prey production. Proceedings of the National Academy of Sciences USA 107:121-126.
deBruyn, A. M. H., D. J. Marcogliese, and J. B. Rasmussen. 2003. The role of sewage in a large river food web. Canadian Journal of Fisheries and Aquatic Sciences 60:1332-1344.
di Lascio, A., L. Rossi, P. Carlino, E. Calizza, D. Rossi, and M. L. Costantini. 2013. Stable isotope variation in macroinvertebrates indicates anthropogenic disturbance along an urban stretch of the river Tiber (Rome, Italy). Ecological Indicators 28:107-114.
Dickman, E. M., J. M. Newell, M. J. González, and M. J. Vanni. 2008. Light, nutrients, and food-chain length constrain planktonic energy transfer efficiency across multiple trophic levels. Proceedings of the National Academy of Sciences USA 105:18408-18412.
Dossena, M., G. Yvon-Durocher, J. Grey, J. M. Montoya, D. M. Perkins, M. Trimmer, and G. Woodward. 2012. Warming alters community size structure and ecosystem functioning. Proceedings of the Royal Society B 279:3011-3019.
Dudgeon, D., et al. 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81:163-182.
Fox, J., and S. Weisberg. 2019. An R companion to applied regression. Third edition. Sage, Thousand Oaks, California, USA.
Fraley, K. M., H. J. Warburton, P. G. Jellyman, D. Kelly, and A. R. McIntosh. 2018. Responsiveness of fish mass-abundance relationships and trophic metrics to flood disturbance, stream size, land cover and predator taxa presence in headwater streams. Ecology of Freshwater Fish 27:999-1014.
He, F., C. Zarfl, V. Bremerich, J. N. W. David, Z. Hogan, G. Kalinkat, K. Tockner, and S. C. Jähnig. 2019. The global decline of freshwater megafauna. Global Change Biology 25:3883-3892.
Hernando, M. D., M. Mezcua, A. R. Fernández-Alba, and D. Barceló. 2006. Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 69:334-342.
Jackson, A. L., R. Inger, A. C. Parnell, and S. Bearhop. 2011. Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80:595-602.
Kraus, J. M., J. F. Pomeranz, A. S. Todd, D. M. Walters, T. S. Schmidt, and R. B. Wanty. 2016. Aquatic pollution increases use of terrestrial prey subsidies by stream fish. Journal of Applied Ecology 53:44-53.
Kuzmanovic, M., A. Ginebreda, M. Petrovic, and D. Barceló. 2015. Risk assessment based prioritization of 200 organic micropollutants in 4 Iberian rivers. Science of the Total Environment 503-504:289-299.
Ledger, M. E., L. E. Brown, F. K. Edwards, A. M. Milner, and G. Woodward. 2013. Drought alters the structure and functioning of complex food webs. Nature Climate Change 3:223-227.
Mandaric, L., J. R. Mor, S. Sabater, and M. Petrovic. 2018. Impact of urban chemical pollution on water quality in small, rural and effluent-dominated Mediterranean streams and rivers. Science of the Total Environment 613-614:763-772.
Marti, E., J. Aumatell, L. Godé, M. Poch, and F. Sabater. 2004. Nutrient retention efficiency in streams receiving inputs from wastewater treatment plants. Journal of Environmental Quality 33:285-293.
Martínez, A., A. Larrañaga, A. Miguélez, G. Yvon-Durocher, and J. Pozo. 2016. Land use change affects macroinvertebrate community size spectrum in streams: the case of Pinus radiata plantations. Freshwater Biology 61:69-79.
McCann, K., A. Hastings, and G. R. Huxel. 1998. Weak trophic interactions and the balance of nature. Nature 395:794-798.
McHugh, P. A., A. R. McIntosh, and P. G. Jellyman. 2010. Dual influences of ecosystem size and disturbance on food chain length in streams. Ecology Letters 13:881-890.
Meyer, E. I., and R. Poepperl. 2003. Secondary production of invertebrates in a Central European mountain stream (Steina, Black Forest, Germany). Archiv Fur Hydrobiologie 158:25-42.
Mor, J. R., S. Dolédec, V. Acuña, S. Sabater, and I. Muñoz. 2019. Invertebrate community responses to urban wastewater effluent pollution under different hydro-morphological conditions. Environmental Pollution 252:483-492.
Mor, J.-R., I. Muñoz, S. Sabater, L. Zamora, and A. Ruhi. 2021. Energy limitation or sensitive predators? Trophic and non-trophic impacts of wastewater pollution on stream food webs. Dryad, Data Set. https://doi.org/10.6078/D1KH7C
Mulder, C., and J. J. Elser. 2009. Soil acidity, ecological stoichiometry and allometric scaling in grassland food webs. Global Change Biology 15:2730-2738.
O'Connor, N. E., and I. Donohue. 2013. Environmental context determines multi-trophic effects of consumer species loss. Global Change Biology 19:431-440.
Palmer, M., and A. Ruhi. 2019. Linkages between flow regime, biota, and ecosystem processes: Implications for river restoration. Science 365.
Pereda, O., D. von Schiller, G. García-Baquero, J. R. Mor, V. Acuña, S. Sabater, and A. Elosegi. 2021. Combined effects of urban pollution and hydrological stress on ecosystem functions of Mediterranean streams. Science of the Total Environment 753:141971.
Perkins, D. M., et al. 2018. Bending the rules: exploitation of allochthonous resources by a top-predator modifies size-abundance scaling in stream food webs. Ecology Letters 21:1771-1780.
Pimm, S. L., and J. H. Lawton. 1977. Number of trophic levels in ecological communities. Nature 268:329-331.
Pomeranz, J. P. F., H. J. Warburton, and J. S. Harding. 2019. Anthropogenic mining alters macroinvertebrate size spectra in streams. Freshwater Biology 64:81-92.
Post, D. M. 2002. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703-718.
Power, M. E., M. S. Parker, and W. E. Dietrich. 2008. Seasonal reassembly of a river food web: floods, droughts, and impacts of fish. Ecological Monographs 78:263-282.
Queirós, A. M., J. G. Hiddink, M. J. Kaiser, and H. Hinz. 2006. Effects of chronic bottom trawling disturbance on benthic biomass, production and size spectra in different habitats. Journal of Experimental Marine Biology and Ecology 335:91-103.
Rabení, C. F., K. E. Doisy, and L. D. Zweig. 2005. Stream invertebrate community functional responses to deposited sediment. Aquatic Sciences 67:395-402.
Reuman, D. C., C. Mulder, D. Raffaelli, and J. E. Cohen. 2009. Three allometric relations of population density to body mass: theoretical integration and empirical tests in 149 food webs. Ecology Letters 11:1216-1228.
Sabater, S., F. Bregoli, V. Acuña, D. Barceló, A. Elosegi, A. Ginebreda, R. Marcé, I. Muñoz, L. Sabater-Liesa, and V. Ferreira. 2018. Effects of human-driven water stress on river ecosystems: a meta-analysis. Scientific Reports 8:1-11.
Sabater, S., and K. Tockner. 2009. Effects of hydrologic alterations on the ecological quality of river ecosystems. Pages 15-39 in S. Sabater and D. Barceló, editors. Water scarcity in the Mediterranean. The Handbook of Environmental Chemistry. Volume 8. Springer, Heidelberg, Berlin, Germany.
Sabater-Liesa, L., N. Montemurro, C. Font, A. Ginebreda, J. D. González-Trujillo, N. Mingorance, S. Pérez, and D. Barceló. 2019. The response patterns of stream biofilms to urban sewage change with exposure time and dilution. Science of the Total Environment 674:401-411.
Schwarzmüller, F., N. Eisenhauer, and U. Brose. 2015. ‘Trophic whales’ as biotic buffers: weak interactions stabilize ecosystems against nutrient enrichment. Journal of Animal Ecology 84:680-691.
Segner, H., M. Schmitt-Jansen, and S. Sabater. 2014. Assesing the impact of multiple stressors on aquatic biota: the receptor's side matters. Environmental Science and Technology 48:7690-7696.
Singer, G. A., and T. J. Battin. 2007. Anthropogenic subsidies alter stream consumer-resource stoichiometry, biodiversity, and food chains. Ecological Applications 17:376-389.
Tachet, H., P. Richoux, M. Bournaud, and P. Usseglio-Polatera. 2010. Invertébrés d'Eau Douce. CNRS éditions. CNRS, Paris, France.
Tickner, D., et al. 2020. Bending the curve of global freshwater biodiversity loss: an emergency recovery plan. BioScience 70:330-342.
White, E. P., S. M. Ernest, A. J. Kerkhoff, and B. J. Enquist. 2007. Relationships between body size and abundance in ecology. Trends in Ecology & Evolution 22:323-330.
Wilcoxon, F. 1945. Individual comparisons by ranking methods. Biometrics Bulletin 1:80-83.
Wilson, S. K., R. Fisher, M. S. Pratchett, N. A. J. Graham, N. K. Dulvy, R. A. Turner, A. Cakacaka, and N. V. C. Polunin. 2010. Habitat degradation and fishing effects on the size structure of coral reef fish communities. Ecological Applications 20:442-451.
Woodward, G., L. E. Brown, F. K. Edwards, L. N. Hudson, A. M. Milner, D. C. Reuman, and M. E. Ledger. 2012. Climate change impacts in multispecies systems: Drought alters food web size structure in a field experiment. Philosophical Transactions of the Royal Society B 367:2990-2997.
Woodward, G., and P. Warren. 2006. Body size and predatory interactions in freshwaters: scaling from individuals to communities. Pages 98-117 in A. G. Hildrew, D. Raffaelli, and R. Edmonds-Brown, editors. Body size: the structure and function of aquatic ecosystems. Cambridge University Press, Cambridge, UK.
Yvon-Durocher, G., and A. P. Allen. 2012. Linking community size structure and ecosystem functioning using metabolic theory. Philosophical Transactions of the Royal Society 367:2998-3007.
Zhang, H., E. S. Rutherford, D. M. Mason, J. T. Breck, M. E. Wittmann, R. M. Cooke, D. M. Lodge, J. D. Rothlisberger, X. Zhu, and T. B. Johnson. 2016. Forecasting the impacts of silver and bighead carp on the Lake Erie food web. Transactions of the American Fisheries Society 145:136-162.

Auteurs

Jordi-René Mor (JR)

Catalan Institute for Water Research (ICRA), Girona, 17003, Spain.
Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, Universitat de Barcelona (UB), Barcelona, 08014, Spain.

Isabel Muñoz (I)

Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, Universitat de Barcelona (UB), Barcelona, 08014, Spain.

Sergi Sabater (S)

Catalan Institute for Water Research (ICRA), Girona, 17003, Spain.
Institute of Aquatic Ecology, University of Girona, Girona, 17003, Spain.

Lluís Zamora (L)

Institute of Aquatic Ecology, University of Girona, Girona, 17003, Spain.

Albert Ruhi (A)

Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, California, 94720, USA.

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