Trophic downgrading decreases species asynchrony and community stability regardless of climate warming.

climate change community stability microbial food web predator loss species asynchrony tank-bromeliad trophic cascades

Journal

Ecology letters
ISSN: 1461-0248
Titre abrégé: Ecol Lett
Pays: England
ID NLM: 101121949

Informations de publication

Date de publication:
Dec 2021
Historique:
revised: 26 08 2021
received: 10 03 2021
accepted: 30 08 2021
pubmed: 20 9 2021
medline: 16 11 2021
entrez: 19 9 2021
Statut: ppublish

Résumé

Theory and some evidence suggest that biodiversity promotes stability. However, evidence of how trophic interactions and environmental changes modulate this relationship in multitrophic communities is lacking. Given the current scenario of biodiversity loss and climate changes, where top predators are disproportionately more affected, filling these knowledge gaps is crucial. We simulated climate warming and top predator loss in natural microcosms to investigate their direct and indirect effects on temporal stability of microbial communities and the role of underlying stabilising mechanisms. Community stability was insensitive to warming, but indirectly decreased due to top predator loss via increased mesopredator abundance and consequent reduction of species asynchrony and species stability. The magnitude of destabilising effects differed among trophic levels, being disproportionally higher at lower trophic levels (e.g. producers). Our study unravels major patterns and causal mechanisms by which trophic downgrading destabilises large food webs, regardless of climate warming scenarios.

Identifiants

pubmed: 34537987
doi: 10.1111/ele.13885
doi:

Types de publication

Letter

Langues

eng

Sous-ensembles de citation

IM

Pagination

2660-2673

Informations de copyright

© 2021 John Wiley & Sons Ltd.

Références

Altermatt, F., Fronhofer, E.A., Garnier, A., Giometto, A., Hammes, F., Klecka, J. et al. (2015) Big answers from small worlds: a user's guide for protist microcosms as a model system in ecology and evolution. Methods in Ecology and Evolution, 6(2), 218-231.
Antiqueira, P.A.P., Petchey, O.L., dos Santos, V.P., de Oliveira, V.M. & Romero, G.Q. (2018a) Environmental change and predator diversity drive alpha and beta diversity in freshwater macro and microorganisms. Global Change Biology, 24(8), 3715-3728.
Antiqueira, P.A.P., Petchey, O.L. & Romero, G.Q. (2018b) Warming and top predator loss drive ecosystem multifunctionality. Ecology Letters, 21(1), 72-82.
Bernabé, T.N., de Omena, P.M., Santos, V.P.D., de Siqueira, V.M., de Oliveira, V.M. & Romero, G.Q. (2018) Warming weakens facilitative interactions between decomposers and detritivores, and modifies freshwater ecosystem functioning. Global Change Biology, 24(7), 3170-3186.
Britten, G.L., Dowd, M., Minto, C., Ferretti, F., Boero, F. & Lotze, H.K. (2014) Predator decline leads to decreased stability in a coastal fish community. Ecology Letters, 17(12), 1518-1525.
Brouard, O., Le Jeune, A.-H., Leroy, C., Cereghino, R., Roux, O., Pelozuelo, L. et al. (2011) Are algae relevant to the detritus-based food web in tank-bromeliads? PLoS One, 6(5), e20129.
Campbell, V., Murphy, G. & Romanuk, T.N. (2011) Experimental design and the outcome and interpretation of diversity-stability relations. Oikos, 120(3), 399-408.
Cardinale, B.J., Bennett, D.M., Nelson, C.E. & Gross, K. (2009) Does productivity drive diversity or vice versa? A test of the multivariate productivity-diversity hypothesis in streams. Ecology, 90(5), 1227-1241.
Cardinale, B.J., Duffy, J.E., Gonzalez, A., Hooper, D.U., Perrings, C., Venail, P. et al. (2012) Biodiversity loss and its impact on humanity. Nature, 486(7401), 59.
Daufresne, M., Lengfellner, K. & Sommer, U. (2009) Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences, 106(31), 12788-12793.
De Boeck, H.J., Bloor, J.M.G., Kreyling, J., Ransijn, J.C.G., Nijs, I., Jentsch, A. et al. (2018) Patterns and drivers of biodiversity-stability relationships under climate extremes. Journal of Ecology, 106(3), 890-902.
Doak, D.F., Bigger, D., Harding, E.K., Marvier, M.A., O'Malley, R.E. & Thomson, D. (1998) The statistical inevitability of stability-diversity relationships in community ecology. The American Naturalist, 151(3), 264-276.
Donohue, I., Petchey, O.L., Kéfi, S., Génin, A., Jackson, A.L., Yang, Q. et al. (2017) Loss of predator species, not intermediate consumers, triggers rapid and dramatic extinction cascades. Global Change Biology, 23(8), 2962-2972.
Donohue, I., Petchey, O.L., Montoya, J.M., Jackson, A.L., McNally, L., Viana, M. et al. (2013) On the dimensionality of ecological stability. Ecology Letters, 16(4), 421-429.
Duffy, J.E., Cardinale, B.J., France, K.E., McIntyre, P.B., Thébault, E. & Loreau, M. (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters, 10(6), 522-538.
Estes, J.A., Terborgh, J., Brashares, J.S., Power, M.E., Berger, J., Bond, W.J. et al. (2011) Trophic downgrading of planet Earth. Science, 333(6040), 301-306.
Finke, D.L. & Denno, R.F. (2004) Predator diversity dampens trophic cascades. Nature, 429(6990), 407.
Fussmann, K.E., Schwarzmüller, F., Brose, U., Jousset, A. & Rall, B.C. (2014) Ecological stability in response to warming. Nature Climate Change, 4(3), 206-210.
Geerts, A.N., Vanoverbeke, J., Vanschoenwinkel, B., Van Doorslaer, W., Feuchtmayr, H., Atkinson, D. et al. (2015) Rapid evolution of thermal tolerance in the water flea Daphnia. Nature Climate Change, 5(7), 665-668.
Gonzalez, A. & Loreau, M. (2009) The causes and consequences of compensatory dynamics in ecological communities. Annual Review of Ecology, Evolution and Systematics, 40, 393-414.
Hallett, L.M., Jones, S.K., MacDonald, A.A.M., Jones, M.B., Flynn, D.F., Ripplinger, J. et al. (2016) codyn: an R package of community dynamics metrics. Methods in Ecology and Evolution, 7(10), 1146-1151.
Halpern, B.S., Borer, E.T., Seabloom, E.W. & Shurin, J.B. (2005) Predator effects on herbivore and plant stability. Ecology Letters, 8(2), 189-194.
Hautier, Y., Tilman, D., Isbell, F., Seabloom, E.W., Borer, E.T. & Reich, P.B. (2015) Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science, 348(6232), 336-340.
Hector, A., Hautier, Y., Saner, P., Wacker, L., Bagchi, R., Joshi, J. et al. (2010) General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology, 91(8), 2213-2220.
Hillebrand, H., Bennett, D.M. & Cadotte, M.W. (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology, 89(6), 1510-1520.
Hooper, D.U., Adair, E.C., Cardinale, B.J., Byrnes, J.E.K., Hungate, B.A., Matulich, K.L. et al. (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature, 486(7401), 105.
Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S. et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs, 75(1), 3-35.
Houlahan, J.E., Currie, D.J., Cottenie, K., Cumming, G.S., Findlay, C.S., Fuhlendorf, S.D. et al. (2018) Negative relationships between species richness and temporal variability are common but weak in natural systems. Ecology, 99(11), 2592-2604.
IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Core Writing Team, Pachauri, R.K., Meyer, L.A.). IPCC, Geneva, Switzerland, pp. 151.
Isbell, F.I., Polley, H.W. & Wilsey, B.J. (2009) Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecology Letters, 12(5), 443-451.
Ives, A.R. & Carpenter, S.R. (2007) Stability and diversity of ecosystems. Science, 317(5834), 58-62.
Jiang, L., Joshi, H. & Patel, S.N. (2009) Predation alters relationships between biodiversity and temporal stability. The American Naturalist, 173(3), 389-399.
Jiang, L. & Pu, Z. (2009) Different effects of species diversity on temporal stability in single-trophic and multitrophic communities. The American Naturalist, 174(5), 651-659.
Kratina, P., Greig, H.S., Thompson, P.L., Carvalho-Pereira, T.S. & Shurin, J.B. (2012) Warming modifies trophic cascades and eutrophication in experimental freshwater communities. Ecology, 93(6), 1421-1430.
Kratina, P., Petermann, J.S., Marino, N.A., MacDonald, A.A. & Srivastava, D.S. (2017) Environmental control of the microfaunal community structure in tropical bromeliads. Ecology and Evolution, 7(5), 1627-1634.
Ladino, G., Ospina-Bautista, F., Estévez Varón, J., Jerabkova, L. & Kratina, P. (2019) Ecosystem services provided by bromeliad plants: a systematic review. Ecology and Evolution, 9(12), 7360-7372.
Lefcheck, J.S. (2016) piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods in Ecology and Evolution, 7(5), 573-579.
Lehman, C.L. & Tilman, D. (2000) Biodiversity, stability, and productivity in competitive communities. The American Naturalist, 156(5), 534-552.
Loreau, M. & de Mazancourt, C. (2008) Species synchrony and its drivers: neutral and nonneutral community dynamics in fluctuating environments. The American Naturalist, 172(2), E48-E66.
Loreau, M. & De Mazancourt, C. (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecology Letters, 16, 106-115.
Lund, J.W.G., Kipling, C. & Le Cren, E.D. (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia, 11(2), 143-170.
Ma, Z., Liu, H., Mi, Z., Zhang, Z., Wang, Y., Xu, W. et al. (2017) Climate warming reduces the temporal stability of plant community biomass production. Nature Communications, 8, 15378.
Marino, N.D.A.C., Romero, G.Q. & Farjalla, V.F. (2018) Geographical and experimental contexts modulate the effect of warming on top-down control: a meta-analysis. Ecology Letters, 21(3), 455-466.
McCann, K.S. (2000) The diversity-stability debate. Nature, 405(6783), 228-233.
Millennium Ecosystem Assessment (MEA) (2005) Ecosystems and Human Well-Being: Scenarios. Washington, DC: Island Press.
Mrowicki, R.J., O'Connor, N.E. & Donohue, I. (2016) Temporal variability of a single population can determine the vulnerability of communities to perturbations. Journal of Ecology, 104(3), 887-897.
O'Gorman, E.J. & Emmerson, M.C. (2009) Perturbations to trophic interactions and the stability of complex food webs. Proceedings of the National Academy of Sciences, 106(32), 13393-13398.
Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution and Systematics, 37, 637-669.
PBMC (2015) Executive summary: impact, vulnerability and adaptation to climate change. In: Assad, E.D. & Magalhães, A.R. (Eds.) Primeiro Relatório de Avaliação Nacional Sobre Mudanças Climáticas (RAN1) of the Painel Brasileiro de Mudanças Climáticas (PBMC). RJ, Brazil: COPPE, Rio de Janeiro, pp. 31.
Pennekamp, F., Pontarp, M., Tabi, A., Altermatt, F., Alther, R., Choffat, Y. et al. (2018) Biodiversity increases and decreases ecosystem stability. Nature, 563(7729), 109-112.
Petchey, O.L., McPhearson, P.T., Casey, T.M. & Morin, P.J. (1999) Environmental warming alters food-web structure and ecosystem function. Nature, 402(6757), 69-72.
Pimm, S.L. (1984) The complexity and stability of ecosystems. Nature, 307(5949), 321-326.
Pinheiro, J.C. & Bates, D.M. (2000) Mixed-effects Models in S and S-Plus. New York: Springer.
Piovia-Scott, J., Yang, L.H. & Wright, A.N. (2017) Temporal variation in trophic cascades. Annual Review of Ecology, Evolution, and Systematics, 48(1), 281-300. https://doi.org/10.1146/annurev-ecolsys-121415-032246.
Pires, A.P., Srivastava, D.S. & Farjalla, V.F. (2018) Is biodiversity able to buffer ecosystems from climate change? what we know and what we don’t. BioScience, 68(4), 273-280.
R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/. Last accessed Y X, 2017.
Romero, G.Q., Gonçalves-Souza, T., Kratina, P., Marino, N.A., Petry, W.K., Sobral-Souza, T. et al. (2018) Global predation pressure redistribution under future climate change. Nature Climate Change, 8(12), 1087-1091.
Romero, G.Q. & Srivastava, D.S. (2010) Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology, 79(5), 1122-1131.
Rosenblatt, A.E. & Schmitz, O.J. (2016) Climate change, nutrition, and bottom-up and top-down food web processes. Trends in Ecology & Evolution, 31(12), 965-975.
Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R. et al. (2000) Global biodiversity scenarios for the year 2100. Science, 287(5459), 1770-1774.
Soliveres, S., Van Der Plas, F., Manning, P., Prati, D., Gossner, M.M., Renner, S.C. et al. (2016) Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality. Nature, 536(7617), 456-459.
Thébault, E. & Loreau, M. (2005) Trophic interactions and the relationship between species diversity and ecosystem stability. The American Naturalist, 166(4), E95-E114.
Thibaut, L.M. & Connolly, S.R. (2013) Understanding diversity-stability relationships: towards a unified model of portfolio effects. Ecology Letters, 16(2), 140-150.
Tilman, D. (1999) The ecological consequences of changes in biodiversity: a search for general principles 101. Ecology, 80(5), 1455-1474.
Trzcinski, M.K., Srivastava, D.S., Corbara, B., Dézerald, O., Leroy, C., Carrias, J.-F. et al. (2016) The effects of food web structure on ecosystem function exceeds those of precipitation. Journal of Animal Ecology, 85(5), 1147-1160.
Utermöhl, H. (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen der Internationalen Vereinigung für theoretische und angewandte Limnologie, 9, 1-38.
Valone, T.J. & Hoffman, C.D. (2003) A mechanistic examination of diversity-stability relationships in annual plant communities. Oikos, 103(3), 519-527.
Voigt, W., Perner, J., Davis, A.J., Eggers, T., Schumacher, J., Bährmann, R. et al. (2003) Trophic levels are differentially sensitive to climate. Ecology, 84(9), 2444-2453.
Walther, G.R. (2010) Community and ecosystem responses to recent climate change. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365(1549), 2019-2024.
Xu, Q., Yang, X., Yan, Y., Wang, S., Loreau, M. & Jiang, L. (2021) Consistently positive effect of species diversity on ecosystem, but not population, temporal stability. Ecology Letters, 24(10), 2256-2266.
Yachi, S. & Loreau, M. (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proceedings of the National Academy of Sciences, 96(4), 1463-1468.
Yang, Z., Zhang, Q., Su, F., Zhang, C., Pu, Z., Xia, J. et al. (2016) Daytime warming lowers community temporal stability by reducing the abundance of dominant, stable species. Global Change Biology, 23(1), 154-163.
Yvon-Durocher, G., Allen, A.P., Cellamare, M., Dossena, M., Gaston, K.J., Leitao, M. et al. (2015) Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biology, 13(12), e1002324.
Yvon-Durocher, G., Montoya, J.M., Trimmer, M. & Woodward, G. (2011) Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems. Global Change Biology, 17(4), 1681-1694.
Zhao, Q., Van den Brink, P.J., Carpentier, C., Wang, Y.X.G., Rodríguez-Sánchez, P., Xu, C. et al. (2019) Horizontal and vertical diversity jointly shape food web stability against small and large perturbations. Ecology Letters, 22(7), 1152-1162.
Zuur, A.F., Ieno, E.N. & Elphick, C.S. (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution, 1(1), 3-14.

Auteurs

Felipe Rezende (F)

Programa de Pós-Graduação em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas-SP, Brazil.
Laboratório de Interações Multitróficas e Biodiversidade, Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas-SP, Brazil.

Pablo A P Antiqueira (PAP)

Laboratório de Interações Multitróficas e Biodiversidade, Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas-SP, Brazil.

Owen L Petchey (OL)

Institute for Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.

Luiz Felipe M Velho (LFM)

Universidade Estadual de Maringá (UEM), DBI/PEA/NUPÉLIA, Av. Colombo, Maringá-PR, Brazil.

Luzia C Rodrigues (LC)

Universidade Estadual de Maringá (UEM), DBI/PEA/NUPÉLIA, Av. Colombo, Maringá-PR, Brazil.

Gustavo Q Romero (GQ)

Laboratório de Interações Multitróficas e Biodiversidade, Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas-SP, Brazil.

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