Abstract
Climate change will alter the forces of predation and competition in temperate ectotherm food webs. This may increase local extinction rates, change the fate of invasions and impede species reintroductions into communities. Invasion success could be modulated by traits (e.g., defenses) and adaptations to climate. We studied how different temperatures affect the time until extinction of species, using bitrophic and tritrophic planktonic food webs to evaluate the relative importance of predatory overexploitation and competitive exclusion, at 15 and 25 °C. In addition, we tested how inclusion of a subtropical as opposed to a temperate strain in this model food web affects times until extinction. Further, we studied the invasion success of the temperate rotifer Brachionus calyciflorus into the planktonic food web at 15 and 25 °C on five consecutive introduction dates, during which the relative forces of predation and competition differed. A higher temperature dramatically shortened times until extinction of all herbivore species due to carnivorous overexploitation in tritrophic systems. Surprisingly, warming did not increase rates of competitive exclusion among the tested herbivore species in bitrophic communities. Including a subtropical herbivore strain reduced top-down control by the carnivore at high temperature. Invasion attempts of temperate B. calyciflorus into the food web always succeeded at 15 °C, but consistently failed at 25 °C due to voracious overexploitation by the carnivore. Pre-induction of defenses (spines) in B. calyciflorus before the invasion attempt did not change its invasion success at the high temperature. We conclude that high temperatures may promote local extinctions in temperate ectotherms and reduce their chances of successful recovery.
Similar content being viewed by others
References
Abrams PA, Vos M (2003) Adaptation, density dependence and the responses of trophic level abundances to mortality. Evol Ecol Res 5:1113–1132
Araujo MB, Ferri-Yanez F, Bozinovic F, Marquet PA, Valladares F, Chown SL (2013) Heat freezes niche evolution. Ecol Lett 16:1206–1219
Barton BT, Beckerman AP, Schmitz OJ (2009) Climate warming strengthens indirect interactions in an old-field food web. Ecology 90:2346–2351
Beisner BE, McCauley E, Wrona FJ (1996) Temperature-mediated dynamics of planktonic food chains: the effect of an invertebrate carnivore. Freshwater Biol 35:219–232
Beisner BE, McCauley E, Wrona FJ (1997a) The influence of temperature and food chain length on plankton predator-prey dynamics. Can J Fish Aquat Sci 54:586–595
Beisner BE, McCauley E, Wrona FJ (1997b) Predator-prey instability: individual-based mechanisms for population-level results. Funct Ecol 11:112–120
Binzer A, Guill C, Brose U, Rall BC (2012) The dynamics of food chains under climate change and nutrient enrichment. Phil Trans R Soc B 1605:2935–2944
Burgmer T, Hillebrand H, Pfenninger M (2007) Effects of climate-driven temperature changes on the diversity of freshwater macro invertebrates. Oecologia 151:93–100
Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, et al. (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105:6668–6672
Edwards M, Richardson AJ (2004) The impact of climate change on the phenology of the plankton community and trophic mismatch. Nature 430:881–884
Ewald NC, Hartley SE, Stewart AJA (2013) Climate change and trophic interactions in model temporary pond systems: the effect of high temperature on predation rate depend on prey size and density. Freshwater Biol 58:2481–2493
Gaedke U, Ruhenstroth-Bauer M, Wiegand I, Tirok K, Aberle N, Breitenhaupt P, Lengfellner K, Wohlers J, Sommer U, et al. (2010) Biotic interactions may overrule direct climate effects on spring phytoplankton dynamics. Glob Change Biol 16:1122–1136
Gilbert JJ (1967) Asplanchna and posterolateral spine induction in Brachionus calyciflorus. Hydrobiologia 64:1–62
Guillard RRL, Lorenzen CJ (1972) Yellow-green algae with chlorophyllide c. J Phycol 8:10–14
Halbach U (1970) Einfluß der temperatur auf die Populations Dynamik des planktischen Rädertieres Brachionus calyciflorus. Oecologia 4:176–207
Hansen J, Sato M, Ruedy R (2012) Perception of climate change. Proc Natl Acad Sci 109:14726–14727
Hoekman D (2010) Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects. Ecology 91:2819–2825
Holzapfel AM, Vinebrooke RD (2005) Environmental warming increases invasion potential of alpine lake communities by imported species. Glob Change Biol 11:2009–2015
Jankowski T, Livingstone DM (2006) Consequences of the 2003 European heat wave for lake temperature profiles, thermal stability, and hypolimnetic oxygen depletion: implications for a warmer world. Limnol Oceanogr 51:815–819
Jeppesen E, Meerhoff M, Jacobsen BA, Hansen RS, Søndergaard M, et al. (2007) Restoration of shallow lakes by nutrient control and biomanipulation—the successful strategy varies with lake size and climate. Hydrobiolobia 581:269–285
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Globak change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363
Kirk KL (1998) Enrichment can stabilize population dynamics: autotoxins and density dependence. Ecology 79:2456–2462
Kishi D, Murakami M, Nakano S, Maekawa K (2005) Water temperature determines strength of top-down control in a stream food web. Freshwater Biol 50:1315–1322
Kratina P, Greig HG, Thompson PL, Carvalho-Pereira TSA, Shurin JB (2012) Warming modifies trophic cascades and eutrophication in experimental freshwater communities. Ecology 93:1421–1430
Krenek S, Petzoldt T, Berendonk TU (2012) Coping with temperature at the warm edge—patterns of thermal adaption in the microbial eukaryote Paramecium caudatum. PLoS One 7:e30598
Logan JD, Wolesensky W (2007) Accounting for temperature in predator functional responses. Nat Resour Model 20:549–574
Lundberg P, Ranta E, Kaitala V (2000) Species loss leads to community closure. Ecol Lett 3:465–468
O’Gorman EJ, Pichler DE, Adams G, et al. (2012) Impacts of warming on the structure and functioning of aquatic communities: individual- to ecosystem-level responses. In: Woodward G, Jacob U, O’Gorman EJ (eds) Advances in ecological research: global change in multispecies systems, vol 47. Academic Press, New York, pp 81–176
Petchey OW, McPhearson PT, Casey TM, Morin PJ (1999) Environmental warming alters food web structure and ecosystem function. Nature 402:69–72
Pörtner HO, Farell AP (2008) Physiology and climate change. Science 322:690–692
Rall BC, Vucic-Pestic O, Ehnes RB, Emmerson M, Brose U (2010) Temperature, predator-prey interaction strength and population stability. Glob Change Biol 16:2145–2157
Richardson AJ, Schoeman DS (2004) Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305:1609–1612
Seifert LI, de Castro F, Marquart A, Gaedke U, Weithoff G, Vos M (2014) Heated relations: temperature-mediated shifts in consumption across trophic levels. PLoS One 9:e95046
Sentis A, Hemptinne JL, Brodeur J (2012) Using functional response modeling to investigate the effect of temperature on predator feeding rate and energetic efficiency. Oecologia 169:1117–1125
Sentis A, Hemptinne JL, Brodeur J (2013) Effects of simulated heat waves on an experimental plant–herbivore–predator food chain. Glob Change Biol 19:833–842
Shurin JB, Clasen JL, Greig HS, Kratina P, Thompson PL (2012) Warming shifts top-down and bottom-up control of pond food web structure and function. Phil Trans R Soc 367:3008–3017
Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci 99:15497–15500
Suikkanen S, Pulina S, Engstrom-Ost J, Lehtiniemi M, Lehtinen S, Brutemark A (2013) Climate change and eutrophication induced shifts in northern summer plankton communities. PLoS One 8:e66475
Texeirade Mello F, Meerhoff M, Pekcan-Hekim Z, Jeppesen E (2009) Substantial differences in littoral fish community structure and dynamics in subtropical and temperate shallow lakes. Freshwater Biol 54:1202–1215
Thompson PL, Shurin JB (2012) Regional zooplankton biodiversity provides limited buffering of pond ecosystems against climate change. J Anim Ecol 81:251–259
van der Stap I, Vos M, Mooji WM (2006) Linking herbivore-induced defences to populations dynamics. Freshwater Biol 51:424–434
van der Stap I, Vos M, Mooji WM (2007a) Inducible defenses and rotifer food chain dynamics. Hydrobiologia 593:103–110
van der Stap I, Vos M, Mooij WM (2007b) Induced defenses in herbivores and plants differentially modulate a trophic cascade. Ecology 88:2474–2481
van der Stap I, Vos M, Tollrian R, Mooij WM (2008) Inducible defenses, competition and shared predation in planktonic food chains. Oecologia 157:697–705
van der Stap I, Vos M, Kooi BW, Mulling BTM, van Donk E, Mooij WM (2009) Algal defenses, population stability and the risk of herbivore extinctions: a chemostat model and experiment. Ecol Res 24:1145–1153
Vandermeer J (2006) Oscillating populations and biodiversity maintenance. Bioscience 56:967–975
Vasseur DA, McCann KS (2005) A mechanistic approach for modeling temperature-dependent consumer-resource dynamics. Am Nat 166:184–198
Verschoor AM, Vos M, van der Stap I (2004) Inducible defenses prevent strong population fluctuations in bi- and tritrophic food chains. Ecol Lett 7:1143–1148
Vijverberg J, Vos M (2006) Predator-released compounds, ambient temperature and competitive exclusion among differently sized Daphnia species. Freshwater Biol 51:756–767
Vucic-Pestic O, Ehnes RB, Rall BC, Brose U (2011) Warming up the system: higher predator feeding rates but lower energetic efficiencies. Glob Change Biol 17:1301–1310
Weithoff G, Walz N (1995) Influence of the cyanobacterium Planktothrix agardhii on population growth and reproductive pattern of the rotifer Brachionus calyciflorus. Hydrobiologia 313(314):381–386
Wentz FJ, Gentemann C, Smith D, Chelton D (2000) Satellite measurements of sea surface temperature through clouds. Science 288:847–850
Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Global Change Biol 10:1844–1856
Woodward G, Perkins DM, Brown LE (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Phil Trans R Soc B 365:2093–2106
Acknowledgments
We thank Sabine Donath for help with the counting. We are grateful to the editor and reviewers for their comments that considerably improved the manuscript. This work was funded through Deutsche Forschungsgemeinschaft grant VO 1669/1-1 to M. V.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Scott D. Peacor.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Seifert, L.I., Weithoff, G., Gaedke, U. et al. Warming-induced changes in predation, extinction and invasion in an ectotherm food web. Oecologia 178, 485–496 (2015). https://doi.org/10.1007/s00442-014-3211-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-014-3211-4