Persistence and extinction dynamics driven by the rate of environmental change in a predator–prey metacommunity

Abstract

Persistence of ecological systems under climate change depends on how fast the environment is changing and on how species respond to that change. The rate of environmental change is a key factor affecting the responses. Adaptation, migration to more favorable habitats, and extinction are fundamental responses that species exhibit to climate change, but extinction is the most extreme one when species are unable to keep pace with climate change. The dynamics of extinction has long been addressed by theories of stochasticity, alternate states, and tipping points. But we are still lacking a non-equilibrium theory that explains how the rate of environmental change affects species responses, especially persistence. Here, we present spatial and non-spatial models of prey–predator interactions with Allee effect and show diverse responses characterized by different rates of environmental change. We show a community collapse to increasing rates of environmental change and also a stabilizing mechanism through unstable states of the non-spatial model. On the other hand, the spatially distributed community through dispersal exhibits multiple responses that include rescue effect, rate-driven extinction, and unexpected critical transitions and regime shifts. Furthermore, our results show a tracking of unstable states describing the role of unstable states in extinction debt and in maintaining spatial heterogeneity. Thus, this study reveals how the rate of environmental change reshapes community responses and predicts community persistence away from equilibrium states and also away from critical points.

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References

  1. Adler PB, Drake JM (2008) Environmental variation, stochastic extinction, and competitive coexistence. The American Naturalist 172(5):E186–E195. https://doi.org/10.1086/591678

    Article  Google Scholar 

  2. Amarasekare P (1998a) Allee effects in metapopulation dynamics. The American Naturalist 152 (2):298–302. https://doi.org/10.1086/286169

    CAS  Article  PubMed  Google Scholar 

  3. Amarasekare P (1998b) Interactions between local dynamics and dispersal: insights from single species models. Theor Popul Biol 53(1):44–59. https://doi.org/10.1006/tpbi.1997.1340

    CAS  Article  PubMed  Google Scholar 

  4. Amarasekare P (2008) Spatial dynamics of foodwebs. Annual Review of Ecology, Evolution, and Systematics 39(1):479–500. https://doi.org/10.1146/annurev.ecolsys.39.110707.173434

    Article  Google Scholar 

  5. Antonovics J, McKane AJ, Newman TJ (2006) Spatiotemporal dynamics in marginal populations. The American Naturalist 167(1):16–27. https://doi.org/10.1086/498539

    CAS  Article  PubMed  Google Scholar 

  6. Arumugam R, Lutscher F, Guichard F (2020) Tracking unstable states: ecosystem dynamics in a changing world. (submitted)

  7. Ashwin P, Wieczorek S, Vitolo R, Cox P (2012) Tipping points in open systems: bifurcation, noise-induced and rate-dependent examples in the climate system. Philosophical Transactions: Mathematical, Phys Eng Sci 370(1962):1166–1184

    Article  Google Scholar 

  8. Bell G, Gonzalez A (2009) Evolutionary rescue can prevent extinction following environmental change. Ecol Lett 12(9):942–948. https://doi.org/10.1111/j.1461-0248.2009.01350.x

    Article  PubMed  Google Scholar 

  9. Berec L, Angulo E, Courchamp F (2007) Multiple Allee effects and population management. Trends in Ecology & Evolution 22(4):185–191

    Article  Google Scholar 

  10. Berg MP, Kiers ET, Driessen G, Van Der Heijden M, Kooi BW, Kuenen F, Liefting M, Verhoef HA, Ellers J (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Chang Biol 16(2):587–598. https://doi.org/10.1111/j.1365-2486.2009.02014.x

    Article  Google Scholar 

  11. Biggs R, Carpenter SR, Brock WA (2009) Turning back from the brink: detecting an impending regime shift in time to avert it. Proceedings of the National Academy of Sciences 106(3):826–831. https://doi.org/10.1073/pnas.0811729106

    Article  Google Scholar 

  12. Briggs CJ, Hoopes MF (2004) Stabilizing effects in spatial parasitoid–host and predator–prey models: a review. Theoretical Population Biology 65(3):299–315. https://doi.org/10.1016/j.tpb.2003.11.001

    Article  PubMed  Google Scholar 

  13. Carlson SM, Cunningham CJ, Westley PA (2014) Evolutionary rescue in a changing world. Trends in Ecology & Evolution 29(9):521–530. https://doi.org/10.1016/j.tree.2014.06.005

    Article  Google Scholar 

  14. Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333(6045):1024–1026. https://doi.org/10.1126/science.1206432

    CAS  Article  PubMed  Google Scholar 

  15. Clements CF, Ozgul A (2016) Rate of forcing and the forecastability of critical transitions. Ecology and Evolution 6(21):7787–7793. https://doi.org/10.1002/ece3.2531

    Article  PubMed  PubMed Central  Google Scholar 

  16. Courchamp F, Berec L, Gascoigne J (2008) Allee effects in ecology and conservation. Oxford University Press, Oxford

    Google Scholar 

  17. Cuddington KM, Yodzis P (1999) Black noise and population persistence. Proceedings of the Royal Society of London Series B:, Biological Sciences 266(1422):969–973. https://doi.org/10.1098/rspb.1999.0731

    Article  Google Scholar 

  18. DeAngelis DL, Waterhouse JC (1987) Equilibrium and nonequilibrium concepts in ecological models. Ecol Monogr 57(1):1–21. https://doi.org/10.2307/1942636

    Article  Google Scholar 

  19. Eriksson A, Elías-wolff F, Mehlig B, Manica A (2014) The emergence of the rescue effect from explicit within- and between-patch dynamics in a metapopulation. Proceedings of the Royal Society B:, Biological Sciences 281(1780):20133,127. https://doi.org/10.1098/rspb.2013.3127

    Article  Google Scholar 

  20. Gotelli NJ (1991) Metapopulation models: the rescue effect, the propagule rain, and the core-satellite hypothesis. The American Naturalist 138(3):768–776. https://doi.org/10.1086/285249

    Article  Google Scholar 

  21. Hanski I (1998) Metapopulation dynamics. Nature 396(6706):41–49. https://doi.org/10.1038/23876

    CAS  Article  Google Scholar 

  22. Hastings A (2001) Transient dynamics and persistence of ecological systems. Ecol Lett 4(3):215–220. https://doi.org/10.1046/j.1461-0248.2001.00220.x

    Article  Google Scholar 

  23. Hastings A, Abbott KC, Cuddington K, Francis T, Gellner G, Lai YC et al (2018) Transient phenomena in ecology. Science 361(6406):eaat6412. https://doi.org/10.1126/science.aat6412

    Article  Google Scholar 

  24. Holt RD, Knight TM, Barfield M (2004) Allee effects, immigration, and the evolution of species’ niches. The American Naturalist 163(2):253–262. https://doi.org/10.1086/381408

    Article  PubMed  Google Scholar 

  25. Hufbauer RA, Szűcs M, Kasyon E, Youngberg C, Koontz MJ, Richards C, Tuff T, Melbourne BA (2015) Three types of rescue can avert extinction in a changing environment. Proceedings of the National Academy of Sciences 112(33):10 562:557–10. https://doi.org/10.1073/pnas.1504732112

    CAS  Article  Google Scholar 

  26. Hughes TP, Linares C, Dakos V, van de Leemput IA, van Nes EH (2013) Living dangerously on borrowed time during slow, unrecognized regime shifts. Trends in Ecology & Evolution 28(3):149–155. https://doi.org/10.1016/j.tree.2012.08.022

    Article  Google Scholar 

  27. Jackson ST, Sax DF (2010) Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends in Ecology & Evolution 25(3):153–160

    Article  Google Scholar 

  28. Keitt TH, Lewis MA, Holt RD (2001) Allee effects, invasion pinning, and species’ borders. The American Naturalist 157(2):203–216. https://doi.org/10.1086/318633

    CAS  Article  PubMed  Google Scholar 

  29. Kot M (2001) Elements of mathematical ecology. Cambridge University Press, Cambridge

    Google Scholar 

  30. Kramer AM, Dennis B, Liebhold AM, Drake JM (2009) The evidence for Allee effects. Popul Ecol 51(3):341–354

    Article  Google Scholar 

  31. Kuussaari M, Bommarco R, Heikkinen RK, Helm A, Krauss J, Lindborg R, Öckinger E, Pärtel M, Pino J, Roda F et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends in Ecology & Evolution 24(10):564–571. https://doi.org/10.1016/j.tree.2009.04.011

    Article  Google Scholar 

  32. Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist 142(6):911–927

    Article  Google Scholar 

  33. Lenton TM (2011) Early warning of climate tipping points. Nat Clim Chang 1(4):201–209. https://doi.org/10.1038/nclimate1143

    Article  Google Scholar 

  34. Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454(7200):100–103. https://doi.org/10.1038/nature06922

    CAS  Article  PubMed  Google Scholar 

  35. Mori AS (2011) Ecosystem management based on natural disturbances: hierarchical context and non-equilibrium paradigm. J Appl Ecol 48(2):280–292. https://doi.org/10.1111/j.1365-2664.2010.01956.x

    Article  Google Scholar 

  36. Morozov A, Abbott K, Cuddington K, Francis T, Gellner G, Hastings A, Lai YC, Petrovskii S, Scranton K, Zeeman ML (2019) Long transients in ecology: theory and applications. Physics of Life Reviews https://doi.org/10.1016/j.plrev.2019.09.004

  37. O’Keeffe PE, Wieczorek S (eds.) (2019) Tipping phenomena and points of no return in ecosystems: beyond classical bifurcations. arXiv:190201796

  38. Ovaskainen O, Meerson B (2010) Stochastic models of population extinction. Trends in Ecology & Evolution 25(11):643–652. https://doi.org/10.1016/j.tree.2010.07.009

    Article  Google Scholar 

  39. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37(1):637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100

    Article  Google Scholar 

  40. Phillips JD (2004) Divergence, sensitivity, and nonequilibrium in ecosystems. Geogr Anal 36 (4):369–383. https://doi.org/10.1111/j.1538-4632.2004.tb01142.x

    Article  Google Scholar 

  41. Post E (2013) Ecology of climate change: the importance of biotic interactions monographs in population biology. Princeton University Press, Princeton

    Google Scholar 

  42. Pöyry J, Luoto M, Heikkinen RK, Kuussaari M, Saarinen K (2009) Species traits explain recent range shifts of Finnish butterflies. Glob Chang Biol 15(3):732–743. https://doi.org/10.1111/j.1365-2486.2008.01789.x

    Article  Google Scholar 

  43. Reed TE, Schindler DE, Waples RS (2011) Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conserv Biol 25(1):56–63. https://doi.org/10.1111/j.1523-1739.2010.01552.x

    Article  PubMed  PubMed Central  Google Scholar 

  44. Rietkerk M, Dekker SC, de Ruiter PC, van de Koppel J (2004) Self-organized patchiness and catastrophic shifts in ecosystems. Science 305(5692):1926–1929. https://doi.org/10.1126/science.1101867

    CAS  Article  PubMed  Google Scholar 

  45. Scheffer M (2009) Critical transitions in nature and society. Princeton Studies in Complexity, Princeton University Press, Princeton

    Google Scholar 

  46. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413(6856):591–596. https://doi.org/10.1038/35098000

    CAS  Article  PubMed  Google Scholar 

  47. Scheffer M, Bascompte J, Brock WA, Brovkin V, Carpenter SR, Dakos V et al (2009) Early-warning signals for critical transitions. Nature 461(7260):53–59. https://doi.org/10.1038/nature08227

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Scheffer M, Carpenter SR, Lenton TM, Bascompte J, Brock W, Dakos V et al (2012) Anticipating critical transitions. Science 338(6105):344–348. https://doi.org/10.1126/science.1225244

    CAS  Article  PubMed  Google Scholar 

  49. Siteur K, Eppinga MB, Doelman A, Siero E, Rietkerk M (2016) Ecosystems off track: rate-induced critical transitions in ecological models. Oikos 125(12):1689–1699. https://doi.org/10.1111/oik.03112

    Article  Google Scholar 

  50. Stephens PA, Sutherland WJ (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends in Ecology & Evolution 14(10):401–405

    CAS  Article  Google Scholar 

  51. Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371(6492):65–66. https://doi.org/10.1038/371065a0

    Article  Google Scholar 

  52. Walther G, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC et al (2002) Ecological responses to recent climate change. Nature 416(6879):389–395. https://doi.org/10.1038/416389a

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

We thank the reviewers for the valuable suggestions.

Funding

RA received partial funding from the Centre for Applied Mathematics in Bioscience and Medicine (CAMBAM) to the postdoctoral research. FG received funding from the Natural Sciences and Engineering Research Council of Canada for funding through the Discovery Grant program (RGPIN-2017-04266) and Discovery Accelerator Supplement (RGPAS-2017-507832). FL received funding from the Natural Sciences and Engineering Research Council of Canada for funding through the Discovery Grant program (RGPIN-2016-04795) and for a Discovery Accelerator Supplement (RGPAS-2016-492872).

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Correspondence to Ramesh Arumugam.

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Arumugam, R., Guichard, F. & Lutscher, F. Persistence and extinction dynamics driven by the rate of environmental change in a predator–prey metacommunity. Theor Ecol (2020). https://doi.org/10.1007/s12080-020-00473-8

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Keywords

  • Rate of environmental change
  • Community rescue
  • Extinction dynamics
  • Critical transitions
  • Regime shifts
  • Extinction debt
  • Tracking unstable states