Advertisement

Theoretical Ecology

, Volume 7, Issue 2, pp 149–162 | Cite as

(A bit) Earlier or later is always better: Phenological shifts in consumer–resource interactions

  • Tomás A. Revilla
  • Francisco Encinas-Viso
  • Michel Loreau
ORIGINAL PAPER

Abstract

Phenology is a crucial life history trait for species interactions and it can have great repercussions on the persistence of communities and ecosystems. Changes in phenology caused by climate change can disrupt species interactions causing decreases in consumer growth rates, as suggested by the match–mismatch hypothesis (MMH). However, it is still not clear what the long-term consequences of such phenological changes are. In this paper, we present models in which phenology and consumer–resource feedbacks determine long-term community dynamics. Our results show that consumer viability is constrained by limits in the amount of phenological mismatch with their resources, in accordance with the MMH, but the effects of phenological shifts are often nonmonotonic. Consumers generally have higher abundances when they recruit some time before or after their resources because this reduces the long-term effects of overexploitation that would otherwise occur under closer synchrony. Changes in the duration of recruitment phenologies also have important impacts on community stability, with shorter phenologies promoting oscillations and cycles. For small community modules, the effects of phenological shifts on populations can be explained, to a great extent, as superpositions of their effects on consumer–resource pairs. We highlight that consumer–resource feedbacks and overexploitation, which are not typically considered in phenological models, are important factors shaping the long-term responses to phenological changes caused by climate change.

Keywords

Phenology Trophic interactions Recruitment Overexploitation Climate change Match–mismatch hypothesis 

Notes

Acknowledgments

We thank Dorixa Monsalve, Harold Perez de Vladar, and Jarad Mellard for comments of earlier versions of this paper. We also thank two anonymous reviewers for comments and criticisms that greatly improved this paper. TAR and ML thank the support by the TULIP Laboratory of Excellence (ANR-10-LABX-41).

Supplementary material

12080_2013_207_MOESM1_ESM.pdf (1.9 mb)
(PDF 1.88 MB)

References

  1. Aberle N, Bauer B, Lewandowska A, Gaedke U, Sommer U (2012) Warming induces shifts in microzooplankton phenology and reduces time-lags between phytoplankton and protozoan production. Mar Biol 159(11):2441–2453CrossRefGoogle Scholar
  2. Abrams PA (2004) When does periodic variation in resource growth allow robust coexistence of competing consumer species? Ecology 85:372–382CrossRefGoogle Scholar
  3. Altermatt F (2009) Climatic warming increases voltinism in European butterflies and moths. Proc R Soc B Biol Sci 277(1685):1281–1287CrossRefGoogle Scholar
  4. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441(7089):81–83PubMedCrossRefGoogle Scholar
  5. Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293CrossRefGoogle Scholar
  6. Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int J Biometeorol 55:805–817PubMedCrossRefGoogle Scholar
  7. Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73(1):69–86CrossRefGoogle Scholar
  8. Durant JM, Hjermann D, Anker-Nilssen T, Beaugrand G, Mysterud A, Pettorelli N, Stenseth NC (2005) Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol Lett 8(9):952–958CrossRefGoogle Scholar
  9. Durant JM, Hjermann DO, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33(3):271–283CrossRefGoogle Scholar
  10. Durant JM, Hjermann DO, Falkenhaug T, Gifford DJ, Naustvoll L-J, Sullivan G, Beaugrand BK, Stenseth NC (2013) Extension of the match–mismatch hypothesis to predator-controlled systems. Mar Ecol Prog Ser 474:43–52CrossRefGoogle Scholar
  11. Ebenhöh W (1992) Temporal organization in a multi-species model. Theor Popul Biol 42:152–171CrossRefGoogle Scholar
  12. Encinas-Viso F, Revilla TA, Etienne RS (2012) Phenology drives mutualistic network structure and diversity. Ecol Lett 15(3):198–208PubMedCrossRefGoogle Scholar
  13. Fleming TH, Partridge BL (1984) On the analysis of phenological overlap. Oecologia 62(3):344–350CrossRefGoogle Scholar
  14. Gause GF (1934) The struggle for existence. Williams & Wilkins, Baltimore, MDCrossRefGoogle Scholar
  15. Gilman RT, Fabina NS, Abbott KC, Rafferty NE (2012) Evolution of plant-pollinator mutualisms in response to climate change. Evol Appl 5(1):2–16PubMedCentralCrossRefGoogle Scholar
  16. Hastings A, Powell T (1991) Chaos in a three-species food chain. Ecology 72(3):896–903CrossRefGoogle Scholar
  17. Holt RD (1997) Community modules. In: Gange AC, Brown VK (eds) 36th symposium of the British ecological society, multitrophic interactions in terrestrial ecosystems. Blackwell Science, pp 333–349Google Scholar
  18. Huffaker CB (1958) Experimental studies on predation: dispersion factors and predator–prey oscillations. Hilgardia 27:795–835Google Scholar
  19. Johansson J, Jonzén N (2012) Game theory sheds new light on ecological responses to current climate change when phenology is historically mismatched. Ecol Lett 15(8):881–888PubMedCrossRefGoogle Scholar
  20. Kallimanis AS, Petanidou T, Tzanopoulos J, Pantis JD, Sgardelis SP (2009) Do plant-pollinator interaction networks result from stochastic processes. Ecol Model 220:684–693CrossRefGoogle Scholar
  21. Kerby JT, Wilmers CC, Post E (2012) Climate change, phenology and the nature of consumer–resource interactions: advancing the match/mismatch hypothesis. In: Ohgushi T, Schmitz OJ, Holt RD (eds) Trait-mediated indirect interactions: ecological and evolutionary perspectives. Cambridge University Press, pp 508–525Google Scholar
  22. Kristiansen T, Drinkwater KF, Lough RG, Sundby S (2011) Recruitment variability in North Atlantic cod and match–mismatch dynamics. PLoS ONE 6(3):e17456PubMedCentralPubMedCrossRefGoogle Scholar
  23. Lawler SP, Morin PJ (1993) Temporal overlap, competition, and priority effects in larval anurans. Ecology 74(1):174–182CrossRefGoogle Scholar
  24. Loreau M (1989) Coexistence of temporally segregated competitors in a cyclic environment. Theor Popul Biol 36(2):181–201CrossRefGoogle Scholar
  25. Loreau M (1992) Time scale of resource dynamics and coexistence through time partitioning. Theor Popul Biol 41(3):401–412CrossRefGoogle Scholar
  26. Luckinbill LS (1973) Coexistence in laboratory populations of Paramecium aurelia and its predator Didinium nasutum. Ecology 54(6):1320–1327CrossRefGoogle Scholar
  27. May RM (1974) Stability and complexity in model ecosystems. Princeton landmarks in biology. Princeton University Press, PrincetonGoogle Scholar
  28. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10(8):710–717PubMedCrossRefGoogle Scholar
  29. Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Phil Trans R Soc B Biol Sci 365(1555):3177–3186CrossRefGoogle Scholar
  30. Morin PJ (1987) Predation, breeding asynchrony, and the outcome of competition among treefrog tadpoles. Ecology 68(3):675– 683CrossRefGoogle Scholar
  31. Morin PJ (1999) Productivity, intraguild predation, and population dynamics in experimental food webs. Ecology 80:752–760CrossRefGoogle Scholar
  32. Murdoch WW, Briggs CJ, Nisbet RM (2003) Consumer–resource dynamics. Number 36 in monographs in population biology. Princeton University Press, PrincetonGoogle Scholar
  33. Nakazawa T, Doi H (2012) A perspective on match/mismatch of phenology in community contexts. Oikos 121(4):489–495CrossRefGoogle Scholar
  34. Namba T (1984) Competitive co-existence in a seasonally fluctuating environment. J Theor Biol 111(2):369–386CrossRefGoogle Scholar
  35. Olesen JM, Bascompte J, Dupont YL, Elberling H, Rasmussen C, Jordano P (2011) Missing and forbidden links in mutualistic networks. Proc R Soc B Biol Sci 278(1706):725–732CrossRefGoogle Scholar
  36. Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466(7305):482–485PubMedCrossRefGoogle Scholar
  37. Pachepsky E, Nisbet RM, Murdoch WW (2008) Between discrete and continuous: consumer–resource dynamics with synchronized reproduction. Ecology 89:280–288PubMedCrossRefGoogle Scholar
  38. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Ann Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  39. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Chang Biol 13(9):1860–1872CrossRefGoogle Scholar
  40. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42PubMedCrossRefGoogle Scholar
  41. Revilla TA (2000) Resource competition in stage-structured populations. J Theor Biol 204:289–298PubMedCrossRefGoogle Scholar
  42. Rivero A, Casas J (1999) Rate of nutrient allocation to egg production in a parasitic wasp. Proc R Soc Lond B 266(1424):1169–1174CrossRefGoogle Scholar
  43. Rockwell RF, Gormezano LJ, Koons DN (2011) Trophic matches and mismatches: can polar bears reduce the abundance of nesting snow geese in Western Hudson Bay. Oikos 120(5):696–709CrossRefGoogle Scholar
  44. Russell FL, Louda SM (2004) Phenological synchrony affects interaction strength of an exotic weevil with platte thistle, a native host plant. Oecologia 139(4):525–534CrossRefGoogle Scholar
  45. Salinger MJ (2005) Climate variability and change: past, present and future–an overview. Clim Chang 70(1):9–29CrossRefGoogle Scholar
  46. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39PubMedCrossRefGoogle Scholar
  47. Wheeler D (1996) The role of nourishment in oogenesis. Ann Rev Entomol 41(1):407–431CrossRefGoogle Scholar
  48. Wilbur HM (1997) Experimental ecology of food webs: complex systems in temporary ponds. Ecology 78:2279–2302CrossRefGoogle Scholar
  49. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13(1):1–10PubMedCrossRefGoogle Scholar
  50. Zonneveld C (1992) Polyandry and protandry in butterflies. Bull Math Biol 54(6):957–976CrossRefGoogle Scholar
  51. Zonneveld C, Metz JAJ (1991) Models on butterfly protandry: virgin females are at risk to die. Theor Popul Biol 40(3):308–321PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Tomás A. Revilla
    • 1
  • Francisco Encinas-Viso
    • 2
    • 3
  • Michel Loreau
    • 1
  1. 1.Centre for Biodiversity Theory and ModellingStation d’Ecologie Expérimentale du CNRSMoulisFrance
  2. 2.CSIRO Plant IndustryCanberraAustralia
  3. 3.Community and Conservation EcologyUniversity of GroningenGroningenthe Netherlands

Personalised recommendations