Does the temporal mismatch hypothesis match in boreal populations?

Abstract

The temporal mismatch hypothesis suggests that fitness is related to the degree of temporal synchrony between the energetic needs of the offspring and their food supply. The hypothesis has been a basis in studying the influence of climate warming on nature. This study enhances the knowledge on prevalence of temporal mismatches and their consequences in boreal populations, and questions the role of the temporal mismatch hypothesis as the principal explanation for the evolution of timing of breeding. To test this, we examined if synchrony with caterpillar prey or timing of breeding per se better explains reproductive output in North European parid populations. We compared responses of temperate-origin species, the great tit (Parus major) and the blue tit (Cyanistes caeruleus), and a boreal species, the willow tit (Poecile montanus). We found that phenologies of caterpillars and great tits, but not of blue tits, have advanced during the past decades. Phenologies correlated with spring temperatures that may function as cues about the timing of the food peak for great and blue tits. The breeding of great and blue tits and their caterpillar food remained synchronous. Synchrony explained breeding success better than timing of breeding alone. However, the synchrony effect arose only in certain conditions, such as with high caterpillar abundances or high breeding densities. Breeding before good synchrony seems advantageous at high latitudes, especially in the willow tit. Thus, the temporal mismatch hypothesis appears insufficient in explaining the evolution of timing of breeding.

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References

  1. Bartón K (2011) Multi-model inference R package version 1.0.0 http://cran.r-project.org/web/packages/MuMIn/index.html

  2. Bates D, Maechler M (2010) lme4: Linear mixed-effects models using S4 classes R package version 0.999375-37 http://cran.r-project.org/web/packages/lme4/index.html

  3. Bauer Z, Trnka M, Bauerová J, Možný M, Štĕpánek P, Bartošova L, Žalud Z (2010) Changing climate and the phenological response of great tit and collared flycatcher populations in floodplain forest ecosystems in Central Europe. Int J Biom 54:99–111

    Article  Google Scholar 

  4. Both C, van Asch M, Bijlsma RG, van den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Anim Ecol 78:73–83

    PubMed  Article  Google Scholar 

  5. Bourgault P, Thomas D, Perret P, Blondel J (2010) Spring vegetation phenology is a robust predictor of breeding date across broad landscapes: a multi-site approach using the Corsican blue tit (Cyanistes caeruleus). Oecologia 162:885–892

    PubMed  Article  Google Scholar 

  6. Bryant DM (1975) Breeding biology of house martins Delichon urbica in relation to aerial insect abundance. Ibis 117:180–216

    Article  Google Scholar 

  7. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  8. Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800–803

    PubMed  Article  CAS  Google Scholar 

  9. Costello JH, Sullivan BK, Gifford DJ (2006) A physical–biological interaction underlying variable phenological responses to climate change by coastal zooplankton. J Plank Res 28:1099–1105

    Article  Google Scholar 

  10. Cresswell W, McCleery R (2003) How great tits maintain synchronization of their hatch date with food supply in response to long-term variability in temperature. J Anim Ecol 72:356–366

    Article  Google Scholar 

  11. Dawson A (2008) Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Phil Trans R Soc B 363:1621–1633

    PubMed  Article  PubMed Central  Google Scholar 

  12. del Hoyo J, Elliott A, Christie D (2007) Handbook of the birds of the world, vol 12. Picathartes to tits and chickadees, Lynx Edicions

    Google Scholar 

  13. Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int J Biom 55:805–817

    Article  Google Scholar 

  14. Dunn P (2004) Breeding dates and reproductive performance. Adv Ecol Res 35:69–87

    Article  Google Scholar 

  15. Dunn PO, Winkler DW, Whittingham LA, Hannon SJ, Robertson RJ (2011) A test of the mismatch hypothesis: how is timing of reproduction related to food abundance in an aerial insectivore? Ecology 92:450–461

    PubMed  Article  Google Scholar 

  16. Durant JM, Hjerman DØ, 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 8:952–958

    Article  Google Scholar 

  17. Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283

    Article  Google Scholar 

  18. Eeva T, Veistola S, Lehikoinen E (2000) Timing of breeding in subarctic passerines in relation to food availability. Can J Zool 78:67–78

    Article  Google Scholar 

  19. Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711

    PubMed  Article  CAS  Google Scholar 

  20. Jonzén N, Hedenström A, Lundberg P (2007) Climate change and the optimal arrival of migratory birds. Proc R Soc Lond B 274:269–274

    Article  Google Scholar 

  21. Karvonen J, Orell M, Rytkönen S, Broggi J, Belda E (2012) Population dynamics of an expanding passerine at the distribution margin. J Avian Biol 43:102–108

    Article  Google Scholar 

  22. Kivelä SM, Välimäki P, Gotthard K (2013) Seasonality maintains alternative life-history phenotypes. Evolution 67:3145–3160

    PubMed  Article  Google Scholar 

  23. Kvist L, Ruokonen M, Lumme J, Orell M (1999) Different population structures in northern and southern populations of the European blue tit (Parus caeruleus). J Evol Biol 12:798–805

    Article  Google Scholar 

  24. Lack D (1950) The breeding seasons of European birds. Ibis 92:288–316

    Article  Google Scholar 

  25. Lahti K (1997) Social status and survival strategies in the Willow Tit Parus montanus PhD thesis, Department of Biology, University of Oulu, Oulu, Finland

  26. Lof ME, Reed TE, McNamara JM, Visser ME (2012) Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction. Proc R Soc Lond B 279:3161–3169

    Article  Google Scholar 

  27. Lyon BE, Chaine AS, Winkler DW (2008) A matter of timing Sci 321:1051–1052

    CAS  Google Scholar 

  28. Martin TE (1987) Food as a limit on breeding birds: a life-history perspective. Annu Rev Ecol Syst 18:453–487

    Article  Google Scholar 

  29. Matthysen E, Adriaensen F, Dhondt AA (2011) Multiple responses to increasing spring temperatures in the breeding cycle of blue and great tits (Cyanistes caeruleus, Parus major). Glob Change Biol 17:1–16

    Article  Google Scholar 

  30. Naef-Daenzer B, Keller LF (1999) The foraging performance of great and blue tits (Parus major and P. caeruleus) in relation to caterpillar development, and its consequences for nestling growth and fledging weight. J Anim Ecol 68:708–718

    Article  Google Scholar 

  31. Nager RG, van Noordwijk AJ (1992) Energetic limitation in the egg-laying period of great tits. Proc R Soc Lond B 249:259–263

    Article  Google Scholar 

  32. Nilsson J-Å, Källander H (2006) Leafing phenology and timing of egg laying in great tits Parus major and blue tits P. caeruleus. J Avian Biol 37:357–363

    Article  Google Scholar 

  33. Orell M, Ojanen M (1983a) Effect of habitat, date of laying and density on clutch size of the Great Tit Parus major in northern Finland. Holarctic Ecol 6:413–423

    Google Scholar 

  34. Orell M, Ojanen M (1983b) Breeding biology and population dynamics of the willow tit Parus montanus. Ann Zool Fenn 20:99–114

    Google Scholar 

  35. Orell M, Ojanen M (1983c) Timing and length of the breeding season of the great tit Parus major and the willow tit P. montanus near Oulu. North Finl Ardea 71:183–198

    Google Scholar 

  36. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  37. Perrins CM (1965) Population fluctuations and clutch-size in the Great Tit, Parus major L. J Anim Ecol 34:601–647

    Article  Google Scholar 

  38. Perrins CM (1991) Tits and their caterpillar food supply. Ibis 133(suppl. 1):49–54

    Google Scholar 

  39. R Development Core Team (2011) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  40. Reed TE, Jenouvrier S, Visser ME (2013) Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine. J Anim Ecol 82:131–144

    PubMed  Article  Google Scholar 

  41. Ruosteenoja K, Räisänen J, Pirinen P (2011) Projected changes in thermal seasons and the growing season in Finland. Int J Clim 31:1473–1487

    Article  Google Scholar 

  42. Rytkönen S, Krams I (2003) Does foraging behaviour explain the poor breeding success of great tits Parus major in northern Europe? J Avian Biol 34:288–297

    Article  Google Scholar 

  43. Rytkönen S, Orell M (2001) Great tits, Parus major, lay too many eggs: experimental evidence in mid-boreal habitats. Oikos 93:439–450

    Article  Google Scholar 

  44. Rytkönen S, Koivula K, Orell M (1996) Patterns of per-brood and per-offspring provisioning efforts in the Willow Tit Parus montanus. J Avian Biol 27:21–30

    Article  Google Scholar 

  45. Silverin B, Wingfield J, Stokkan K-A, Massa R, Järvinen A, Andersson N-Å, Lambrechts M, Sorace A, Blomqvist D (2008) Ambient temperature effects on photo induced gonadal cycles and hormonal secretion patterns in Great Tits from three different breeding latitudes. Horm Behav 54:60–68

    PubMed  Article  CAS  Google Scholar 

  46. Stevenson IR, Bryant DM (2000) Climate change and constraints on breeding. Nature 406:366–367

    PubMed  Article  CAS  Google Scholar 

  47. Svensson L (1992) Identification guide to european passerines, 4th edn. British Trust for Ornithology

  48. Thackeray SJ, Sparks TH, Frederiksen M, Burthe S, Bacon PJ, Bell JR, Botham MS, Brereton TM, Bright PW, Carvalho L, Clutton-Brock T, Dawson A, Edwards M, Elliott JM, Harrington R, Johns D, Jones ID, Jones JT, Leech DI, Roy DB, Scott WA, Smith M, Smithers RJ, Winfield IJ, Wanless S (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313

    Article  Google Scholar 

  49. Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600

    PubMed  Article  CAS  Google Scholar 

  50. Thomas DW, Bourgault P, Shipley B, Perret P, Blondel J (2010) Context-dependent changes in the weighting of environmental cues that initiate breeding in a temperate passerine, the Corsican blue tit (Cyanistes caeruleus). Auk 127:129–139

    Article  Google Scholar 

  51. Väisänen RA, Lammi E, Koskimies P (1998) Distribution, numbers and population changes of Finnish breeding birds. Otava, Helsinki

  52. van Balen JH (1973) A comparative study of the breeding ecology of the great tit Parus major in different habitats. Ardea 61:1–93

    Google Scholar 

  53. Vatka E, Orell M, Rytkönen S (2011) Warming climate advances breeding and improves synchrony of food demand and food availability in a boreal passerine. Glob Change Biol 17:3002–3009

    Article  Google Scholar 

  54. Visser ME, Holleman LJM (2001) Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc R Soc Lond B 268:289–294

    Article  CAS  Google Scholar 

  55. Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Lond B 265:1867–1870

    Article  Google Scholar 

  56. Visser ME, Adriaensen F, van Balen JH, Blondel J, Dhondt AA, van Dongen S, du Feu C, Ivankina EV, Kerimov AB, de Laet J, Matthysen E, McCleery R, Orell M, Thomson DL (2003) Variable responses to large-scale climate change in European Parus populations. Proc R Soc Lond B 270:367–372

    Article  Google Scholar 

  57. Visser ME, Both C, Lambrechts MM (2004) Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35:89–110

    Article  Google Scholar 

  58. Visser ME, Holleman LJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147:164–172

    PubMed  Article  Google Scholar 

  59. Visser ME, Holleman LJM, Caro SP (2009) Temperature has a causal effect on avian timing of reproduction. Proc R Soc Lond B 276:2323–2331

    Article  Google Scholar 

  60. Visser ME, te Marvelde L, Lof ME (2012) Adaptive phenological mismatches of birds and their food in a warming world. J Ornithol 153:S75–S84

    Article  Google Scholar 

  61. Zandt HS (1994) A comparison of three sampling techniques to estimate the population size of caterpillars in trees. Oecologia 97:399–406

    Google Scholar 

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Acknowledgments

We acknowledge all the people who took part in the data collection, especially staff of the Zoological Museum and Experimental Zoo of the University of Oulu, M Ojanen, P Kärkkäinen, N Verboven, M Leppäjärvi, J Broggi, E Belda, J Karvonen and J Ollinmäki. We thank ME Visser, P Dunn, V-M Pakanen and P Välimäki for commenting the manuscript. The study was funded by the Academy of Finland, Research Council for Biosciences and Environment (project number 128193) and Thule Institute of the University of Oulu.

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Correspondence to Emma Vatka.

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Communicated by Ola Olsson.

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Vatka, E., Rytkönen, S. & Orell, M. Does the temporal mismatch hypothesis match in boreal populations?. Oecologia 176, 595–605 (2014). https://doi.org/10.1007/s00442-014-3022-7

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Keywords

  • Caterpillar peak
  • Fecundity
  • Phenological shifts
  • Timing-related constraints
  • Time-series data