Abstract
Despite the recent plethora of studies investigating biotic implications of climate change, most research has been undertaken without the need for change being quantified. Failure to link observed responses to selection pressure is a fundamental omission because whether change is appropriate cannot then be determined. We use almost 7,000 records to analyse long-term (1974–2004) changes in breeding phenology for six co-occurring woodland birds at a site with significantly increasing spring temperatures. We link observed change to changes in selection for early laying (calculated using differential breeding success as the season progresses) to determine whether change is: (1) necessary, (2) appropriate, and (3) sufficient. Three (resident) species—blue tit, great tit, and nuthatch—started clutches significantly earlier over time without selection for early laying becoming stronger over the same period. This suggests that observed advancements are appropriate, and sufficient, to track climate change. For another species—coal tit—there was no change in lay date, and although there was always selection to lay early, selection intensity did not change over time. For this, the earliest-laying species, bet-hedging to prevent maladaptation (laying too early) or stabilising selection may be acting to maintain phenological inertia, even when phenological change could be adaptive. For the final two (migratory) species—pied flycatcher and redstart—there was no temporal change in lay date, despite selection for early laying becoming significantly stronger over time. This study indicates that some species are tracking climate change successfully while ecologically-similar species, at the same study site, are failing to do so.
References
Ahola MP, Laaksonen T, Eeva T, Lehikoinen E (2009) Great tits lay increasingly smaller clutches than selected for: a study of climate- and density-related changes in reproductive traits. J Anim Ecol 78:1298–1306
Baillie SR, Marchant JH, Leech DI, Joys AC, Noble DG, Barimore C, Downie IS, Grantham MJ, Risely K, Robinson RA (2010) Breeding birds in the wider countryside: their conservation status 2009. BTO Research Report No 541, BTO, Thetford
Beebee TJC (1995) Amphibian breeding and climate. Nature 374:219–220
Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298
Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83
Buse A, Dury SJ, Woodburn RJW, Perrins CM, Good JEG (1999) Effects of elevated temperature on multi-species interactions: the case of pedunculate oak, winter moth and tits. Funct Ecol 13:74–82
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
Chmielewski FM, Rotzer T (2001) Response of tree phenology to climate change across Europe. Agric For Meteorol 108:101–112
Cresswell W, McCleery RH (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
Crick HQP, Sparks TH (1999) Climate change related to egg-laying trends. Nature 399:423–424
Crick HQP, Dudley C, Glue DE, Thomson DL (1997) UK birds are laying eggs earlier. Nature 388:526
DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81
Dunn PO, Winkler DW (1999) Climate change has affected the breeding date of tree swallows throughout North America. Proc R Soc B 266:2487–2490
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, London
Fontaine JJ, Decker KL, Skagen SK, van Riper C (2009) Spatial and temporal variation in climate change: a bird’s eye view. Clim Change 97:305–311
Goodenough AE (2008) Factors influencing nest-site choice and reproductive success in Cyanistes caeruleus (blue tit), Parus major (great tit) and Ficedula hypoleuca (pied flycatcher). PhD Thesis, University of Gloucestershire, UK
Goodenough AE, Elliot SL, Hart AG (2009) Annual variation in the relationship between lay date and clutch size in passerines. Acta Ornithol 44:27–36
Goodenough AE, Hart AG, Elliot SL (2010) What prevents phenological adjustment to climate change in migrant bird species? Evidence against the “arrival constraint” hypothesis. Int J Biometeorol. doi:10.1007/s00484-010-0312-6
Järvinen A (1991) A meta-analytic study of the effects of female age on laying-date and clutch-size in the great tit Parus major and the pied flycatcher Ficedula hypoleuca. Ibis 133:62–66
Lack DL (1966) Population studies of birds. Clarendon, London
Merilä J, Sheldon B, Kruuk LEB (2001) Explaining stasis: microevolutionary studies in natural populations. Genetica 112:199–222
Olofsson H, Ripa J, Jonzén N (2009) Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proc R Soc B 276:2963–29639
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669
Perrins CM (1970) The timing of birds’ breeding seasons. Ibis 112:242–255
Perrins CM (1991) Tits and their caterpillar food supply. Ibis 133:S49–S54
Perrins CM, McCleery RH (1989) Laying dates and clutch size in the great tit. Wilson Bull 101:236–253
Price T, Kirkpatrick M, Arnold SJ (1988) Directional selection and the evolution of breeding date in birds. Science 240:798–799
Sanz JJ, Potti J, Moreno J, Merino S, Frías O (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Glob Chang Biol 9:461–472
Slatkin M (1974) Hedging one’s evolutionary bets. Nature 250:704–705
Smallegange IM, Fiedler W, Köppen U, Geiter O, Bairlein F (2010) Tits on the move: exploring the impact of environmental change on blue tit and great tit migration distance. J Anim Ecol 79:350–357
Stenseth NC, Mysterud A (2002) Climate, changing phenology, and other life-history traits: non-linearity and match–mismatch to the environment. Proc Natl Acad Sci USA 99:13379–13381
Stevenson IR, Bryant DM (2000) Climate change and constraints on breeding. Nature 406:366–367
Strode PK (2003) Implications of climate change for North American wood warblers (Parulidae). Glob Chang Biol 9:1137–1144
Tryjanowski P, Kuzniak S, Sparks TH (2005) What affects the magnitude of change in first arrival dates of migrant birds? J Ornithol 146:200–205
van der Jeugd HP, McCleery R (2002) Effects of spatial autocorrelation, natal philopatry and phenotypic plasticity on the heritability of laying date. J Evol Biol 15:380–387
van Noordwijk AJ, McCleery RH, Perrins CM (1995) Selection for the timing of great tit breeding in relation to caterpillar growth and temperature. J Anim Ecol 64:451–458
Visser ME (2008) Keeping up with a warming world: assessing the rate of adaptation to climate change. Proc R Soc B 275:649–659
Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B 272:2561–2569
Visser ME, Holleman LJM, Caro SP (2009) Temperature has a causal effect on avian timing of reproduction. Proc R Soc B 276:2323–2331
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Goodenough, A.E., Hart, A.G. & Stafford, R. Is adjustment of breeding phenology keeping pace with the need for change? Linking observed response in woodland birds to changes in temperature and selection pressure. Climatic Change 102, 687–697 (2010). https://doi.org/10.1007/s10584-010-9932-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10584-010-9932-4