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Reduced compensatory growth capacity in mistimed broods of a migratory passerine

  • Global change ecology - Original research
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Abstract

Phenotypic plasticity has recently been proposed to increase population viability when rapid anthropogenic environmental changes cannot be tracked by means of evolution. This assumes that environmental changes do not constrain phenotypic plasticity itself, which has rarely been examined in natural populations. In areas of climate warming, many long-distance migratory birds breed increasingly late relative to the period of peak food supply, and the temporal mismatch may constrain plastic life-history traits such as nestling growth. We combined 23 years of food availability and breeding data with a 3-year experimental manipulation of nestling growth trajectories in a Central European population of collared flycatchers (Ficedula albicollis) to examine the potential impact of climate-related mistimed breeding on nestling developmental plasticity. Timing of the food peak was predicted by winter climate, and the median hatching date of broods was earlier in springs with earlier food peaks. However, the adjustment of hatching date was incomplete and the population largely missed the food peak in years with very early food peaks. After imposing a temporary, experimental food shortage on nestlings, the extent of compensatory growth in body mass differed among years, and this difference was apparently related to the distance of hatching dates from the yearly food peak. Growth compensation declined with distance from the peak. These results suggest that mistimed phenology may not only create permanently adverse conditions for migratory species but it may also constrain the plastic responses of individuals to temporary disturbances. Therefore, climate change may not only favour but also restrict phenotypic plasticity.

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References

  • Arlettaz R, Schaad M, Reichlin TS, Schaub M (2010) Impact of weather and climate variation on hoopoe reproductive ecology and population growth. J Ornithol 151:889–899

    Article  Google Scholar 

  • Avery MI, Krebs JR (1984) Temperature and foraging success of great tits Parus major hunting for spiders. Ibis 126:33–38

    Article  Google Scholar 

  • Balbontin J, Møller AP, Hermosell IG, Marzal A, Reviriego M, de Lope F (2009) Individual responses in spring arrival date to ecological conditions during winter and migration in a migratory bird. J Anim Ecol 78:981–989

    Article  PubMed  Google Scholar 

  • Beldade P, Mateus ARA, Keller RA (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20:1347–1363

    Article  PubMed  Google Scholar 

  • Bize P, Roulin A, Bersier LF, Pflüger D, Richner H (2003) Parasitism and developmental plasticity in Alpine swift nestlings. J Anim Ecol 72:633–639

    Article  Google Scholar 

  • Blondel J, Maistre M, Perret P, Hurtrez-Boussés S, Lambrechts MM (1998) Is the small clutch size of a Corsican blue tit population optimal? Oecologia 117:80–89

    Article  Google Scholar 

  • Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20:243–248

    Article  PubMed  CAS  Google Scholar 

  • Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298

    Article  PubMed  CAS  Google Scholar 

  • Both C, Visser ME, Verboven N (1999) Density-dependent recruitment rates in great tits: the importance of being heavier. Proc R Soc Lond B 266:465–469

    Article  Google Scholar 

  • Both C, Artemyev AV, Blaauw B, Cowie RJ, Dekhuijzen AJ, Eeva T, Enemar A, Gustafsson L, Ivankina EV, Järvinen A, Metcalfe NB, Nyholm NEI, Potti J, Ravussin PA, Sanz JJ, Silverin B, Slater FM, Sokolov LV, Török J, Winkel W, Wright J, Zang H, Visser ME (2004) Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proc R Soc Lond B 271:1657–1662

    Article  Google Scholar 

  • Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83

    Article  PubMed  CAS  Google Scholar 

  • Both C, van Turnhout CAM, Bijlsma RG, Siepel H, van Strien AJ, Foppen RPB (2010) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc Lond B 277:1259–1266

    Article  Google Scholar 

  • Braendle C, Felix MA (2009) The other side of phenotypic plasticity: a developmental system that generates an invariant phenotype despite environmental variation. J Biosci 34:543–551

    Article  PubMed  Google Scholar 

  • Brommer JE, Rattiste K, Wilson AJ (2008) Exploring plasticity in the wild: laying date-temperature reaction norms in the common gull Larus canus. Proc R Soc Lond B 275:687–693

    Article  Google Scholar 

  • Brzek P, Konarzewski M (2004) Effect of refeeding on growth, development and behavior of undernourished bank swallow (Riparia riparia) nestlings. Auk 121:1187–1198

    Article  Google Scholar 

  • Carey C (2009) The impacts of climate change on the annual cycles of birds. Philos Trans R Soc Lond B 364:3321–3330

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chevin L-M, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8:e1000357

    Article  PubMed  Google Scholar 

  • Cleasby IR, Nakagawa S, Gillespie DOS, Burke T (2010) The influence of sex and body size on nestling survival and recruitment in the house sparrow. Biol J Linn Soc 101:680–688

    Article  Google Scholar 

  • Easterling DR, Meehl GA, Parmesan C, Changnon AS, Karl TR, Mearns LO (2000) Climate extremes: observations, modelling and impacts. Science 289:2068–2074

    Article  PubMed  CAS  Google Scholar 

  • Emlen ST, Wrege PH, Demong NJ, Hegner RE (1991) Flexible growth rates in nestling white-fronted bee-eaters: a possible adaptation to short-term food shortage. Condor 93:591–597

    Article  Google Scholar 

  • Etterson JR, Shaw RG (2001) Constraint to adaptive evolution in response to global warming. Science 294:151–154

    Article  PubMed  CAS  Google Scholar 

  • Garamszegi LZ, Török J, Michl G, Møller AP (2004) Female survival, lifetime reproductive success and mating status in a passerine bird. Oecologia 138:48–56

    Article  PubMed  Google Scholar 

  • García-Navas V, Sanz JJ (2011) The importance of a main dish: nestling diet and foraging behaviour in Mediterranean blue tits in relation to prey phenology. Oecologia 165:639–649

    Article  PubMed  Google Scholar 

  • Gebhardt-Henrich SG, van Noordwijk AJ (1991) Nestling growth in the great tit I. Heritability estimates under different environmental conditions. J Evol Biol 4:341–362

    Article  Google Scholar 

  • Ghalambor CK, McKay JK, Carroll S, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation to new environments. Funct Ecol 21:394–407

    Article  Google Scholar 

  • Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

    Article  PubMed  CAS  Google Scholar 

  • Hegyi G, Garamszegi LZ (2011) Using information theory as a substitute for stepwise regression in ecology and behavior. Behav Ecol Sociobiol 65:69–76

    Article  Google Scholar 

  • Hegyi G, Török J (2007) Developmental plasticity in a passerine bird: an experiment with collared flycatchers Ficedula albicollis. J Avian Biol 38:327–334

    Google Scholar 

  • Hegyi G, Rosivall B, Török J (2006) Paternal age and offspring growth: separating the intrinsic quality of young from rearing effects. Behav Ecol Sociobiol 60:672–682

    Article  Google Scholar 

  • Hegyi G, Rosivall B, Szöllősi E, Eens M, Török J (2011) Context-dependent effects of nestling growth trajectories on recruitment probability in the collared flycatcher. Behav Ecol Sociobiol 65:1647–1658

    Article  Google Scholar 

  • Hoffmann AA, Sgró CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  PubMed  CAS  Google Scholar 

  • Honarmand M, Goymann W, Naguib M (2010) Stressful dieting: nutritional conditions but not compensatory growth elevate corticosterone levels in zebra finch nestlings and fledglings. PLoS ONE 5:e12930

    Article  PubMed  Google Scholar 

  • Hüppop O, Hüppop K (2011) Bird migration on Helgoland: the yield from 100 years of research. J Ornithol 152:S25–S40

    Article  Google Scholar 

  • Hurrell JW, Deser C (2010) North Atlantic climate variability: the role of the North Atlantic oscillation. J Mar Syst 79:231–244

    Article  Google Scholar 

  • Husby A, Kruuk LEB, Visser ME (2009) Decline in the frequency and benefits of multiple brooding in great tits as a consequence of a changing environment. Proc R Soc Lond B 276:845–1854

    Article  Google Scholar 

  • Husby A, Nussey DH, Wilson AJ, Visser ME, Sheldon BC, Kruuk LEB (2010) Contrasting patterns of phenotypic plasticity in reproductive traits in two great tit (Parus major) populations. Evolution 64:2221–2237

    PubMed  Google Scholar 

  • Husby A, Visser ME, Kruuk LEB (2011) Speeding up microevolution: the effects of increasing temperature on selection and genetic variance in a wild bird population. PLoS Biol 9:e1000585

    Article  PubMed  CAS  Google Scholar 

  • Jones PD, Jónsson T, Wheeler D (1997) Extension to the North Atlantic oscillation using early instrumental pressure observations from Gibraltar and South-West Iceland. Int J Climatol 17:1433–1450

    Article  Google Scholar 

  • Karell P, Ahola K, Karstinen T, Valkama J, Brommer JE (2011) Climate change drives microevolution in a wild bird. Nat Comm 2:208

    Article  Google Scholar 

  • Kellermann V, van Heerwaarden B, Sgró CM, Hoffmann AA (2009) Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325:1244–1246

    Article  PubMed  CAS  Google Scholar 

  • Laaksonen T, Ahola M, Eeva T, Väisänen RA, Lehikoinen E (2006) Climate change, migratory connectivity and changes in laying date and clutch size of the pied flycatcher. Oikos 114:277–290

    Article  Google Scholar 

  • Leech DI, Crick HQP (2007) Influence of climate change on the abundance, distribution and phenology of woodland bird species in temperate regions. Ibis 149:S128–S145

    Article  Google Scholar 

  • Lepczyk CA, Karasov WH (2000) Effect of ephemeral food restrictions on growth of house sparrows. Auk 117:164–174

    Google Scholar 

  • Lindstrom A, Enemar A, Andersson G, von Proschwitz T, Nyholm NEI (2005) Density-dependent reproductive output in relation to a drastically varying food supply: getting the density measure right. Oikos 110:155–163

    Article  Google Scholar 

  • 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 

  • McCarty JP (2001) Variation in growth of nestling tree swallows across multiple temporal and spatial scales. Auk 118:176–190

    Google Scholar 

  • McGuigan K, Van Homrigh A, Blows MW (2008) Genetic analysis of female preference functions as function-valued traits. Am Nat 172:194–202

    Article  PubMed  Google Scholar 

  • McNeil K, Newman I, Kelly FJ (1996) Testing research hypotheses with the general linear model. Southern Illinois University Press, Carbondale and Edwardsville

    Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  • Mitchell JFB, Lowe J, Wood RA, Vellinga M (2006) Extreme events due to human-induced climate change. Philos Trans R Soc Lond B 364:2117–2133

    Article  Google Scholar 

  • Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc Natl Acad Sci USA 105:16195–16200

    Article  PubMed  Google Scholar 

  • Møller AP, Flensted-Jensen E, Klarborg K, Mardal W, Nielsen JT (2010) Climate change affects the duration of the reproductive season in birds. J Anim Ecol 79:777–784

    PubMed  Google Scholar 

  • Moreno J, Lobato E, Morales J, Merino S, Martínez-De La Puente J, Tomás G (2008) Pre-laying nutrition mediates maternal effects on offspring immune capacity and growth in the pied flycatcher. Oecologia 156:727–735

    Article  PubMed  Google Scholar 

  • Moussus J-P, Clavel J, Jiguet F, Julliard R (2011) Which are the phenologically flexible species? A case study with common passerine birds. Oikos 120:991–998

    Article  Google Scholar 

  • Nussey DH, Postma E, Gienapp P, Visser ME (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science 310:304–306

    Article  PubMed  CAS  Google Scholar 

  • Ozgul A, Tuljapurkar S, Benton TG, Pemberton JM, Clutton-Brock TH, Coulson T (2009) The dynamics of phenotypic change and the shrinking sheep of St Kilda. Science 325:464–467

    Article  PubMed  CAS  Google Scholar 

  • Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Perrins CM (1991) Tits and their caterpillar food supply. Ibis 133:S49–S54

    Article  Google Scholar 

  • Postma E (2006) Implications of the difference between true and predicted breeding values for the study of natural selection and micro-evolution. J Evol Biol 19:309–320

    Article  PubMed  CAS  Google Scholar 

  • Réale D, McAdam AG, Boutin S, Berteaux D (2003) Genetic and plastic responses of a northern mammal to climate change. Proc R Soc Lond B 270:591–596

    Article  Google Scholar 

  • Reed TE, Schindler DE, Waples RS (2011) Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conserv Biol 25:56–63

    Article  PubMed  Google Scholar 

  • Robinson JA, Hamer KC, Chivers LS (1992) Developmental plasticity in arctic terns Sterna paradisaea and common terns Sterna hirundo in response to a period of extremely bad weather. Ibis 144:344–346

    Article  Google Scholar 

  • Rosivall B, Török J, Hasselquist D, Bensch S (2004) Brood sex ratio adjustment in collared flycatchers (Ficedula albicollis): results differ between populations. Behav Ecol Sociobiol 56:346–351

    Article  Google Scholar 

  • Rosivall B, Szöllősi E, Török J (2005) Maternal compensation for hatching asynchrony in the collared flycatcher. J Avian Biol 36:531–537

    Article  Google Scholar 

  • Rosivall B, Szöllősi E, Hasselquist D, Török J (2009) Effects of extra-pair paternity and sex on nestling growth and condition in the collared flycatcher (Ficedula albicollis). Anim Behav 77:611–617

    Article  Google Scholar 

  • Rubolini D, Møller AP, Rainio K, Lehikoinen E (2007) Intraspecific consistency and geographic variability in temporal trends of spring migration phenology among European bird species. Climate Res 35:135–146

    Article  Google Scholar 

  • Saino N, Ambrosini R, Rubolini D, von Hardenberg J, Provenzale A, Hüppop K, Hüppop O, Lehikoinen A, Lehikoinen E, Rainio K, Romano M, Sokolov L (2011) Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc R Soc Lond B 278:835–842

    Article  Google Scholar 

  • Sanz JJ, Potti J, Moreno J, Merino S, Frias O (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Glob Change Biol 9:461–472

    Article  Google Scholar 

  • Schleucher E (2004) Taxonomy, energetics, and ecology. Physiol Biochem Zool 77:942–949

    Article  PubMed  Google Scholar 

  • Sheldon BC, Kruuk LEB, Merilä J (2003) Natural selection and inheritance of breeding time and clutch size in the collared flycatcher. Evolution 57:406–420

    PubMed  CAS  Google Scholar 

  • Siikamäki P (1996) Nestling growth and mortality of pied flycatchers Ficedula hypoleuca in relation to weather and breeding effort. Ibis 138:471–478

    Article  Google Scholar 

  • Smallegange E, 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

    Article  PubMed  Google Scholar 

  • Smith HG, Wettermark KJ (1995) Heritability of nestling growth in cross-fostered European starlings. Genetics 141:657–665

    PubMed  CAS  Google Scholar 

  • Starck JM, Ricklefs RE (1998) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, Oxford

    Google Scholar 

  • Szöllősi E, Rosivall B, Török J (2007) Is hatching asynchrony beneficial for the brood? Behav Ecol 18:420–426

    Article  Google Scholar 

  • Teplitsky C, Mills JA, Alho JS, Yarrall JW, Merilä J (2008) Bergmann’s rule and climate change revisited: disentangling environmental and genetic responses in a wild bird population. Proc Natl Acad Sci USA 105:13492–13496

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tinbergen JM, Verhulst S (2000) A fixed energetic ceiling to parental effort in the great tit? J Anim Ecol 69:323–334

    Article  Google Scholar 

  • Török J (1986) Food segregation in three hole-nesting bird species during the breeding season. Ardea 74:129–136

    Google Scholar 

  • Török J, Hegyi G, Tóth L, Könczey R (2004) Unpredictable food supply modifies costs of reproduction and hampers individual optimization. Oecologia 141:432–443

    Article  PubMed  Google Scholar 

  • Tøttrup AP, Thorup K, Rainio K, Yosef R, Lehikoinen E, Rahbek C (2008) Avian migrants adjust migration in response to environmental conditions en route. Biol Lett 4:685–688

    Article  PubMed  Google Scholar 

  • Umina PA, Weeks AR, Kearney MR, McKechnie SW, Hoffmann AA (2005) A rapid shift in a classical clinal pattern in Drosophila reflecting climate change. Science 308:691–693

    Article  PubMed  CAS  Google Scholar 

  • Van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55

    Article  PubMed  Google Scholar 

  • van Buskirk J, Mulvihill RS, Leberman RC (2009) Variable shifts in spring and autumn migration phenology in North American songbirds associated with climate change. Glob Change Biol 15:760–771

    Article  Google Scholar 

  • Végvári Z, Bókony V, Barta Z, Kovács G (2010) Life history predicts advancement of avian spring migration in response to climate change. Glob Change Biol 16:1–11

    Article  Google Scholar 

  • 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 

  • Walsh B, Blows MW (2009) Abundant genetic variation plus strong selection = multivariate genetic constraints: a geometric view of adaptation. Annu Rev Ecol Evol Syst 40:41–59

    Article  Google Scholar 

  • Wilson AJ, Pemberton JM, Pilkington JG, Coltman DW, Mifsud DV, Clutton-Brock TH, Kruuk LEB (2006) Environmental coupling of selection and heritability limits evolution. PLoS Biol 4:1270–1275

    Article  CAS  Google Scholar 

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Acknowledgments

We thank M. Herényi, M. Laczi, B. Rosivall and E. Szöllősi for help with the fieldwork. Supported by Országos Tudományos Kutatási Alapprogramok (Grants K75618 to J.T. and PD72117 and K101611 to G.H.), a Bolyai fellowship to G.H., the Erdők a Közjóért Alapítvány and the Pilis Park Forestry.

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The authors declare that they have no conflict of interest.

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Correspondence to Gergely Hegyi.

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Communicated by Indrikis Krams.

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Hegyi, G., Nagy, G. & Török, J. Reduced compensatory growth capacity in mistimed broods of a migratory passerine. Oecologia 172, 279–291 (2013). https://doi.org/10.1007/s00442-012-2487-5

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