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Seasonal trends in adult apparent survival and reproductive trade-offs reveal potential constraints to earlier nesting in a migratory bird

  • Population ecology – original research
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Abstract

Birds aim to optimize resources for feeding young and self-maintenance by timing reproduction to coincide with peak food availability. When reproduction is mistimed, birds could incur costs that affect their survival. We studied whether nesting phenology correlated with the apparent survival of American kestrels (Falco sparverius) from two distinct populations and examined trends in clutch-initiation dates. We estimated apparent survival using multi-state mark-recapture models with nesting timing, nesting success, sex, age, and weather covariates. Nesting timing predicted the apparent survival of successful adults; however, the effect differed between populations. Early nesting kestrels had higher apparent survival than later nesters in the western population, where kestrels have a relatively long nesting season. At the eastern site, where kestrels have a relatively short nesting season, the pattern was reversed—later nesters had higher apparent survival than earlier nesters. Nesting timing did not affect the apparent survival of adults with failed nests suggesting that the energetic cost of producing fledglings contributed to the timing effect. Finally, clutch-initiation dates advanced in the western population and remained static in the eastern population. Given that both populations have seasonal declines in productivity, population-specific survival patterns provide insight into seasonal trade-offs. Specifically, nesting timing effects on survival paralleled productivity declines in the western population and inverse patterns of survival and reproduction in the eastern population suggest a condition-dependent trade-off. Concomitant seasonal declines in reproduction and survival may facilitate population-level responses to earlier springs, whereas seasonal trade-offs may constrain phenology shifts and increase vulnerability to mismatch.

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Data availability

Data are available at Callery et al. (2022b).

References

  • Albright TP, Pidgeon AM, Rittenhouse CD, Clayton MK, Wardlow BD, Flather CH, Culbert PD, Radeloff VC (2010) Combined effects of heat waves and droughts on avian communities across the conterminous United States. Ecosphere 1:1–22

    Article  Google Scholar 

  • Anderson D, Burnham K (2004) Model selection and multi-model inference Second NY. Springer-Verlag 63:1007

    Google Scholar 

  • Anderson AM, Novak SJ, Smith JF, Steenhof K, Heath JA (2016) Nesting phenology, mate choice, and genetic divergence within a partially migratory population of American kestrels. Auk: Ornithol Adv 133:99–109

    Article  Google Scholar 

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike’s Information Criterion. J Wildl Manag 74:1175–1178

    Article  Google Scholar 

  • Bastianelli O, Charmantier A, Biard C, Bonamour S, Teplitsky C, Robert A (2021) Is earlier reproduction associated with higher or lower survival? Antagonistic results between individual and population scales in the blue tit. bioRxiv. https://doi.org/10.1101/2021.01.11.426202

    Article  Google Scholar 

  • Bird DM, Palmer RS (1988) American kestrel. In: Palmer RS (ed) Handbook of North American birds, vol 5: diurnal raptors, part 2. Yale University Press, New Haven, pp 253–290

    Google Scholar 

  • Blums P, Nichols JD, Hines JE, Lindberg MS, Mednis A (2005) Individual quality, survival variation and patterns of phenotypic selection on body condition and timing of nesting in birds. Oecologia 143:365–376

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Machler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400

    Article  Google Scholar 

  • Callery KR, Schulwitz SE, Hunt AR, Winiarski JM, McClure CJ, Fischer RA, Heath JA (2022a) Phenology effects on productivity and hatching-asynchrony of American kestrels (Falco sparverius) across a continent. bioRxiv. https://doi.org/10.1101/2022.01.14.476385

    Article  Google Scholar 

  • Callery KR, Smallwood JA, Hunt AR, Snyder ER, Heath JA (2022b) Dataset for Seasonal trends in adult apparent survival and reproductive trade-offs reveal potential constraints to earlier nesting in a migratory bird [Data set]. https://doi.org/10.18122/bio_data.9.boisestate

  • Catry T, Moreira F, Alcazar R, Rocha PA, Catry I (2016) Mechanisms and fitness consequences of laying decisions in a migratory raptor. Behav Ecol 28:222–232

    Article  Google Scholar 

  • Clutton-Brock TH (2019) The evolution of parental care. Princeton University Press, Princeton

    Book  Google Scholar 

  • Cohen J, Pfeiffer K, Francis JA (2018) Warm Arctic episodes linked with increased frequency of extreme winter weather in the United States. Nat Commun 9:1–12

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Dushoff J, Kain MP, Bolker BM (2019) I can see clearly now: reinterpreting statistical significance. Methods Ecol Evol 10:756–759

    Article  Google Scholar 

  • Garcia-Heras MS, Arroyo B, Mougeot F, Amar A, Simmons RE (2016) Does timing of breeding matter less where the grass is greener? Seasonal declines in breeding performance differ between regions in an endangered endemic raptor. Nat Conserv 15:23–45

    Article  Google Scholar 

  • Gimenez O, Lebreton J-D, Choquet R, Pradel R (2018) R2ucare: an r package to perform goodness-of-fit tests for capture–recapture models. Methods Ecol Evol 9:1749–1754

    Article  Google Scholar 

  • Golet GH, Irons DB, Estes JA (1998) Survival costs of chick rearing in black-legged kittiwakes. J Anim Ecol 67:827–841

    Article  Google Scholar 

  • Gorelick N, Hancher M, Dixon M, Ilyushchenko S, Thau D, Moore R (2017) Google earth engine: planetary-scale geospatial analysis for everyone. Remote Sens Environ 202:18–27

    Article  Google Scholar 

  • Griggs GR, Steenhof K (1993) Photographic guide for aging nestling American kestrels. USDI Bureau of Land Management Raptor Research Technical Assistance Center, Boise

  • Heath JA, Steenhof K, Foster MA (2012) Shorter migration distances associated with higher winter temperatures suggest a mechanism for advancing nesting phenology of American kestrels Falco sparverius. J Avian Biol 43:376–384

    Article  Google Scholar 

  • Hillström L, Moreno J (1992) Variation in time and energy budgets of breeding wheatears. Behaviour 120:11–39

    Article  Google Scholar 

  • Huang H, Winter JM, Osterberg EC, Horton RM, Beckage B (2017) Total and extreme precipitation changes over the northeastern United States. J Hydrometeorol 18:1783–1798

    Article  PubMed  PubMed Central  Google Scholar 

  • Irons RD, Harding Scurr A, Rose AP, Hagelin JC, Blake T, Doak DF (2017) Wind and rain are the primary climate factors driving changing phenology of an aerial insectivore. Proc R Soc B: Biol Sci 284:20170412

    Article  Google Scholar 

  • Izquierdo-Verdiguier E, Zurita-Milla R, Ault TR, Schwartz MD (2018) Development and analysis of spring plant phenology products: 36 years of 1-km grids over the conterminous US. Agric for Meteorol 262:34–41

    Article  Google Scholar 

  • Kelly JF, Horton KG, Stepanian PM, de Beurs KM, Fagin T, Bridge ES, Chilson PB (2016) Novel measures of continental-scale avian migration phenology related to proximate environmental cues. Ecosphere 7:e01434

    Article  Google Scholar 

  • Klaassen RH, Hake M, Strandberg R, Koks BJ, Trierweiler C, Exo KM, Bairlein F, Alerstam T (2014) When and where does mortality occur in migratory birds? Direct evidence from long-term satellite tracking of raptors. J Anim Ecol 83:176–184

    Article  PubMed  Google Scholar 

  • Laake J, Rexstad E (2008) RMark—an alternative approach to building linear models in MARK. In: Cooch E, White GC (eds) Program MARK: a gentle introduction

  • Lack DL (1968) Ecological adaptations for breeding in birds. London, Methuen & Co

  • Lafage D, Secondi J, Georges A, Bouzillé JB, Pétillon J (2014) Satellite-derived vegetation indices as surrogate of species richness and abundance of ground beetles in temperate floodplains. Insect Conserv Divers 7:327–333

    Article  Google Scholar 

  • Lebreton JD, Pradel R (2002) Multistate recapture models: modelling incomplete individual histories. J Appl Stat 29:353–369

    Article  Google Scholar 

  • 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 B: Biol Sci 279:3161–3169

    Article  Google Scholar 

  • Martin K (1995) Patterns and mechanisms for age-dependent reproduction and survival in birds. Am Zool 35:340–348

    Article  Google Scholar 

  • McCaslin HM, Caughlin TT, Heath JA (2020) Long-distance natal dispersal is relatively frequent and correlated with environmental factors in a widespread raptor. J Anim Ecol 89:2077–2088

    Article  PubMed  PubMed Central  Google Scholar 

  • McClure CJ, Schulwitz SE, van Buskirk R, Pauli BP, Heath JA (2017) Commentary: research recommendations for understanding the decline of American kestrels (Falco sparverius) across much of North America. J Raptor Res 51:455–464

    Article  Google Scholar 

  • McClure CJ, Brown JL, Schulwitz SE, Smallwood J, Farley KE, Therrien JF, Heath JA (2021) Demography of a widespread raptor across disparate regions. Ibis 163:658–670

    Article  Google Scholar 

  • Meijer T, Nienaber U, Langer U, Trillmich R (1999) Temperature and timing of egg-laying of European Starlings. Condor 101:124–132

    Article  Google Scholar 

  • Miller KE, Smallwood JA (1997) Natal dispersal and philopatry of southeastern American Kestrels in Florida. Wilson Bull 1:226–232

    Google Scholar 

  • Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc B: Biol Sci 365:3177–3186

    Article  Google Scholar 

  • Møller AP (1994) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35:115–122

    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 105:16195–16200

    Article  PubMed  PubMed Central  Google Scholar 

  • Nilsson JǺ, Svensson E (1996) The cost of reproduction: a new link between current reproductive effort and future reproductive success. Proc R Soc Lond B 263:711–714

    Article  Google Scholar 

  • Olsen P, Olsen J (1992) Does rain hamper hunting by breeding raptors? Emu-Austral Ornithol 92:184–187

    Article  Google Scholar 

  • Powers BF, Winiarski JM, Requena-Mullor JM, Heath JA (2021) Intra-specific variation in migration phenology of American kestrels (Falco sparverius) in response to spring temperatures. Ibis 163:1448–1456

    Article  Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing R Foundation for Statistical Computing. Vienna, Austria. https://wwwR-project.org/

  • 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

    Article  PubMed  Google Scholar 

  • Robinson RA, Meier CM, Witvliet W, Kéry M, Schaub M (2020) Survival varies seasonally in a migratory bird: Linkages between breeding and non-breeding periods. J Anim Ecol 89:2111–2121

    Article  PubMed  Google Scholar 

  • Root T (1988) Energy constraints on avian distributions and abundances. Ecology 69:330–339

    Article  Google Scholar 

  • Rosemartin AH, Denny EG, Weltzin JF, Lee Marsh R, Wilson BE, Mehdipoor H, Zurita-Milla R, Schwartz MD (2015) Lilac and honeysuckle phenology data 1956–2014. Sci Data 2:1–8

    Article  Google Scholar 

  • Rubolini D, Saino N, Møller AP (2010) Migratory behaviour constrains the phenological response of birds to climate change. Climate Res 42:45–55

    Article  Google Scholar 

  • Ruegg KC, Brinkmeyer M, Bossu CM, Bay RA, Anderson EC, Boal CW, Dawson RD, Eschenbauch A, McClure CJ, Miller KE, Morrow L, Morrow J, Oleyar MD, Ralph B, Schulwitz S, Swem T, Therrien J, van Buskirk RW, Smith TB, Heath JA (2021) The American kestrel (Falco sparverius) genoscape: Implications for monitoring, management, and subspecies boundaries. Ornithology 138:ukaa051

    Article  Google Scholar 

  • Saino N, Ambrosini R, Albetti B, Caprioli M, De Giorgio B, Gatti E, Leichti F, Parolini M, Romano A, Romano M, Scandolara C, Gianfranceschi L, Bollati V, Rubolini D (2017) Migration phenology and breeding success are predicted by methylation of a photoperiodic gene in the barn swallow. Sci Rep 7:1–10

    Article  CAS  Google Scholar 

  • Samplonius JM, Bartošová L, Burgess MD, Bushuev AV, Eeva T, Ivankina EV, Kerimov AB, Krams I, Laaksonen T, Magi M, Mand R, Potti J, Torok J, Trnka M, Visser ME, Zang H, Both C (2018) Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders. Glob Change Biol 24:3780–3790

    Article  Google Scholar 

  • Schaub M, Royle JA (2014) Estimating true instead of apparent survival using spatial Cormack-Jolly-Seber models. Methods Ecol Evol 5:1316–1326

    Article  Google Scholar 

  • Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the Northern Hemisphere. Glob Change Biol 12:343–351

    Article  Google Scholar 

  • Schwarz CJ, Schweigert JF, Arnason AN (1993) Estimating migration rates using tag-recovery data. Biometrics 49:177–193

    Article  Google Scholar 

  • Shutler D, Clark RG, Fehr C, Diamond AW (2006) Time and recruitment costs as currencies in manipulation studies on the costs of reproduction. Ecology 87:2938–2946

    Article  PubMed  Google Scholar 

  • Smallwood JA (1988) A mechanism of sexual segregation by habitat in American Kestrels (Falco sparverius) wintering in southcentral Florida. Auk 105:36–46

    Article  Google Scholar 

  • Smallwood JA (2016) Effects of researcher-induced disturbance on American Kestrels breeding in nest boxes in northwestern New Jersey. J Raptor Res 50:54–59

    Article  Google Scholar 

  • Smallwood JA, Bird DM (2020) American Kestrel (Falco sparverius), version 10. In: Poole AF, Gill FB (eds) Birds of the World. Cornell Lab of Ornithology, Ithaca. https://doi.org/10.2173/bow.amekes.01

  • Smallwood PD, Smallwood JA (1998) Seasonal shifts in sex ratios of fledgling American kestrels (Falco sparverius paulus): the early bird hypothesis. Evol Ecol 12:839–853

    Article  Google Scholar 

  • Smallwood JA, Causey MF, Mossop DH, Klucsarits JR, Robertson B, Robertson S, Mason J, Maurer MJ, Melvin RJ, Dawson RD, Bortolotti G, Parrish JW, Breen TF, Boyd K (2009) Why are American kestrel (Falco sparverius) populations declining in North America? Evidence from nest-box programs. J Raptor Res 43:274–282

    Article  Google Scholar 

  • Smith SH, Steenhof K, McClure CJ, Heath JA (2017) Earlier nesting by generalist predatory bird is associated with human responses to climate change. J Anim Ecol 86:98–107

    Article  PubMed  Google Scholar 

  • Sohrabi MM, Ryu JH, Abatzoglou J, Tracy J (2013) Climate extreme and its linkage to regional drought over Idaho, USA. Nat Hazards 65:653–681

    Article  Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Article  Google Scholar 

  • Steenhof K, Heath JA (2009) American Kestrel reproduction: evidence for the selection hypothesis and the role of dispersal. Ibis 151:493–501

    Article  Google Scholar 

  • Steenhof K, Heath JA (2013) Local recruitment and natal dispersal distances of American kestrels. Condor 115:584–592

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Thornton PE, Thornton M, Mayer BW, Wei Y, Devarakonda R, Vose RS, Cook RB (2018) Daymet: Daily Surface Weather Data on a 1-km Grid for North America, Version 3. ORNL DAAC, Oak Ridge

  • Verhulst S, Nilsson JA (2008) The timing of birds’ breeding seasons: A review of experiments that manipulated timing of breeding. Philos Trans R Soc B 363:399–410

    Article  Google Scholar 

  • Verhulst S, Tinbergen JM (1991) Experimental evidence for a causal relationship between timing and success of reproduction in the great tit Parus major. J Anim Ecol 60:269–282

    Article  Google Scholar 

  • Visser ME, Holleman LJ, 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

    Article  PubMed  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139

    Article  Google Scholar 

  • Woodworth BK, Wheelwright NT, Newman AE, Schaub M, Norris DR (2017) Winter temperatures limit population growth rate of a migratory songbird Nature. Communications 8:1–9

    Google Scholar 

  • Zuckerberg B, Bonter DN, Hochachka WM, Koenig WD, DeGaetano AT, Dickinson JL (2011) Climatic constraints on wintering bird distributions are modified by urbanization and weather. J Anim Ecol 80:403–413

    Article  PubMed  Google Scholar 

  • Zurita-Milla R, Goncalves R, Izquierdo-Verdiguier E, Ostermann FO (2017) Exploring vegetation phenology at continental scales: linking temperature-based indices and land surface phenological metrics. In: Proceedings of the 2017 Conference on Big Data from Space, Toulouse, pp 28–30

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Acknowledgements

We thank Jason Winiarski for the extended spring index analysis. Jason Winiarski and Chris McClure provided statistical advice and thoughtful comments on early drafts of the manuscript. Comments from our handling editor, Rob Robinson, and two anonymous reviewers greatly improved the manuscript. We thank landowners for allowing access to their property.

Funding

Funding for this project was provided by a grant from the Strategic Environmental Research and Development Program (SERDP) of the US Department of Defense (US DoD; Award Number: RC-2702) and the Boise State and American Kestrel Partnership Adopt-A-Box Partners. Release time for JAS was provided by the Faculty Scholarship Program, Montclair State University.

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  1. Emilie R. Snyder

    Present address: New Jersey Department of Environmental Protection, Trenton, NJ, USA

Authors and Affiliations

  1. Department of Biological Sciences and Raptor Research Center, Boise State University, Boise, ID, USA

    Kathleen R. Callery, Anjolene R. Hunt & Julie A. Heath

  2. Department of Biology, Montclair State University, Montclair, NJ, USA

    John A. Smallwood & Emilie R. Snyder

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  1. Kathleen R. Callery
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Contributions

KRC, JAH, JAS, ARH originally formulated the idea, all authors conducted fieldwork and curated data for analysis, KRC and JAH analyzed data, KRC wrote the first draft of the manuscript and all authors contributed to revision.

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Correspondence to Julie A. Heath.

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The authors have no conflicts of interest to declare.

Ethics approval

American kestrels were handled and marked under the authority of federal bird banding permits (JAH: 23307, JAS: 21378), New Jersey scientific collecting permit SC 2017023, and its predecessors, Idaho scientific collecting permits, and institutional IACUCs.

Additional information

Communicated by Thomas Koert Lameris.

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Callery, K.R., Smallwood, J.A., Hunt, A.R. et al. Seasonal trends in adult apparent survival and reproductive trade-offs reveal potential constraints to earlier nesting in a migratory bird. Oecologia 199, 91–102 (2022). https://doi.org/10.1007/s00442-022-05169-w

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