Climate is an important driver of changes in animal population size, but its effect on the underlying demographic rates remains insufficiently understood. This is particularly true for avian long-distance migrants which are exposed to different climatic factors at different phases of their annual cycle. To fill this knowledge gap, we used data collected by a national-wide bird ringing scheme for eight migratory species wintering in sub-Saharan Africa and investigated the impact of climate variability on their breeding productivity and adult survival. While temperature at the breeding grounds could relate to the breeding productivity either positively (higher food availability in warmer springs) or negatively (food scarcity in warmer springs due to trophic mismatch), water availability at the non-breeding should limit the adult survival and the breeding productivity. Consistent with the prediction of the trophic mismatch hypothesis, we found that warmer springs at the breeding grounds were linked with lower breeding productivity, explaining 29% of temporal variance across all species. Higher water availability at the sub-Saharan non-breeding grounds was related to higher adult survival (18% temporal variance explained) but did not carry-over to breeding productivity. Our results show that climate variability at both breeding and non-breeding grounds shapes different demographic rates of long-distance migrants.

Bird Ringing Centre National Museum Prague Hornoměcholupská 34 102 00 Praha 10 Czech Republic

Department of Zoology and Laboratory of Ornithology Faculty of Science Palacky University in Olomouc 17 listopadu 50 771 46 Olomouc Czech Republic

Institute for Environmental Studies Faculty of Science Charles University Prague Benátská 2 128 01 Praha 2 Czech Republic

Institute of Vertebrate Biology Academy of Sciences of the Czech Republic Květná 8 603 65 Brno Czech Republic

Zobrazit více v PubMed

Hawkins BA, et al. Energy, water, and broad-scale geographic patterns of species richness. Ecology. 2003;84:3105–3117. doi: 10.1890/03-8006. DOI

Pecl GT, et al. Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science. 2017;355:eaai9214. doi: 10.1126/science.aai9214. PubMed DOI

Pearce-Higgins JW, Eglington SM, Martay B, Chamberlain DE. Drivers of climate change impacts on bird communities. J. Anim. Ecol. 2015;84:943–954. doi: 10.1111/1365-2656.12364. PubMed DOI

Sanderson FJ, Donald PF, Pain DJ, Burfield IJ, van Bommel FPJ. Long-term population declines in Afro-Palearctic migrant birds. Biol. Conserv. 2006;131:93–105. doi: 10.1016/j.biocon.2006.02.008. DOI

Wilcove DS, Wikelski M. Going, going, gone: Is animal migration disappearing. PLoS Biol. 2008;6:e188. doi: 10.1371/journal.pbio.0060188. PubMed DOI PMC

Koleček J, Procházka P, Ieronymidou C, Burfield IJ, Reif J. Non-breeding range size predicts the magnitude of population trends in trans-Saharan migratory passerine birds. Oikos. 2018;127:599–606. doi: 10.1111/oik.04549. DOI

Marra PP, Cohen EB, Loss SR, Rutter JE, Tonra CM. A call for full annual cycle research in animal ecology. Biol. Lett. 2015;11:20150552. doi: 10.1098/rsbl.2015.0552. PubMed DOI PMC

Rolland J, et al. The impact of endothermy on the climatic niche evolution and the distribution of vertebrate diversity. Nat. Ecol. Evol. 2018;2:459–464. doi: 10.1038/s41559-017-0451-9. PubMed DOI

Jiguet F, et al. Population trends of European common birds are predicted by characteristics of their climatic niche. Global Change Biol. 2010;16:497–505. doi: 10.1111/j.1365-2486.2009.01963.x. DOI

Eglington SM, et al. Latitudinal gradients in the productivity of European migrant warblers have not shifted northwards during a period of climate change. Global Ecol. Biogeogr. 2015;24:427–436. doi: 10.1111/geb.12267. DOI

Meller K, Piha M, Vähätalo AV, Lehikoinen A. A positive relationship between spring temperature and productivity in 20 songbird species in the boreal zone. Oecologia. 2018;186:883–893. doi: 10.1007/s00442-017-4053-7. PubMed DOI

Townsend AK, et al. Warm springs, early lay dates, and double brooding in a North American migratory songbird, the Black-Throated Blue Warbler. PLoS ONE. 2013;8:e59467. doi: 10.1371/journal.pone.0059467. PubMed DOI PMC

Whittaker RJ, Nogués-Bravo D, Araújo MB. Geographical gradients of species richness: a test of the water-energy conjecture of Hawkins et al. (2003) using European data for five taxa. Global Ecol. Biogeogr. 2007;16:76–89. doi: 10.1111/j.1466-8238.2006.00268.x. DOI

Visser ME, Gienapp P. Evolutionary and demographic consequences of phenological mismatches. Nat. Ecol. Evol. 2019;3:879–885. doi: 10.1038/s41559-019-0880-8. PubMed DOI PMC

Thackeray SJ, et al. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob. Change Biol. 2010;16:3304–3313. doi: 10.1111/j.1365-2486.2010.02165.x. DOI

Donnelly A, Yu R, Liu L. Trophic level responses differ as climate warms in Ireland. Int. J. Biometeorol. 2014;59:1007–1017. doi: 10.1007/s00484-014-0914-5. PubMed DOI

Ross MV, Alisauskas RT, Douglas DC, Kelletti DK. Decadal declines in avian herbivore reproduction: density-dependent nutrition and phenological mismatch in the Arctic. Ecology. 2017;98:1869–1883. doi: 10.1002/ecy.1856. PubMed DOI

Visser ME, Holleman LJM, Gienapp P. Shifts in caterpillar biomassphenology due to climate change and its impact on the breeding biology of aninsectivorous bird. Oecologia. 2006;147:164–172. doi: 10.1007/s00442-005-0299-6. PubMed DOI

Samplonius JM, Kappers EF, Brands S, Both C. Phenological mismatch and ontogenetic diet shifts interactively affect offspring condition in a passerine. J. Anim. Ecol. 2016;85:1255–1264. doi: 10.1111/1365-2656.12554. PubMed DOI

Finch T, Pearce-Higgins J, Leech DI, Evans K. Carry-over effects from passage regions are more important than breeding climate in determining the breeding phenology and performance of three avian migrants of conservation concern. Biodivers. Conserv. 2014;23:2427–2444. doi: 10.1007/s10531-014-0731-5. DOI

Both C, Ubels R, Ravussin P-A. Life-history innovation to climate change: can single-brooded migrant birds become multiple breeders? J. Avian Biol. 2019;50:01951. doi: 10.1111/jav.01951. DOI

Ockendon N, et al. Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects. Global Change Biol. 2014;20:2221–2229. doi: 10.1111/gcb.12559. PubMed DOI

Ambrosini R, Saino N, Rubolini D, Møller AP. Higher degree-days at the time of breeding predict size of second clutches in the barn swallow. Clim. Res. 2011;50:43–50. doi: 10.3354/cr01034. DOI

Cayton HL, Haddad NM, Gross K, Diamond SE, Ries L. Do growing degree days predict phenology across butterfly species? Ecology. 2015;96:1473–1479. doi: 10.1890/15-0131.1. DOI

Saino N, et al. Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc. R. Soc. B. 2011;278:835–842. doi: 10.1098/rspb.2010.1778. PubMed DOI PMC

Winstanley D, Spencer R, Williamson K. Where have all the Whitethroats gone? Bird Study. 1974;21:1–14.

Peach WJ, Baillie SR, Balmer DE. Survival of British Sedge Warblers Acrocephalus schoenobaenus in relation to west African rainfall. Ibis. 1991;133:300–305. doi: 10.1111/j.1474-919X.1991.tb04573.x. DOI

Johnston A, et al. Survival of Afro-Palaearctic passerine migrants in western Europe and the impacts of seasonal weather variables. Ibis. 2016;158:465–480. doi: 10.1111/ibi.12366. DOI

Norris DR, Marra PP. Seasonal interactions, habitat quality, and population dynamics in migratory birds. Condor. 2007;109:535–547. doi: 10.1093/condor/109.3.535. DOI

Gordo O, Sanz JJ. The relative importance of conditions in wintering and passage areas on spring arrival dates: the case of long-distance Iberian migrants. J. Ornith. 2008;149:199–210. doi: 10.1007/s10336-007-0260-z. DOI

Saino N, et al. Temperature and rainfall anomalies in Africa predict timing of spring migration in trans-Saharan migratory birds. Clim. Res. 2007;35:123–134. doi: 10.3354/cr00719. DOI

Smith RJ, Moore FR. Arrival fat and reproductive performance in a long-distance passerine migrant. Oecologia. 2003;134:325–331. doi: 10.1007/s00442-002-1152-9. PubMed DOI

Norman D, Peach WJ. Density-dependent survival and recruitment in a long-distance Palaearctic migrant, the Sand Martin Riparia riparia. Ibis. 2013;155:284–296. doi: 10.1111/ibi.12036. DOI

Nicholson SE. The nature of rainfall variability over Africa on time scales of decades to millenia. Glob. Planet. Change. 2000;26:137–158. doi: 10.1016/S0921-8181(00)00040-0. DOI

Vickery JA, et al. The decline of Afro-Palaearctic migrants and an assessment of potential causes. Ibis. 2014;156:1–22. doi: 10.1111/ibi.12118. DOI

Post E, Forchhammer MC. Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos. Trans. R. Soc. B. 2008;363:2369–2375. doi: 10.1098/rstb.2007.2207. PubMed DOI PMC

Møller AP, Rubolini D, Lehikoinen E. Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc. Natl. Acad. Sci. U. S. A. 2008;105:16195–16200. doi: 10.1073/pnas.0803825105. PubMed DOI PMC

Both C, Bouwhuis S, Lessells CM, Visser ME. Climate change and population declines in a long-distance migratory bird. Nature. 2006;441:81–83. doi: 10.1038/nature04539. PubMed DOI

Sanz JJ, Potti J, Moreno J, Merino S, Frías O. Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Global Change Biol. 2003;9:461–472. doi: 10.1046/j.1365-2486.2003.00575.x. DOI

Skwarska J, et al. Long-term variation in laying date and clutch size of Pied Flycatchers Ficedula hypoleuca in central Poland. Pol. J. Ecol. 2012;60:187–192.

González-Braojos S, Jose Sanz J, Moreno J. Decline of a montane Mediterranean pied flycatcher Ficedula hypoleuca population in relation to climate. J. Avian Biol. 2017;48:1383–1393. doi: 10.1111/jav.01405. DOI

Suryan RM, Irons DB, Brown ED, Jodice PGR, Roby DD. Site-specific effects on productivity of an upper trophic-level marine predator: bottom-up, top-down, and mismatch effects on reproduction in a colonial seabird. Prog. Oceanogr. 2006;68:303–328. doi: 10.1016/j.pocean.2006.02.006. DOI

Gaston AJ, Gilchrist HG, Mallory ML, Smith PA. Changes in seasonal events, peak food availability, and consequent breeding adjustment in a marine bird: a case of progressive mismatching. Condor. 2009;111:111–119. doi: 10.1525/cond.2009.080077. DOI

Ramírez F, et al. Oceanographic drivers and mistiming processes shape breeding success in a seabird. Proc. R. Soc. B. 2016;283:20152287. doi: 10.1098/rspb.2015.2287. PubMed DOI PMC

Doiron M, Gauthier G, Lévesque E. Trophic mismatch and its effects on the growth of young in an Arctic herbivore. Glob. Chang. Biol. 2015;21:4364–4376. doi: 10.1111/gcb.13057. PubMed DOI

McKinnon L, Picotin M, Bolduc E, Juillet C, Bêty J. Timing of breeding, peak food availability, and effects of mismatch on chick growth in birds nesting in the High Arctic. Can. J. Zoo. 2012;90:961–971. doi: 10.1139/z2012-064. DOI

Bowers EK, et al. Spring temperatures influence selection on breeding date and the potential for phenological mismatch in a migratory bird. Ecology. 2016;97:2880–2891. doi: 10.1002/ecy.1516. PubMed DOI PMC

Charmentier A, et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science. 2008;320:800–803. doi: 10.1126/science.1157174. PubMed DOI

Koleček J, Adamík P, Reif J. Shifts in migration phenology under climate change: temperature vs. abundance effects in birds. Climatic Change. 2020;159:177–194. doi: 10.1007/s10584-020-02668-8. DOI

Rubolini D, Saino N, Møller AP. Migratory behaviour constrains the phenological response of birds to climate change. Clim. Res. 2010;42:45–55. doi: 10.3354/cr00862. DOI

Schmaljohann H, Both C. The limits of modifying migration speed to adjust to climate change. Nat. Clim. Change. 2017;7:573–576. doi: 10.1038/nclimate3336. DOI

Kolarova E, Adamik P. Bird arrival dates in Central Europe based on one of the earliest phenological networks. Clim. Res. 2015;63:91–98. doi: 10.3354/cr01290. DOI

Rubolini D, Møller AP, Rainio K, Lehikoinen E. Intraspecific consistency and geographic variability in temporal trends of spring migration phenology among European bird species. Clim. Res. 2007;35:135–146. doi: 10.3354/cr00720. DOI

Reed TE, Grøtan V, Jenouvrier S, Sæther B-E, Visser ME. Population growth in a wild bird is buffered against phenological mismatch. Science. 2013;340:488–491. doi: 10.1126/science.1232870. PubMed DOI

Mallord JW, et al. Diet flexibility in a declining long-distance migrant may allow it to escape the consequences of phenological mismatch with its caterpillar food supply. Ibis. 2017;159:76–90. doi: 10.1111/ibi.12437. DOI

Simmonds EG, Sheldon BC, Coulson T, Cole EF. Incubation behavior adjustments, driven by ambient temperature variation, improve synchrony between hatch dates and caterpillar peak in a wild bird population. Ecol. Evol. 2017;7:9415–9425. doi: 10.1002/ece3.3446. PubMed DOI PMC

Tomotani BM, et al. Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird. Glob. Change Biol. 2018;24:823–835. doi: 10.1111/gcb.14006. PubMed DOI

Vatka E, Rytkonen S, Orell M. Does the temporal mismatch hypothesis match in boreal populations? Oecologia. 2014;176:595–605. doi: 10.1007/s00442-014-3022-7. PubMed DOI

Eeva T, Lehikoinen E, Rönkä M, Lummaa V, Currie D. Different responses to cold weather in two pied flycatcher populations. Ecography. 2002;25:705–713. doi: 10.1034/j.1600-0587.2002.250606.x. DOI

McKinnon L, Nol E, Juillet C. Arctic-nesting birds find physiological relief in the face of trophic constraints. Sci. Rep. 2013;3:1816. doi: 10.1038/srep01816. PubMed DOI PMC

Wittwer T, O’Hara RB, Caplat P, Hickler T, Smith HG. Long-term population dynamics of a migrant bird suggests interaction of climate change and competition with resident species. Oikos. 2015;124:1151–1159. doi: 10.1111/oik.01559. DOI

Wiebe KL. Interspecific competition for nests: Prior ownership trumps resource holding potential for Mountain Bluebird competing with Tree Swallow. Auk. 2016;133:512–519. doi: 10.1642/AUK-16-25.1. DOI

Ahola MP, Laaksonen T, Eeva T, Lehikoinen E. Climate change can alter competitive relationships between resident and migratory birds. J. Anim. Ecol. 2007;76:1045–1052. doi: 10.1111/j.1365-2656.2007.01294.x. PubMed DOI

Samplonius JM, Both C. Climate change may affect fatal competition between two bird species. Curr. Biol. 2019;29:327–331. doi: 10.1016/j.cub.2018.11.063. PubMed DOI

Wesolowski T. Primeval conditions—what can we learn from them? Ibis. 2007;149:64–77. doi: 10.1111/j.1474-919X.2007.00721.x. DOI

Adamík P, Král M. Climate-and resource-driven long-term changes in dormice populations negatively affect hole-nesting songbirds. J. Zool. 2008;275:209–215. doi: 10.1111/j.1469-7998.2008.00415.x. DOI

Ӧberg M, et al. Rainfall during parental care reduces reproductive and survival components of fitness in a passerine bird. Ecol. Evol. 2015;5:345–356. doi: 10.1002/ece3.1345. PubMed DOI PMC

Mazer SJ, Gerst KL, Matthews ER, Evenden A. Species-specific phenological responses to winter temperature and precipitation in a waterlimited ecosystem. Ecosphere. 2015;6:1–27. doi: 10.1890/ES14-00433.1. DOI

Morrison CA, Robinson RA, Butler SJ, Clark JA, Gill JA. Demographic drivers of decline and recovery in an Afro-Palaearctic migratory bird population. Proc. R. Soc. B. 2016;283:20161387. doi: 10.1098/rspb.2016.1387. PubMed DOI PMC

Ockendon N, Hewson CM, Johnston A, Atkinson PW. Declines in British breeding populations of Afro-Palaearctic migrant birds are linked to bioclimatic wintering zone in Africa, possibly via constraints on arrival time advancement. Bird Study. 2012;59:111–125. doi: 10.1080/00063657.2011.645798. DOI

Zwarts L, Bijlsma RG, van der Kamp J, Wymenga E. Living on the Edge: Wetlands and Birds in a Changing Sahel. KNNV Uitgeveri: Zeist; 2009.

Tøttrup AP, et al. Drought in Africa caused delayed arrival of European songbirds. Science. 2012;338:1307–1307. doi: 10.1126/science.1227548. PubMed DOI

Woodworth BK, Wheelwright NT, Newman AE, Schaub M, Norris DR. Winter temperatures limit population growth rate of a migratory songbird. Nature Commun. 2017;8:14812. doi: 10.1038/ncomms14812. PubMed DOI PMC

Calvert AM, Walde SJ, Taylor PD. Nonbreeding-season drivers of population dynamics in seasonal migrants: conservation parallels across taxa. Avian Conserv. Ecol. 2009;4:5–5. doi: 10.5751/ACE-00335-040205. DOI

Cresswell W. Migratory connectivity of Palaearctic-African migratory birds and their responses to environmental change: the serial residency hypothesis. Ibis. 2014;156:493–510. doi: 10.1111/ibi.12168. DOI

Brlík V, et al. Weak effects of geolocators on small birds: a meta-analysis controlled for phylogeny and publication bias. J. Anim. Ecol. 2020;89:207–220. doi: 10.1111/1365-2656.12962. PubMed DOI

Cepák, J. et al. (eds) Czech and Slovak Bird Migration Atlas (Aventinum, 2008).

Šťastný, K. & Hudec, K. (eds) Fauna of the Czech Republic. Birds III. (Academia, 2011).

Dinerstein E, et al. An ecoregion-based approach to protecting half the terrestrial realm. Bioscience. 2017;67:534–545. doi: 10.1093/biosci/bix014. PubMed DOI PMC

Anonymus. Metodický předpis č. 10: Návod pro činnost fenologických stanic. Lesní rostliny[Methodical instruction No.10: Instructions for phenological stations. Wild plants] (ČHMÚ, 2009).

Šímová I, Storch D. The enigma of terrestrial primary productivity: measurements, models, scales and the diversity-productivity relationship. Ecography. 2017;40:239–252. doi: 10.1111/ecog.02482. DOI

Huntley, B., Green, R. E., Collingham, Y. C. & Willis, S. G. A Climatic Atlas of European Breeding Birds (Lynx Edicions, 2007) PubMed PMC

Mu QZ, Zhao MS, Running SW. Improvements to a MODIS global terrestrial evapotranspiration algorithm. Remote Sens. Environ. 2011;115:1781–1800. doi: 10.1016/j.rse.2011.02.019. DOI

Adamík P, et al. Barrier crossing in small avian migrants: individual tracking reveals prolonged nocturnal flights into the day as a common migratory strategy. Sci. Rep. 2016;6:21560. doi: 10.1038/srep21560. PubMed DOI PMC

Koleček J, et al. Cross-continental migratory connectivity and spatiotemporal migratory patterns in the great reed warbler. J. Avian Biol. 2016;47:756–767. doi: 10.1111/jav.00929. DOI

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Soft. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

R Core Team. R: A language and environment for statistical computing. https://www.r-project.org/ (2016).

Kéry, M. & Royle, J. A. Applied Hierarchical Modeling in Ecology: Analysis of Distribution, Abundance and Species Richness in R and BUGS. Volume 1: Prelude and Static Models. (Academic, 2016)

Grosbois V, et al. Assessing the impact of climate variation on survival in vertebrate populations. Biol. Rev. 2008;83:357–399. doi: 10.1111/j.1469-185X.2008.00047.x. PubMed DOI

Pradel R, Hines JE, Lebreton JD, Nichols JD. Capture-recapture survival models taking account of transients. Biometrics. 1997;53:60–72. doi: 10.2307/2533097. DOI

Laake, J. L. RMark: An R Interface for Analysis of Capture-recapture Data with MARK (AFSC Processed Rep., 2013).

Gelman A, Rubin DB. Inference from iterative simulation using multiple sequences. Stat. Sci. 1992;7:457–472. doi: 10.1214/ss/1177011136. DOI

Plummer M, Best N, Cowles K, Vines K. CODA: convergence diagnosis and output analysis for MCMC. R News. 2006;6:7–11.

Westoby M, Leishman M, Lord J. Further remarks on phylogenetic correction. J. Ecol. 1995;83:727–729. doi: 10.2307/2261640. DOI

de Bello F, et al. On the need for phylogenetic ‘corrections’ in functional trait-based approaches. Folia Geobot. 2015;50:349–357. doi: 10.1007/s12224-015-9228-6. DOI

Reif J, Telenský T, Klvaňa P, Jelínek M, Cepák J. Data from: The influence of climate variability on demographic rates of avian Afro-palearctic migrants. Dryad. 2020 doi: 10.5061/dryad.x95x69pgf. PubMed DOI PMC

Survival fluctuation is linked to precipitation variation during staging in a migratory shorebird

The influence of climate variability on demographic rates of avian Afro-palearctic migrants