A full annual perspective on sex-biased migration timing in long-distance migratory birds
Language English Country Great Britain, England Media print
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
30963841
PubMed Central
PMC6408886
DOI
10.1098/rspb.2018.2821
Knihovny.cz E-resources
- Keywords
- annual cycle, geolocator, long-distance migrant, migration phenology, protandry, protogyny,
- MeSH
- Animal Migration * MeSH
- Birds physiology MeSH
- Seasons MeSH
- Reproduction MeSH
- Sex Factors MeSH
- Songbirds physiology MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe MeSH
- Africa, Northern MeSH
In many taxa, the most common form of sex-biased migration timing is protandry-the earlier arrival of males at breeding areas. Here we test this concept across the annual cycle of long-distance migratory birds. Using more than 350 migration tracks of small-bodied trans-Saharan migrants, we quantify differences in male and female migration schedules and test for proximate determinants of sex-specific timing. In autumn, males started migration about 2 days earlier, but this difference did not carry over to arrival at the non-breeding sites. In spring, males on average departed from the African non-breeding sites about 3 days earlier and reached breeding sites ca 4 days ahead of females. A cross-species comparison revealed large variation in the level of protandry and protogyny across the annual cycle. While we found tight links between individual timing of departure and arrival within each migration season, only for males the timing of spring migration was linked to the timing of previous autumn migration. In conclusion, our results demonstrate that protandry is not exclusively a reproductive strategy but rather occurs year-round and the two main proximate determinants for the magnitude of sex-biased arrival times in autumn and spring are sex-specific differences in departure timing and migration duration.
Department of Animal Ecology Ecology and Genetics Uppsala University Uppsala Sweden
Department of Bird Migration Swiss Ornithological Institute Sempach Switzerland
Department of Zoology Palacký University Olomouc Czech Republic
Institute of Vertebrate Biology The Czech Academy of Sciences Brno Czech Republic
Museum of Natural History Olomouc Czech Republic
South Iceland Research Centre University of Iceland Laugarvatn Iceland
See more in PubMed
Bauer S, Hoye BJ. 2014. Migratory animals couple biodiversity and ecosystem functioning worldwide. Science 344, 1242552 (10.1126/science.1242552) PubMed DOI
Alerstam T, Hedenström A, Åkesson S. 2003. Long-distance migration: evolution and determinants. Oikos 2103, 247–260. (10.1034/j.1600-0706.2003.12559.x) DOI
Dingle H. 2014. Migration: the biology of life on the move, 2nd edn Oxford, UK: Oxford University Press.
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, 16 195–16 200. (10.1073/pnas.0803825105) PubMed DOI PMC
Kokko H. 1999. Competition for early arrival birds in migratory birds. J. Anim. Ecol. 68, 940–950. (10.1046/j.1365-2656.1999.00343.x) DOI
Kokko H, Gunnarsson TG, Morrell LJ, Gill JA. 2006. Why do female migratory birds arrive later than males? J. Anim. Ecol. 75, 1293–1303. (10.1111/j.1365-2656.2006.01151.x) PubMed DOI
Møller AP. 2004. Protandry, sexual selection and climate change. Glob. Chang. Biol. 10, 2028–2035. (10.1111/j.1365-2486.2004.00874.x) DOI
Cristol DA, Baker MB, Carbone C. 1999. Differential migration revisited: latitudinal segregation by age and sex class. Curr. Ornithol. 15, 33–88. (10.1007/978-1-4757-4901-4_2) DOI
Morbey YE, Ydenberg RC. 2001. Protandrous arrival timing to breeding areas: a review. Ecol. Lett. 4, 663–673. (10.1046/j.1461-0248.2001.00265.x) DOI
Oring LW, Lank DB. 1982. Sexual selection, arrival times, philopatry and site fidelity in the polyandrous spotted sandpiper. Behav. Ecol. Sociobiol. 10, 185–191. (10.1007/BF00299684) DOI
Ydenberg RC, Niehaus AC, Lank DB. 2005. Interannual differences in the relative timing of southward migration of male and female western sandpipers (Calidris mauri). Naturwissenschaften 92, 332–335. (10.1007/s00114-005-0637-x) PubMed DOI
Mills AM. 2005. Protogyny in autumn migration: do male birds ‘play chicken’? Auk 122, 71 (10.1642/0004-8038(2005)122[0071:PIAMDM]2.0.CO;2) DOI
Morbey YE, Coppack T, Pulido F. 2012. Adaptive hypotheses for protandry in arrival to breeding areas: a review of models and empirical tests. J. Ornithol. 153, 207–215. (10.1007/s10336-012-0854-y) DOI
Schmaljohann H, et al. 2016. Proximate causes of avian protandry differ between subspecies with contrasting migration challenges. Behav. Ecol. 27, 321–331. (10.1093/beheco/arv160) DOI
Both C, Bijlsma RG, Ouwehand J. 2016. Repeatability in spring arrival dates in pied flycatchers varies among years and sexes. Ardea 104, 3–21. (10.5253/arde.v104i1.a1) DOI
Tarka M, Hansson B, Hasselquist D. 2015. Selection and evolutionary potential of spring arrival phenology in males and females of a migratory songbird. J. Evol. Biol. 28, 1024–1038. (10.1111/jeb.12638) PubMed DOI
Klvaňa P, Cepák J, Munclinger P, Michálková R, Tomášek O, Albrecht T. 2017. Around the Mediterranean: an extreme example of loop migration in a long-distance migratory passerine. J. Avian Biol. 39, 133–138. (10.1111/jav.01595) DOI
Tøttrup AP, Thorup K. 2008. Sex-differentiated migration patterns, protandry and phenology in north European songbird populations. J. Ornithol. 149, 161–167. (10.1007/s10336-007-0254-x) DOI
Becker PH, Schmaljohann H, Riechert J, Wagenknecht G, Zajková Z, González-Solís J. 2016. Common terns on the East Atlantic Flyway: temporal–spatial distribution during the non-breeding period. J. Ornithol. 157, 927–940. (10.1007/s10336-016-1346-2) DOI
Cadahía L, Labra A, Knudsen E, Nilsson A, Lampe HM, Slagsvold T, Stenseth NC. 2017. Advancement of spring arrival in a long-term study of a passerine bird: sex, age and environmental effects. Oecologia 184, 917–929. (10.1007/s00442-017-3922-4) PubMed DOI
Ouwehand J, Both C. 2017. African departure rather than migration speed determines variation in spring arrival in pied flycatchers. J. Anim. Ecol. 86, 88–97. (10.1111/1365-2656.12599) PubMed DOI
Briedis M, Krist M, Král M, Voigt CC, Adamík P. 2018. Linking events throughout the annual cycle in a migratory bird—wintering period buffers accumulation of carry-over effects. Behav. Ecol. Sociobiol. 72, 93 (10.1007/s00265-018-2509-3) DOI
Marra PP, Hobson KA, Holmes RT. 1998. Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282, 1884–1886. (10.1126/science.282.5395.1884) PubMed DOI
Tøttrup AP, Klaassen RHG, Kristensen MW, Strandberg R, Vardanis Y, Lindström Å, Rahbek C, Alerstam T, Thorup K. 2012. Drought in Africa caused delayed arrival of European songbirds. Science 338, 1307 (10.1126/science.1227548) PubMed DOI
Both C, et al. 2006. Pied flycatchers Ficedula hypoleuca travelling from Africa to breed in Europe: differential effects of winter and migration conditions on breeding date. Ardea 94, 511–525.
Briedis M, Bauer S. 2018. Migratory connectivity in the context of differential migration. Biol. Lett. 14, 20180679 (10.1098/rsbl.2018.0679) PubMed DOI PMC
Arlt D, Olsson P, Fox JW, Low M, Pärt T. 2015. Prolonged stopover duration characterises migration strategy and constraints of a long-distance migrant songbird. Anim. Migr. 2, 47–62. (10.1515/ami-2015-0002) DOI
Arizaga J, Willemoes M, Unamuno E, Unamuno JM, Thorup K. 2015. Following year-round movements in barn swallows using geolocators: could breeding pairs remain together during the winter? Bird Study 62, 141–145. (10.1080/00063657.2014.998623) DOI
Briedis M, Träff J, Hahn S, Ilieva M, Král M, Peev S, Adamík P. 2016. Year-round spatiotemporal distribution of the enigmatic semi-collared flycatcher Ficedula semitorquata. J. Ornithol. 157, 895–900. (10.1007/s10336-016-1334-6) DOI
Briedis M, Hahn S, Gustafsson L, Henshaw I, Träff J, Král M, Adamík P. 2016. Breeding latitude leads to different temporal but not spatial organization of the annual cycle in a long-distance migrant. J. Avian Biol. 47, 743–748. (10.1111/jav.01002) DOI
Liechti F, et al. 2015. Timing of migration and residence areas during the non-breeding period of barn swallows Hirundo rustica in relation to sex and population. J. Avian Biol. 46, 254–265. (10.1111/jav.00485) DOI
Koleček J, et al. 2016. Cross-continental migratory connectivity and spatiotemporal migratory patterns in the great reed warbler. J. Avian Biol. 47, 756–767. (10.1111/jav.00929) DOI
Gow EA, et al. 2019. A range-wide domino effect and resetting of the annual cycle in a migratory songbird. Proc. R. Soc. B 286, 20181916 (10.1098/rspb.2018.1916) PubMed DOI PMC
Marra PP, Cohen EB, Loss SR, Rutter JE, Tonra CM. 2015. A call for full annual cycle research in animal ecology. Biol. Lett. 11, 20150552 (10.1098/rsbl.2015.0552) PubMed DOI PMC
Coppack T, Pulido F. 2009. Proximate control and adaptive potential of protandrous migration in birds. Integr. Comp. Biol. 49, 493–506. (10.1093/icb/icp029) PubMed DOI
Bäckman J, Andersson A, Pedersen L, Sjöberg S, Tøttrup AP, Alerstam T. 2017. Actogram analysis of free-flying migratory birds: new perspectives based on acceleration logging. J. Comp. Physiol. A 203, 543–564. (10.1007/s00359-017-1165-9) PubMed DOI PMC
Pakanen VM, Jaakkonen T, Saarinen J, Rönkä N, Thomson RL, Koivula K. 2018. Migration strategies of the Baltic dunlin: rapid jump migration in the autumn but slower skipping type spring migration. J. Avian Biol. 49, e01513 (10.1111/jav.01513) DOI
Buechley ER, McGrady MJ, Çoban E, Şekercioğlu ÇH. 2018. Satellite tracking a wide-ranging endangered vulture species to target conservation actions in the Middle East and East Africa. Biodivers. Conserv. 27, 2293–2310. (10.1007/s10531-018-1538-6) DOI
Rotics S, et al. 2018. Early arrival at breeding grounds: causes, costs and a trade-off with overwintering latitude. J. Anim. Ecol. 87, 1627–1638. (10.1111/1365-2656.12898) PubMed DOI
Piersma T. 1987. Hop, skip, or jump? Constraints on migration of Arctic waders by feeding, fattening, and flight speed. Limosa 60, 185–194.
Thorup K, et al. 2017. Resource tracking within and across continents in long-distance bird migrants. Sci. Adv. 3, e1601360 (10.1126/sciadv.1601360) PubMed DOI PMC
Rodríguez-Ruiz J, De La Puente J, Parejo D, Valera F, Calero-Torralbo MA, Reyes-González JM, Zajková Z, Bermejo A, Avilés JM. 2014. Disentangling migratory routes and wintering grounds of Iberian near-threatened European rollers Coracias garrulus. PLoS ONE 9, 1–19. (10.1371/journal.pone.0115615) PubMed DOI PMC
Briedis M, Hahn S, Adamík P. 2017. Cold spell en route delays spring arrival and decreases apparent survival in a long-distance migratory songbird. BMC Ecol. 17, 11 (10.1186/s12898-017-0121-4) PubMed DOI PMC
Alerstam T. 2003. Bird migration speed. In Avian migration (eds Berthold P, Gwinner E, Sonnenschein E), pp. 253–267. Berlin, Germany: Springer.
Lisovski S, et al. 2018. Inherent limits of light-level geolocation may lead to over-interpretation. Curr. Biol. 28, R99–R100. (10.1016/j.cub.2017.11.072) PubMed DOI
Cramp S, Simmons K.. 2006. Birds of the western Palearctic interactive (ver. 2.0). Totnes, UK: Gostours.
Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO. 2012. The global diversity of birds in space and time. Nature 491, 444–448. (10.1038/nature11631) PubMed DOI
R Core Team. 2018. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. (10.18637/jss.v067.i01) DOI
Kuznetsova A, Brockhoff PB, Christensen RHB. 2017. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26. (10.18637/jss.v082.i13) DOI
Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22. (10.1002/ana.22635) PubMed DOI
Tøttrup AP, et al. 2012. The annual cycle of a trans-equatorial Eurasian-African passerine migrant: different spatio-temporal strategies for autumn and spring migration. Proc. R. Soc. B 279, 1008–1016. (10.1098/rspb.2011.1323) PubMed DOI PMC
Briedis M, Hahn S, Krist M, Adamík P. 2018. Finish with a sprint: evidence for time-selected last leg of migration in a long-distance migratory songbird. Ecol. Evol. 8, 6899–6908. (10.1002/ece3.4206) PubMed DOI PMC
Maggini I, Bairlein F. 2012. Innate sex differences in the timing of spring migration in a songbird. PLoS ONE 7, e31271 (10.1371/journal.pone.0031271) PubMed DOI PMC
Lehikoinen A, Santaharju J, Pape Møller A. 2017. Sex-specific timing of autumn migration in birds: The role of sexual size dimorphism, migration distance and differences in breeding investment. Ornis Fenn. 94, 53–65.
Scandolara C, et al. 2014. Impact of miniaturized geolocators on barn swallow Hirundo rustica fitness traits. J. Avian Biol. 45, 417–423. (10.1111/jav.00412) DOI
Brlík V. et al. Accepted Weak effects of geolocators on small birds: a meta-analysis controlled for phylogeny and publication bias. J. Anim. Ecol. (10.1111/1365-2656.12962) PubMed DOI
Rushing CS, Marra PP, Dudash MR. 2016. Winter habitat quality but not long-distance dispersal influences apparent reproductive success in a migratory bird. Ecology 97, 1218–1227. (10.1890/15-1259.1/suppinfo) PubMed DOI
Borowske A, Gjerdrum C, Elphick C. 2017. Timing of migration and prebasic molt in tidal marsh sparrows with different breeding strategies: comparisons among sexes and species. Auk 134, 51–64. (10.1642/AUK-16-116.1) DOI
Flinks H, Helm B, Rothery P. 2008. Plasticity of moult and breeding schedules in migratory European stonechats Saxicola rubicola. Ibis 150, 687–697. (10.1111/j.1474-919X.2008.00833.x) DOI
Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S. 2011. Carry-over effects as drivers of fitness differences in animals. J. Anim. Ecol. 80, 4–18. (10.1111/j.1365-2656.2010.01740.x) PubMed DOI
Wiggins DA, Pärt T, Gustafsson L, Part T. 1994. Seasonal decline in collared flycatcher Ficedula albicollis reproductive success: an experimental approach. Oikos 70, 359 (10.2307/3545773) DOI
Saino N, Ambrosini R, Caprioli M, Romano A, Romano M, Rubolini D, Scandolara C, Liechti F. 2017. Sex-dependent carry-over effects on timing of reproduction and fecundity of a migratory bird. J. Anim. Ecol. 86, 239–249. (10.1111/1365-2656.12625) PubMed DOI
van Wijk RE, Schaub M, Bauer S. 2017. Dependencies in the timing of activities weaken over the annual cycle in a long-distance migratory bird. Behav. Ecol. Sociobiol. 71, 73 (10.1007/s00265-017-2305-5) DOI
Senner NR, Hochachka WM, Fox JW, Afanasyev V. 2014. An exception to the rule: carry-over effects do not accumulate in a long-distance migratory bird. PLoS ONE 9, e0086588 (10.1371/journal.pone.0086588) PubMed DOI PMC
Lerche-Jørgensen M, Korner-Nievergelt F, Tøttrup AP, Willemoes M, Thorup K. 2018. Early returning long-distance migrant males do pay a survival cost. Ecol. Evol. 8, 11 434–11 449. (10.1002/ece3.4569) PubMed DOI PMC
Briedis M, et al. 2019. Data from: A full annual perspective on sex-biased migration timing in long-distance migratory birds Dryad Digital Repository. (10.5061/dryad.t78400r) PubMed DOI PMC
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A full annual perspective on sex-biased migration timing in long-distance migratory birds