Abstract
Protandry, the earlier arrival of males at the breeding grounds relative to females, is common in migratory birds. However, due to difficulties in following individual birds on migration, we still lack knowledge about the spatiotemporal origin of protandry during the annual cycle, impeding our understanding of the proximate drivers of this phenomenon. Here, we use full annual cycle tracking data of red-backed shrikes Lanius collurio to investigate the occurrence of sex-related differences in migratory pattern, which could be viewed as precursors (proximate causes) to protandry. We find protandry with males arriving an estimated 8.3 days (SE = 4.1) earlier at the breeding area than females. Furthermore, we find that, averaged across all departure and arrival events throughout the annual cycle, males migrate an estimated 5.3 days earlier than females during spring compared to 0.01 days in autumn. Event-wise estimates suggest that a divergence between male and female migratory schedules is initiated at departure from the main non-breeding area, thousands of kilometres from-, and several months prior to arrival at the breeding area. Duration of migration, flight speed during migration and spatial locations of stationary sites were similar between sexes. Our results reveal that protandry might arise from sex-differential migratory schedules emerging at the departure from the main non-breeding area in southern Africa and retained throughout spring migration, supporting the view that sex-differential selection pressure operates during spring migration rather than autumn migration.
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References
Alerstam T (2003) Bird migration speed. In: Berthold P et al (eds) Avian migration. Springer, Berlin, pp 253–267
Alerstam T, Lindström Å (1990) Optimal bird migration: the relative importance of time, energy, and safety. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 331–351
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Bazzi G, Ambrosini R, Caprioli M, Costanzo A, Liechti F, Gatti E, Gianfranceschi L, Podofillini S, Romano A, Romano M, Scandolara C, Saino N, Rubolini D (2015) Clock gene polymorphism and scheduling of migration: a geolocator study of the barn swallow Hirundo rustica. Sci Rep 5:12443. https://doi.org/10.1038/srep12443
Berthold P (2001) Bird migration: a general survey, 2nd edn. Oxford University Press, Oxford
Both C, Bijlsma RG, Ouwehand J (2016) Repeatability in spring arrival dates in pied flycatchers varies among years and sexes. Ardea 104:3–21. https://doi.org/10.5253/arde.v104i1.a1
Bridge ES, Thorup K, Bowlin MS, Chilson PB, Diehl RH, Fléron RW, Hartl P, Kays R, Kelly JF, Robinson WD, Wikelski M (2011) Technology on the move: recent and forthcoming innovations for tracking migratory birds. Am Inst Biol Sci 61:689–698. https://doi.org/10.1525/bio.2011.61.9.7
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. https://doi.org/10.1111/jav.01002
Briedis M, Bauer S, Adamík P, Alves JA, Costa JS, Emmenegger T, Gustafsson L, Koleček J, Liechti F, Meier CM, Petr Procházka P, Hahn S (2019) A full annual perspective on sex-biased migration timing in long-distance migratory birds. Proc R Soc B 286:20182821. https://doi.org/10.1098/rspb.2018.2821
Bruderer B, Bruderer H (1994) Numbers of red-backed shrikes Lanius collurio in different habitats of South Africa. Bull Br Ornithol Club 114:192–202
Bulmer MG (1983) Models for the evolution of protandry in insects. Theor Popul Biol 23:314–322. https://doi.org/10.1016/0040-5809(83)90021-7
Chandler CR, Mulvihill RS (1992) Effects of age, sex, and fat level on wing loading in dark-eyed juncos. Auk 109:235–241. https://doi.org/10.2307/4088191
Conklin JR, Battley PF, Potter MA (2013) Absolute consistency: individual versus population variation in annual-cycle schedules of a long-distance migrant bird. PLoS One 8:e54535. https://doi.org/10.1371/journal.pone.0054535
Cooper NW, Sherry TW, Marra PP, Inouye BD (2015) Experimental reduction of winter food decreases body condition and delays migration in a long-distance migratory bird. Ecology 96:1933–1942. https://doi.org/10.1890/14-1365.1
Coppack T, Pulido F (2009) Proximate control and adaptive potential of protandrous migration in birds. Integr Comp Biol 49:493–506. https://doi.org/10.1093/icb/icp029
Coppack T, Tøttrup AP, Spottiswoode C (2006) Degree of protandry reflects level of extrapair paternity in migratory songbirds. J Ornithol 147:260–265. https://doi.org/10.1007/s10336-006-0067-3
Deakin JE, Guglielmo CG, Morbey YE (2019) Sex differences in migratory restlessness behavior in a Nearctic–Neotropical songbird. Auk. https://doi.org/10.1093/auk/ukz017
Dierschke V, Mendel B, Schmaljohann H (2005) Differential timing of spring migration in northern wheatears Oenanthe oenanthe: hurried males or weak females? Behav Ecol Sociobiol 57:470–480. https://doi.org/10.1007/s00265-004-0872-8
Fagerström T, Wiklund C (1982) Why do males emerge before females? Protandry as a mating strategy in male and female butterflies. Oecologia 52:164–166. https://doi.org/10.1007/BF00363830
Francis CM, Cooke F (1986) Differential timing of spring migration in wood warblers (parulinae). Auk 103:548–556. https://doi.org/10.1093/auk/103.3.548
Fudickar AM, Wikelski M, Partecke J (2012) Tracking migratory songbirds: accuracy of light-level loggers (geolocators) in forest habitats. Methods Ecol Evol 3:47–52. https://doi.org/10.1111/j.2041-210X.2011.00136.x
Gienapp P, Bregnballe T (2012) Fitness consequences of timing of migration and breeding in cormorants. PLoS One 7:e46165. https://doi.org/10.1371/journal.pone.0046165
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. https://doi.org/10.1111/j.1365-2656.2010.01740.x
Hedenström A (2008) Adaptations to migration in birds: behavioural strategies, morphology and scaling effects. Philos Trans R Soc Lond Ser B Biol Sci 363:287–299. https://doi.org/10.1098/rstb.2007.2140
Hedenström A, Pettersson J (1986) Differences in fat deposits and wing pointedness between male and female willow warblers caught on spring migration at Ottenby, SE Sweden. Ornis Scand 17:182–185. https://doi.org/10.2307/3676868
Herremans M (1997) Habitat segregation of male and female red-backed shrikes Lanius collurio and lesser grey shrikes Lanius minor in the Kalahari basin, Botswana. J Avian Biol 28:240–248. https://doi.org/10.2307/3676975
Hijmans RJ (2016) Geosphere: spherical trigonometry. https://www.rdocumentation.org/packages/geosphere/versions/1.5-5. Accessed 24 October 2018
Hill GE (1989) Late spring arrival and dull nuptial plumage: aggression avoidance by yearling males? Anim Behav 37:665–673. https://doi.org/10.1016/0003-3472(89)90045-6
Jahn AE, Cueto VR, Fox JW, Husak MS, Kim DH, Landoll DV, Ledezma JP, LePage HK, Levey DJ, Murphy MT, Renfrew RB (2013) Migration timing and wintering areas of three species of flycatchers (Tyrannus) breeding in the Great Plains of North America. Auk 130:247–257. https://doi.org/10.1525/auk.2013.13010
Jakober H, Stauber W, Bairlein F, Voss M (2007) Analysis of stable isotopes in feathers of red-backed shrikes (Lanius collurio): no evidence for different wintering habitats of males and females. J Ornithol 148:129–131. https://doi.org/10.1007/s10336-006-0110-4
Kokko H (1999) Competition for early arrival birds in migratory birds. J Anim Ecol 68:940–950. https://doi.org/10.1046/j.1365-2656.1999.00343.x
Kokko H, Gunnarsson TG, Morrell LJ, Gill JA (2006) Why do female migratory birds arrive later than males? J Anim Ecol 75:1293–1303. https://doi.org/10.1111/j.1365-2656.2006.01151.x
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–26. https://doi.org/10.18637/jss.v082.i13
Lenth R (2019) Emmeans: estimated marginal means, aka least-squares means. https://CRAN.R-project.org/package=emmeans. Accessed 26 January 2019
Liechti F, Scandolara C, Rubolini D, Ambrosini R, Korner-Nievergelt F, Hahn S, Lardelli R, Romano M, Caprioli M, Romano A, Sicurella B, Saino N (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. https://doi.org/10.1111/jav.00485
Lindström Å, Alerstam T (1992) Optimal fat loads in migrating birds: a test of the time-minimization hypothesis. Am Nat 140:477–491. https://doi.org/10.1086/285422
Lindström Å, Alerstam T, Bahlenberg P, Ekblom R, Fox JW, Råghall J, Klaassen RHG (2016) The migration of the great snipe Gallinago media: intriguing variations on a grand theme. J Avian Biol 47:321–334. https://doi.org/10.1111/jav.00829
Lisovski S, Hahn S (2012) GeoLight—processing and analysing light-based geolocator data in R. Methods Ecol Evol 3:1055–1059. https://doi.org/10.1111/j.2041-210X.2012.00248.x
Lisovski S, Hewson CM, Klaassen RHG, Korner-Nievergelt F, Kristensen MW, Hahn S (2012) Geolocation by light: accuracy and precision affected by environmental factors. Methods Ecol Evol 3:603–612. https://doi.org/10.1111/j.2041-210X.2012.00185.x
Lozano GA, Perreault S, Lemon RE (1995) Age, arrival date and reproductive success of male American redstarts Setophaga ruticilla. J Avian Biol 27:164–170. https://doi.org/10.2307/3677146
Maggini I, Bairlein F (2012) Innate sex differences in the timing of spring migration in a songbird. PLoS One 7:e31271. https://doi.org/10.1371/journal.pone.0031271
McKinnon EZ, Love OP (2018) Ten years tracking the migrations of small landbirds: lessons learned in the golden age of bio-logging. Auk 135:834–856. https://doi.org/10.1642/AUK-17-202.1
Mckinnon EA, Fraser KC, Stanley CQ, Stutchbury BJM (2014) Tracking from the tropics reveals behaviour of juvenile songbirds on their first spring migration. PLoS One 9(8):e105605. https://doi.org/10.1371/journal.pone.0105605
McKinnon EA, Macdonald CM, Gilchrist HG, Love OP (2016) Spring and fall migration phenology of an Arctic-breeding passerine. J Ornithol 157:681–693. https://doi.org/10.1007/s10336-016-1333-7
McNamara JM, Welham RK, Houston AI (1998) The timing of migration within the context of an annual routine. J Avian Biol 29:416–423. https://doi.org/10.2307/3677160
Mills AM (2005) Protogyny in autumn migration: do male birds “play chicken”? Auk 122:71–81. https://doi.org/10.1642/0004-8038(2005)122[0071:PIAMDM]2.0.CO;2
Mitchell GW, Woodworth BK, Taylor PD, Norris DR (2015) Automated telemetry reveals age specific differences in flight duration and speed are driven by wind conditions in a migratory songbird. Mov Ecol 3:19. https://doi.org/10.1186/s40462-015-0046-5
Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673. https://doi.org/10.1046/j.1461-0248.2001.00265.x
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. https://doi.org/10.1007/s10336-012-0854-y
Naef-Daenzer B (2007) An allometric function to fit leg-loop harnesses to terrestrial birds. J Avian Biol 38:404–407. https://doi.org/10.1111/j.2007.0908-8857.03863.x
Newton I (2008) The migration ecology of birds. Elsevier-Academic Press, Amsterdam
Nilsson C, Klaassen RHG, Alerstam T (2013) Differences in speed and duration of bird migration between spring and autumn. Am Nat 181:837–845. https://doi.org/10.1086/670335
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. https://doi.org/10.1111/1365-2656.12599
Pedersen L, Fraser KC, Kyser TK, Tøttrup AP (2016) Combining direct and indirect tracking techniques to assess the impact of sub-Saharan conditions on cross-continental songbird migration. J Ornithol 157:1037–1047. https://doi.org/10.1007/s10336-016-1360-4
Pedersen L, Jackson K, Thorup K, Tøttrup AP (2018) Full-year tracking suggests endogenous control of migration timing in a long-distance migratory songbird. Behav Ecol Sociobiol 72:139. https://doi.org/10.1007/s00265-018-2553-z
Pedersen L, Jakobsen NM, Strandberg, R, Thorup K, Tøttrup AP (2019) Data from: sex-specific difference in migration schedule as a precursor of protandry in a long-distance migratory bird. Movebank Data Repository. https://doi.org/10.5441/001/1.j71640kh
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: Linear and Nonlinear Mixed Effects Models. https://CRAN.R-project.org/package=nlme. Accessed 26 January 2019
Potti J (1998) Arrival time from spring migration in male pied flycatchers: individual consistency and familial resemblance. Condor 100:702–708. https://doi.org/10.2307/1369752
R Core Team (2017) R: A language and environment for statistical computing. https://www.r-project.org. Accessed 24 October 2018
R Core Team (2018) R: A language and environment for statistical computing. https://www.r-project.org. Accessed 26 January 2019
Reudink MW, Marra PP, Kyser TK, Boag PT, Langin KM, Ratcliffe LM (2009) Non-breeding season events influence sexual selection in a long-distance migratory bird. Proc R Soc London B Biol Sci 276:1619–1626. https://doi.org/10.1098/rspb.2008.1452
Robinson WD, Bowlin MS, Bisson I, Shamoun-Baranes J, Thorup K, Diehl RH, Kunz TH, Mabey S, Winkler DW (2010) Integrating concepts and technologies to advance the study of bird migration. Front Ecol Environ 8:354–361. https://doi.org/10.1890/080179
Rubolini D, Spina F, Saino N (2004) Protandry and sexual dimorphism in trans-Saharan migratory birds. Behav Ecol 15:592–601. https://doi.org/10.1093/beheco/arh048
Saino N, Bazzi G, Gatti E, Caprioli M, Cecere JG, Possenti CD, Galimberti A, Orioli V, Bani L, Rubolini D, Gianfranceschi L, Spina F (2015) Polymorphism at the clock gene predicts phenology of long-distance migration in birds. Mol Ecol 24:1758–1773. https://doi.org/10.1890/080179
Schmaljohann H, Meier C, Arlt D, Bairlein F, van Oosten H, Morbey YE, Åkesson S, Buchmann M, Chernetsov N, Desaever R, Elliott J, Hellström M, Liechti F, López A, Middleton J, Ottosson U, Pärt T, Spina F, Eikenaar C (2016) Proximate causes of avian protandry differ between subspecies with contrasting migration challenges. Behav Ecol 27:321–331. https://doi.org/10.1093/beheco/arv160
Seewagen CL, Guglielmo CG, Morbey YE (2013) Stopover refueling rate underlies protandry and seasonal variation in migration timing of songbirds. Behav Ecol 24:634–642. https://doi.org/10.1093/beheco/ars225
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:e86588. https://doi.org/10.1371/journal.pone.0086588
Sergio F, Tanferna A, De Stephanis R, Jiménez LL, Blas J, Tavecchia G, Preatoni D, Hiraldo F (2014) Individual improvements and selective mortality shape lifelong migratory performance. Nature 515:410–413. https://doi.org/10.1038/nature13696
Smith RJ, Moore FR (2005) Arrival timing and seasonal reproductive performance in a long-distance migratory landbird. Behav Ecol Sociobiol 57:231–239. https://doi.org/10.1007/s00265-004-0855-9
Snow D, Perrins C (1998) The birds of the Western Palearctic, vol 2. Oxford University Press, New York
Stanley CQ, MacPherson M, Fraser KC, McKinnon EA, Stutchbury BJM (2012) Repeat tracking of individual songbirds reveals consistent migration timing but flexibility in route. PLoS One 7:e40688. https://doi.org/10.1371/journal.pone.0040688
Stewart RLM, Francis CM, Massey C (2002) Age-related differential timing of spring migration within sexes in passerines. Wilson Bull 114:264–271
Studds CE, Marra PP (2011) Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird. Proc R Soc B Biol Sci 278:3437–3443. https://doi.org/10.1098/rspb.2011.0332
Svensson L (1992) Identification guide to European passerines. British Trust Ornithol
Thorup K, Tøttrup AP, Willemoes M, Klaassen RHG, Strandberg R, Vega ML, Dasari HP, Araújo MB, Wikelski M, Rahbek C (2017) Resource tracking within and across continents in long-distance bird migrants. Sci Adv 3:e1601360. https://doi.org/10.1126/sciadv.1601360
Tøttrup AP, Thorup K (2008) Sex-differentiated migration patterns, protandry and phenology in North European songbird populations. J Ornithol 149:161–167. https://doi.org/10.1007/s10336-007-0254-x
Tøttrup AP, Klaassen R, Strandberg R, Thorup K, Kristensen MW, Jørgensen PS, Fox J, Afanasyev V, Rahbek C, Alerstam T (2012a) 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. https://doi.org/10.1098/rspb.2011.1323
Tøttrup AP, Klaassen RHG, Kristensen MW, Strandberg R, Vardanis Y, Lindström Å, Rahbek C, Alerstam T, Thorup K (2012b) Drought in Africa caused delayed arrival of European songbirds. Science 338:1307. https://doi.org/10.1126/science.1227548
Tøttrup AP, Pedersen L, Onrubia A, Klaassen RHG, Thorup K (2017) Migration of red-backed shrikes from the Iberian Peninsula: optimal or sub-optimal detour? J Avian Biol 48:149–154. https://doi.org/10.1111/jav.01352
Underhill LG, Brooks M (2016) SABAP2 after nine years, mid 2007–mid 2016: coverage progress and priorities for the Second Southern African Bird Atlas Project. Biodivers Obs 7:1–17 https://journals.uct.ac.za/index.php/BO/article/view/330. Accessed 24 October 2018
van Wijk RE, Schaub M, Bauer S (2016) Dependencies in the timing of activities weaken over the annual cycle in a long-distance migratory bird. Behav Ecol Sociobiol 71:73. https://doi.org/10.1007/s00265-017-2305-5
Wiklund C, Fagerström T (1977) Why do males emerge before females? A hypothesis to explain the incidence of protandry in butterflies. Oecologia 31:153–158. https://doi.org/10.1007/BF00346917
Woodworth BK, Newman AEM, Turbek SP, Bryant C, Hobson KA, Wassenaar LI, Mitchell GW, Nathaniel T, Norris DR (2016) Differential migration and the link between winter latitude, timing of migration, and breeding in a songbird. Oecologia 181:413–422. https://doi.org/10.1007/s00442-015-3527-8
Woodworth BK, Wheelwright NT, Newman AE, Schaub M, Norris DR (2017) Winter temperatures limit population growth rate of a migratory songbird. Nat Commun 8:14812. https://doi.org/10.1038/ncomms14812
Wotherspoon S, Sumner M, Lisovski S (2016) BAStag: basic data processing for British Antarctic Survey archival tags. https://github.com/SWotherspoon/BAStag. Accessed 24 October 2018
Wunderle JM, Lebow PK, White JD, Currie D (2014) Sex and age differences in site fidelity, food resource tracking, and body condition of wintering Kirtland’s warblers (Setophaga Kirtlandii) in the Bahamas. Ornithol Monogr 80:1–62. https://doi.org/10.1642/aoum.80-1
Acknowledgements
We thank P Ekberg, TE Ortvad, TL Petersen, PS Jørgensen, D Papageorgiou, DP Eskildsen, RHG Klaassen, Y Vardanis and M Ström-Eriksson for field assistance, H Sørensen and A Tolver for advice on statistical procedures and T Alerstam for advice and comments on the manuscript. We acknowledge the Aage V Jensen Foundation, as well as the Danish National Research Foundation, for supporting the Center for Macroecology, Evolution and Climate (Grant No. DNRF96). Capture and sampling methods were approved by the Copenhagen Bird Ringing Center with permission from the Danish Nature Agency (J.nr. SN 302-009). In Sweden, capture methods were approved by the Swedish Ringing Center with permission from the ethical committees in Malmö/Lund (M112-09).
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Pedersen, L., Jakobsen, N.M., Strandberg, R. et al. Sex-specific difference in migration schedule as a precursor of protandry in a long-distance migratory bird. Sci Nat 106, 45 (2019). https://doi.org/10.1007/s00114-019-1637-6
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DOI: https://doi.org/10.1007/s00114-019-1637-6