Autumn migratory departure is influenced by reproductive timing and weather in an Arctic passerine
Tóm tắt
Numerous studies of spring migration have discovered that environmental conditions experienced on the wintering grounds and/or during vernal migration itself can have “carry-over effects” altering timing or success of the subsequent breeding season. Few studies have evaluated whether breeding and pre-basic molt have carry-over effects on autumn migration. The aim of this study was to test the expectations that (1) at broad temporal scales carry-over effects from breeding and molt constrain migratory departure but that (2) at finer temporal scales local weather will further refine this decision. We monitored nests of Gambel’s white-crowned sparrows breeding in the low Arctic in Alaska over three years and used radio-telemetry to track autumn migratory departure. We found that reproductive timing and weather parameters, but not molt timing, contributed to variation in autumn departure from the breeding site. Birds that terminated parental care late in the summer departed from the breeding grounds late relative to other birds. Birds were more likely to leave on nights without precipitation, when barometric pressure was increasing, and when ground level south winds were prominent. We also observed that, on average, birds departed 2.5 h after sunset and shifted the hour of departure as sunset advanced over the migration season. Our findings, in conjunction with observations of migration from earlier studies, raise the possibility that global climate change may be delaying autumn migratory departure in Gambel’s white-crowned sparrows breeding in Alaska.
Tài liệu tham khảo
Agatsuma R, Ramenofsky M (2006) Migratory behaviour of captive white-crowned sparrows, Zonotrichia leucophrys gambelii, differs during autumn and spring migration. Behaviour 143:1219–1240
Alerstam T, Chapman JW, Bäckman J, Smith AD, Karlsson H, Nilsson C, Reynolds DR, Klaassen RHG, Hill JK (2011) Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds. Proc R Soc B 278(1721):3074–3080. https://doi.org/10.1098/rspb.2011.0058
Bates D (2004) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-6
Boelman NT, Krause JS, Sweet SK, Chmura HE, Perez JH, Gough L, Wingfield JC (2017) Extreme spring conditions in the Arctic delay spring phenology of long-distance migratory songbirds. Oecologia 185(1):69–80. https://doi.org/10.1007/s00442-017-3907-3
Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20:243–248. https://doi.org/10.1016/j.cub.2009.11.074
Both C, te Marvelde L (2007) Climate change and timing of avian breeding and migration throughout Europe. Clim Res 35:93–105. https://doi.org/10.3354/cr00716
Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298. https://doi.org/10.1038/35077063
Breuner CW, Sprague RS, Patterson SH, Woods HA (2013) Environment, behavior and physiology: do birds use barometric pressure to predict storms? J Exp Biol 216:1982–1990. https://doi.org/10.1242/jeb.081067
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(6):743–748. https://doi.org/10.1111/jav.01002
Briedis M, Krist M, Kral M, Voigt CC, Adamik P (2018) Linking events throughout the annual cycle in a migratory bird-non-breeding period buffers accumulation of carry-over effects. Behav Ecol Sociobiol. 72(6). doi:10.1007/s00265-018-2509-3.
Catry P, Dias MP, Phillips RA, Granadeiro JP (2013) Carry-over effects from breeding modulate the annual cycle of a long-distance migrant: an experimental demonstration. Ecology 94:1230–1235
Chahad-Ehlers S, Lozovei AL, Marques MD (2007) Reproductive and post-embryonic daily rhythm patterns of the malaria vector Anopheles (Kerteszia) cruzii: aspects of the life cycle. Chronobiol Int 24(2):289–304. https://doi.org/10.1080/07420520701282174
Chilton G, Baker MC, Barrentine CD, Cunninghan MA (1995) White-crowned Sparrow (Zonotrichialeucophrys). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. Retrieved from The Birds of North America: https://birdsna.org
Chmura HE, Krause JS, Pérez JH, Asmus A, Sweet SK, Hunt KE, Meddle SL, McElreath R, Boelman NT, Gough L et al (2018) Late-season snowfall is associated with decreased offspring survival in two migratory arctic-breeding songbird species. J Avian Biol 49(9):e01712. https://doi.org/10.1111/jav.01712
Chmura HE, Kharouba HM, Ashander J, Ehlman SM, Rivest EB, Yang LH (2019) The mechanisms of phenology: the patterns and processes of phenological shifts. Ecol Monogr 89(1):e01337. https://doi.org/10.1002/ecm.1337
Cochran WW, Mouritsen H, Wikelski M (2004) Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304(5669):405. https://doi.org/10.1126/science.1095844
Cooper NW, Sherry TW, Marra pp. (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, Bairlein F (2011) Circadian control of nocturnal songbird migration. J Ornithol 152:67–73. https://doi.org/10.1007/s10336-011-0708-z
Coppack T, Becker SF, Becker PJJ (2008) Circadian flight schedules in night-migrating birds caught on migration. Biol Lett. https://doi.org/10.1098/rsbl.2008.0388
Coverdill AJ, Bentley GE, Ramenofsky M (2008) Circadian and masking control of migratory restlessness in Gambel’s white-crowned sparrow (Zonotrichia leucophrysgambelii). J Biol Rhythms 23:59–68. https://doi.org/10.1177/0748730407311456
Davison AC, Hinkley DV (1997) Bootstrap methods and their applications. Cambridge University Press, Cambridge
de Zwaan DR, Wilson S, Gow EA, Martin K (2019) Sex-specific spatiotemporal variation and carry-over effects in a migratory alpine songbird. Front Ecol Evol. https://doi.org/10.3389/fevo.2019.00285
DeWolfe BB (1967) Biology of white-crowned sparrows in late summer at College Alaska. Condor 69:110–132. https://doi.org/10.2307/1366602
Dietz MW, Rogers KG, Piersma T (2013) When the seasons don’t fit: speedy molt as a routine carry-over cost of reproduction. PLoS ONE. https://doi.org/10.1371/journal.pone.0053890
Environmental Data Center Team (2017) Meteorological monitoring program at Toolik, Alaska. Toolik Field Station, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK 99775. https://toolik.alaska.edu/edc/abiotic_monitoring/data_query.php.
Erni B, Liechti F, Underhill LG, Bruderer B (2002) Wind and rain govern the intensity of nocturnal bird migration in central Europe - a log-linear regression analysis. Ardea. 90.
Erni B, Bonnevie BT, Oschadleus HD, Altwegg R, Underhill LG (2013) moult: an R package to analyze moult in birds. J Stat Softw 52:1–23
Euskirchen ES, Bret-Harte MS, Scott GJ, Edgar C, Shaver GR (2012) Seasonal patterns of carbon dioxide and water fluxes in three representative tundra ecosystems in northern Alaska. Ecosphere 3:1–19. https://doi.org/10.1890/ES11-00202.1
Fayet AL, Freeman R, Shoji A, Kirk HL, Padget O, Perrins CM, Guilford T (2016) Carry-over effects on the annual cycle of a migratory seabird: an experimental study. J Anim Ecol 85:1516–1527. https://doi.org/10.1111/1365-2656.12580
Flinks H, Helm B, Rothery P (2008) Plasticity of moult and breeding schedules in migratory European Stonechats Saxicola rubicola. Ibis 150:687–697. https://doi.org/10.1111/j.1474-919X.2008.00833.x
Gallinat AS, Primack RB, Wagner DL (2015) Autumn, the neglected season in climate change research. Trends Ecol Evol 30:169–176. https://doi.org/10.1016/j.tree.2015.01.004
Ge QS, Wang HJ, Rutishauser T, Dai JH (2015) Phenological response to climate change in China: a meta-analysis. Glob Change Biol 21:265–274. https://doi.org/10.1111/gcb.12648
Gill JA, Alves JA, Sutherland WJ, Appleton GF, Potts PM, Gunnarsson TG (2014) Why is timing of bird migration advancing when individuals are not? Proc R Soc B 281:6. https://doi.org/10.1098/rspb.2013.2161
Gow EA, Burke L, Winkler DW, Knight SM, Bradley DW, Clark RG, Bélisle M, Berzins LL, Blake T, Bridge ES et al (2019) A range-wide domino effect and resetting of the annual cycle in a migratory songbird. Proc R Soc B 286(1894):20181916. https://doi.org/10.1098/rspb.2018.1916
Gwinner E (1996a) Circadian and circannual programmes in avian migration. J Exp Biol 199:39–48
Gwinner E (1996b) Circannual clocks in avian reproduction and migration. Ibis 138:47–63. https://doi.org/10.1111/j.1474-919X.1996.tb04312.x
Hall KSS, Fransson T (2001) Wing moult in relation to autumn migration in adult common whitethroats Sylvia communis communis. Ibis 143:580–586. https://doi.org/10.1111/j.1474-919X.2001.tb04885.x
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
Hemborg C, Sanz JJ, Lundberg A (2001) Effects of latitude on the trade-off between reproduction and moult: a long-term study with pied flycatcher. Oecologia 129:206–212. https://doi.org/10.1007/s004420100710
Jenni L, Kéry M (2003) Timing of autumn bird migration under climate change: advances in long–distance migrants, delays in short–distance migrants. Proc R Soc B 270:1467–1471. https://doi.org/10.1098/rspb.2003.2394
Jonzén N, Linden A, Ergon T, Knudsen E, Vik JO, Rubolini D, Piacentini D, Brinch C, Spina F, Karlsson L et al (2006) Rapid advance of spring arrival dates in long-distance migratory birds. Science 312:1959–1961. https://doi.org/10.1126/science.1126119
Jonzén N, Linden A, Ergon T, Knudsen E, Vik JO, Rubolini D, Piacentini D, Brinch C, Spina F, Karlsson L et al (2007) Response to comment on ‘Rapid advance of spring arrival dates in long-distance migratory birds’. Science 315:1. https://doi.org/10.1126/science.1136920
Karlsson H, Nilsson C, Backman J, Alerstam T (2011) Nocturnal passerine migration without tailwind assistance. Ibis 153:485–493
Kerlinger P (1995) How birds migrate. Stackpole, Michigan
King JR, Farner DS (1965) Studies of fat deposition in migratory birds. Ann N Y Acad Sci 131:422–440. https://doi.org/10.1111/j.1749-6632.1965.tb34808.x
Knudsen E, Linden A, Both C, Jonzen N, Pulido F, Saino N, Sutherland WJ, Bach LA, Coppack T, Ergon T et al (2011) Challenging claims in the study of migratory birds and climate change. Biol Rev 86:928–946. https://doi.org/10.1111/j.1469-185X.2011.00179.x
Kumar V, Wingfield JC, Dawson A, Ramenofsky M, Rani S, Bartell P (2010) Biological clocks and regulation of seasonal reproduction and migration in birds. Physiol Biochem Zool Ecol Evol Appl 83(5):827–835. https://doi.org/10.1086/652243
Legagneux P, Fast PLF, Gauthier G, Bety J (2012) Manipulating individual state during migration provides evidence for carry-over effects modulated by environmental conditions. Proc R Soc B 279:876–883. https://doi.org/10.1098/rspb.2011.1351
Liechti F (2006) Birds: blowin’ by the wind? J Ornithol. https://doi.org/10.1007/s10336-006-0061-9
Liechti F, Bruderer B (1998) The relevance of wind for optimal migration theory. J Avian Biol 29(4):561–568. https://doi.org/10.2307/3677176
Lisovski S, Németh Z, Wingfield JC, Krause JS, Hobson KA, Seavy NE, Gee J, Ramenofsky M (2019) Migration pattern of Gambel’s white-crowned sparrow along the Pacific Flyway. J Ornithol. https://doi.org/10.1007/s10336-019-01685-4
Lourenco PM, Kentie R, Schroeder J, Groen NM, Hooijmeijer JCEW, Piersma T (2011) Repeatable timing of northward departure, arrival and breeding in Black-tailed Godwits Limosa l. limosa, but no domino effects. J Ornithol 152(4):1023–1032. doi:10.1007/s10336-011-0692-3
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. https://doi.org/10.1126/science.282.5395.1884
McCabe JD, Olsen BJ, Osti B, Koons PO (2017) The influence of wind selectivity on migratory behavioral strategies. Behav Ecol 29(1):160–168. https://doi.org/10.1093/beheco/arx141
McKinnon EA, Stanley CQ, Stutchbury BJM (2015) Carry-over effects of nonbreeding habitat on start-to-finish spring migration performance of a songbird. PLoS ONE 10:17. https://doi.org/10.1371/journal.pone.0141580
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
Metcalfe J, Schmidt KL, Bezner Kerr W, Guglielmo CG, MacDougall-Shackleton SA (2013) White-throated sparrows adjust behaviour in response to manipulations of barometric pressure and temperature. Anim Behav. https://doi.org/10.1016/j.anbehav.2013.09.033
Mills AM (2005) Changes in the timing of spring and autumn migration in North American migrant passerines during a period of global warming. Ibis 147:259–269. https://doi.org/10.1111/j.1474-919X.2005.00380.x
Mitchell GW, Newman AEM, Wikelski M, Norris DR (2012a) Timing of breeding carries over to influence migratory departure in a songbird: an automated radiotracking study. J Anim Ecol 81:1024–1033. https://doi.org/10.1111/j.1365-2656.2012.01978.x
Mitchell GW, Wheelwright NT, Guglielmo CG, Norris DR (2012b) Short- and long-term costs of reproduction in a migratory songbird. Ibis 154:325–337. https://doi.org/10.1111/j.1474-919X.2012.01212.x
Moore FR (1987) Sunset and the orientation behaviour of migrating birds. Biol Rev 62:65–86. https://doi.org/10.1111/j.1469-185X.1987.tb00626.x
Moore MC, Donham RS, Farner DS (1982) Physiological preparation for autumnal migration in white-crowned sparrows. Condor 84:410–419. https://doi.org/10.2307/1367445
Morton ML, King JR, Farner DS (1969) Postnuptial and postjuvenile molt in white-crowned sparrows in Central Alaska. Condor 71:376–385. https://doi.org/10.2307/1365736
Morton ML, Orejuela JE, Budd SM (1972) The biology of immature mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) on the breeding ground. Condor 74:423–430. https://doi.org/10.2307/1365894
Morton ML, Wakamatsu MW, Pereyra ME, Morton GA (1991) Postfledging dispersal, habitat imprinting, and philopatry in a montane, migratory sparrow. Ornis Scan 22:98–106. https://doi.org/10.2307/3676540
Müller F, Taylor PD, Sjöberg S, Muheim R, Tsvey A, Mackenzie SA, Schmaljohann H (2016) Towards a conceptual framework for explaining variation in nocturnal departure time of songbird migrants. Mov Ecol 4:24. https://doi.org/10.1186/s40462-016-0089-2
Newton I (1966) Moult of bullfinch Pyrrhula pyrrhula. Ibis 108:41–67. https://doi.org/10.1111/j.1474-919X.1966.tb07251.x
Newton I (2006) Can conditions experienced during migration limit the population levels of birds? J Ornithol 147:146–166. https://doi.org/10.1007/s10336-006-0058-4
Nilsson C, Bäckman J, Alerstam T (2014) Seasonal modulation of flight speed among nocturnal passerine migrants: differences between short- and long-distance migrants. Behav Ecol Sociobiol 68:1799–1807. https://doi.org/10.1007/s00265-014-1789-5
Nilsson C, Backman J, Karlsson H, Alerstam T (2015) Timing of nocturnal passerine migration in Arctic light conditions. Polar Biol 38:1453–1459. https://doi.org/10.1007/s00300-015-1708-x
Norment CJ (1992) Comparative breeding biology of Harris’ sparrows and Gambel’s white-crowned sparrows in the northwest territories, Canada. Condor 94:955–975. https://doi.org/10.2307/1369292
Norris DR, Marra PP, Kyser TK, Sherry TW, Ratcliffe LM (2004) Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proc R Soc Lond B. https://doi.org/10.1098/rspb.2003.2569
Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872. https://doi.org/10.1111/j.1365-2486.2007.01404.x
Pérez JH, Krause JS, Chmura HE, Bowman S, McGuigan M, Asmus AL, Meddle SL, Hunt KE, Gough L, Boelman NT et al (2016) Nestling growth rates in relation to food abundance and weather in the Arctic. Auk 133(2):261–272
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing
Ramenofsky M (2011) Hormones in migration and reproductive cycles of birds. In: Norris DR, Lopez KH (eds) Hormones and reproduction of vertebrates, vol 4. Academic Press, London, pp 205–236
Ramenofsky M, Nemeth Z (2014) Regulatory mechanisms for the development of the migratory phenotype: Roles for photoperiod and the gonad. Horm Behav 66:148–158. https://doi.org/10.1016/j.yhbeh.2014.04.012
Ramenofsky M, Agatsuma R, Ramfar T (2008) Environmental conditions affect the behavior of captive, migratory white-crowned sparrows. Condor 110(4):658–671. https://doi.org/10.1525/cond.2008.8523
Ramenofsky M, Campion AW, Pérez JH, Krause JS, Németh Z (2017) Behavioral and physiological traits of migrant and resident White-crowned Sparrows: a common garden approach. J Exp Biol. https://doi.org/10.1242/jeb.148171
Rani S, Singh S, Misra M, Malik S, Singh BP, Kumar V (2005) Daily light regulates seasonal responses in the migratory male redheaded bunting (Emberiza bruniceps). J Exp Zool Part A 303A(7):541–550. https://doi.org/10.1002/jez.a.187
Refinetti R, Cornelissen G, Halberg F (2007) Procedures for numerical analysis of circadian rhythms. Biol Rhythm Res 38(4):275–325. https://doi.org/10.1080/09291010600903692
Richardson WJ (1978) Timing and amount of bird migration in relation to weather: a review. Oikos. https://doi.org/10.2307/3543482
Richardson WJ (1990) Timing of bird migration in relation to weather: updated review. In: Gwinner E (ed) Bird migration. Springer, Berlin
Rockwell SM, Bocetti CI, Marra pp. (2012) Carry-over effects of winter climate on spring arrival date and reproductive success in an endangered migratory bird, Kirtland’s warbler (Setophaga kirtlandii). Auk 129:744–752. https://doi.org/10.1525/auk.2012.12003
Saino N, Romano M, Rubolini D, Ambrosini R, Romano A, Caprioli M, Costanzo A, Bazzi G (2014) A trade-off between reproduction and feather growth in the barn swallow (Hirundo rustica). PLoS ONE. https://doi.org/10.1371/journal.pone.0096428
Saino N, Ambrosini R, Albetti B, Caprioli M, De Giorgio B, Gatti E, Liechti F, Parolini M, Romano A, Romano M et al (2017) Migration phenology and breeding success are predicted by methylation of a photoperiodic gene in the barn swallow. Sci Rep. https://doi.org/10.1038/srep45412
Schaub M, Liechti F, Jenni L (2004) Departure of migrating European robins, Erithacus rubecula, from a stopover site in relation to wind and rain. Anim Behav 67:229–237. https://doi.org/10.1016/j.anbehav.2003.03.011
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
Senner NR, Verhoeven MA, Abad-Gómez JM, Alves JA, Hooijmeijer JCEW, Howison RA, Kentie R, Loonstra AHJ, Masero JA, Rocha A et al (2019) High migratory survival and highly variable migratory behavior in black-tailed godwits. Front Ecol Evol 7:96. https://doi.org/10.3389/fevo.2019.00096
Shamoun-Baranes J, Liechti F, Vansteelant WMG (2017) Atmospheric conditions create freeways, detours and tailbacks for migrating birds. J Comp Physiol A 203(6):509–529. https://doi.org/10.1007/s00359-017-1181-9
Singer HV, Sedinger JS, Nicolai CA, Van Dellen AW, Person BT (2012) Timing of adult remigial wing molt in female black brant (Branta bernicla nigricans). Auk 129:239–246. https://doi.org/10.1525/auk.2012.11180
Sjöberg S, Alerstam T, Åkesson S, Muheim R (2017) Ecological factors influence timing of departures in nocturnally migrating songbirds at Falsterbo, Sweden. Anim Behav 127:253–269. https://doi.org/10.1016/j.anbehav.2017.03.007
Stutchbury BJM, Gow EA, Done T, MacPherson M, Fox JW, Afanasyev V (2011) Effects of post-breeding moult and energetic condition on timing of songbird migration into the tropics. Proc R Soc B 278(1702):131–137. https://doi.org/10.1098/rspb.2010.1220
Thackeray SJ, Sparks TH, Frederiksen M, Burthe S, Bacon PJ, Bell JR, Botham MS, Brereton TM, Bright PW, Carvalho L et al (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313. https://doi.org/10.1111/j.1365-2486.2010.02165.x
Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Springer, New York
Thorup K, Tøttrup AP, Rahbek C (2007) Patterns of phenological changes in migratory birds. Oecologia 151:697–703. https://doi.org/10.1007/s00442-006-0608-8
Tomotani BM, Gienapp P, Beersma DGM, Visser ME (2016) Climate change relaxes the time constraints for late-born offspring in a long-distance migrant. Proc R Soc B 283:8. https://doi.org/10.1098/rspb.2016.1366
Tottrup AP, Thorup K, Rahbek C (2006) Changes in timing of autumn migration in North European songbird populations. Ardea 94:527–536
Underhill LG, Zucchini W, Summers RW (1990) A model for avian primary moult-data types based on migration strategies and an example using the Redshank Tringa totanus. Ibis 132:118–123. https://doi.org/10.1111/j.1474-919X.1990.tb01024.x
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. https://doi.org/10.1111/j.1365-2486.2008.01751.x
Watts HE, Cornelius JM, Fudickar AM, Pérez J, Ramenofsky M (2018) Understanding variation in migratory movements: a mechanistic approach. Gen Comp Endocrinol 256:112–122. https://doi.org/10.1016/j.ygcen.2017.07.027
Wingfield JC (2008) Organization of vertebrate annual cycles: implications for control mechanisms. Philos Trans R Soc B 363:425–441. https://doi.org/10.1098/rstb.2007.2149
Wingfield JC, Farner DS (1979) Some endocrine correlates of renesting after loss of clutch or brood in the white-crowned sparrow, Zonotrichia leucophrys gambelii. Gen Comp Endocrinol 38:322–331. https://doi.org/10.1016/0016-6480(79)90066-2
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York