Abstract
Ecological processes are changing in response to climatic warming. Birds, in particular, have been documented to arrive and breed earlier in spring and this has been attributed to elevated spring temperatures. It is not clear, however, how long-distance migratory birds that overwinter thousands of kilometers to the south in the tropics cue into changes in temperature or plant phenology on northern breeding areas. We explored the relationships between the timing and rate of spring migration of long-distance migratory birds, and variables such as temperature, the North Atlantic Oscillation (NAO) and plant phenology, using mist net capture data from three ringing stations in North America over a 40-year period. Mean April/May temperatures in eastern North America varied over a 5°C range, but with no significant trend during this period. Similarly, we found few significant trends toward earlier median capture dates of birds. Median capture dates were not related to the NAO, but were inversely correlated to spring temperatures for almost all species. For every 1°C increase in spring temperature, median capture dates of migratory birds averaged, across species, one day earlier. Lilac (Syringa vulgaris) budburst, however, averaged 3 days earlier for every 1°C increase in spring temperature, suggesting that the impact of temperature on plant phenology is three times greater than on bird phenology. To address whether migratory birds adjust their rate of northward migration to changes in temperature, we compared median capture dates for 15 species between a ringing station on the Gulf Coast of Louisiana in the southern USA with two stations approximately 2,500 km to the north. The interval between median capture dates in Louisiana and at the other two ringing stations was inversely correlated with temperature, with an average interval of 22 days, that decreased by 0.8 days per 1°C increase in temperature. Our results suggest that, although the onset of migration may be determined endogenously, the timing of migration is flexible and can be adjusted in response to variation in weather and/or phenology along migration routes.
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References
Åkesson SG, Walinder L, Karlsson L, Ehnbom S (2002) Nocturnal migratory flight initiation in reed warblers Acrocephalus scirpaceus: effect of wind on orientation and timing of migration. J Avian Biol 33:349–357
Berthold P (1984) The endogenous control of bird migration: a survey of experimental evidence. Bird Study 31:19–27
Berthold P (1993) Bird migration. A general survey. Oxford University Press, Oxford
Berthold P (1996) Control of bird migration. Chapman and Hall, London
Berthold P, Querner U (1981) Genetic basis of migratory behavior in European warblers. Science 212:77–79
Berthold P, Terrill SB (1991) Recent advances in studies of bird migration. Annu Rev Syst 22:357-378
Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298
Bradley NL, Leopold AC, Ross J, Huffaker W (1999) Phenological changes reflect climate change in Wisconsin. Proc Natl Acad Sci USA 96:9701–9704
Brown JL, Li S-H, Bhagabati N (1999) Long-term trend toward earlier breeding in an American bird: a response to global warming? Proc Natl Acad Sci USA 96:5565–5569
Buse A, Good JEG (1996) Synchronization of larval emergence in winter moth (Operophtera brumata L.) and budburst in pedunculate oak (Quercus robur) under simulated climate change. Ecol Entomol 21:335–343
Crick HQP, Sparks TH (1999) Climate change related to egg-laying trends. Nature 399:423–424
Crick HQP, Dudley C, Glue DE, Thomson DL (1997) UK birds are laying eggs earlier. Nature 388:526
Dewer RC, Watt AD (1992) Predicted changes in the synchrony of larval emergence and budburst under climatic warming. Oecologia 89:557–559
Dunn EH (2000) Temporal and spatial patterns in daily mass gain of magnolia warblers during migration. Auk 117:12–21
Dunn PO, Winkler DW (1999) Climate change has affected the breeding date of tree swallows throughout North America. Proc R Soc Lond B 266:2487–2490
Easterling DR, Karl TR, Mason EH, Hughes PY, Bowman DP, Daniels RC, Boden TA (eds) (1997) United States Historical Climatology Network (USA HCN) Monthly Temperature and Precipitation Data. ORNL/CDIAC-87, NDP-019/R3. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, Oak Ridge
Elkins N (1993) Weather and bird behaviour, 2nd edn. Poyser, Calton
Francis CM, Hussell DJT (1998) Changes in numbers of land birds counted in migration at Long Point Bird Observatory, 1961–1997. Bird Popul 4:37–66
Gwinner E (1990) Circannual rhythms in bird migration: control of temporal patterns and interactions with photoperiod. In: Gwinner E (ed) Bird migration. Springer, Berlin Heidelberg New York, pp 257–268
Gwinner E, Biebach H, vonKries I (1985) Food availability affects migratory restlessness in caged Garden Warblers (Sylvia borin). Naturwissenschaften 72:51–52
Hagan JM, Lloyd-Evans TL, Atwood JL (1991) The relationship between latitude and the timing of spring migration of North American landbirds. Ornis Scand 22:129–136
Holmes RT, Sherry TW, Sturges FW (1986) Bird community dynamics in a temperate deciduous forest: long-term trends at Hubbard Brook. Ecol Monogr 56:201–220
Houghton JT, Meria Filho LG, Callender B, Harris N (eds) (1995) Intergovernmental Panel on Climate Change (IPCC). Climate change 1995: the science of climate change. Cambridge University Press, Cambridge
Huin N, Sparks TH (1998) Arrival and progression of the swallow Hirundo rustica through Britain. Bird Study 45:361–370
Huin N, Sparks TH (2000) Spring arrival patterns of the Cuckoo Cuculus canorus, Nightingale Luscina megarhynchos, and Spotted Flycatcher Musciapa striata in Britain. Bird Study 47:22–31
Hüppop O, Hüppop K (2003) North Atlantic Oscillation and the timing of spring migration in birds. Proc R Soc Lond B 270:233–240
Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proc Natl Acad Sci USA 97:1630–1633
Ivanauskas F, Nedzinskas V, Zalakevicius M (1997) The impact of global warming upon spring arrival of birds. Acta Zool Ornithol 6:31–36
Karasov WH, Pinshow B (1998) Changes in lean mass and in organs of nutrient assimilation in a long-distance migrant at a springtime stopover site. Physiol Biochem Zool 50:115–129
Kok OB, Van Ee CA, Nel DG (1990) Daylength determines departure date of the spotted flycatcher (Muscicapa striata) from its winter quarters. Ardea 79:63–66
Leberman RC, Clench MH (1972) Bird-ban ding at Powdermill, 1971, and ten years reviewed. Powdermill Nature Reserve Research Report No. 30. Carnegie Museum, Pittsburgh
Leberman RC, Wood D S (1983) Bird-banding at Powdermill: twenty years reviewed. Powdermill Nature Reserve Research Report No. 42. Carnegie Museum, Pittsburgh
Leberman RC, Mulvihill RS, Wood DS (1990) Bird-banding at Powdermill, 1988, including an analysis of banding effort for the period 1962–1988. Powdermill Nature Reserve Research Report No. 49. Carnegie Museum, Pittsburgh
Leberman RC, Mulvihill RS, Niedermeier M (1994) Bird-banding at Powdermill: 1991 and thirty years reviewed. Powdermill Nature Reserve Research Report No. 52. Carnegie Museum, Pittsburgh
Lindstrom A (1991) Maximum fat deposition rates in migrating birds. Ornis Scand 22:12–19
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
McCleery RH, Perrins CM (1998) Temperature and egg-laying trends. Nature 391:30–31
Moore FR, Kerlinger P (1987) Stopover and fat deposition by North American wood-warblers (Parulinae) following spring migration over the Gulf of Mexico. Oecologia 74:47–54
Moore FR, Simons TR (1992) Habitat suitability and stopover ecology of Neotropical landbird migrants. In: Hagan JM III, Johnston DW (eds) Ecology and conservation of neotropical migrant landbirds. Smithsonian Institution Press, Washington, pp 345–355
Parmesan C, Ryrholm N, Stefanescus C, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (2003) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 421:37–42
Penuelas J, Filella I (2001) Responses to a changing world. Science 294:793–795
Przyblo R, Sheldon BC, Merila J (2000) Climatic effects on breeding and morphology: evidence for phenotypic plasticity. J Anim Ecol 69:395–403
Pulida F, Berthold P, Moh G, Querner U (2001) Heritability of the timing of autumn migration in a natural bird population. Proc Soc R Lond B 268:885–993
Richardson WJ (1978) Timing and the amount of bird migration in relation to we ather: a review. Oikos 30:224–272
Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60
Saunders AA (1959) Forty years of spring migration in southern Connecticut. Wilson Bull 7:208–219
SAS Institute (1999) The SAS system for Windows, release 8.00. Cary, N.C.
Schaub M, Jenni L (2001) Variation of fuelling rates among sites, days and individuals in migrating passerine birds. Funct Ecol 15:584–594
Schwartz MD (1994) Monitoring global change with phenology: the case of the spring green wave. Int J Biometeorol 38:18-22
Schwartz MD (1998) Green-wave phenology. Nature 394:839–840
Sokolov LV, Markovets MY, Shapoval AP, Morozov YG (1998) Long-term trends in the timing of spring migration of passerines on the Courish Spit of the Baltic Sea. Avian Ecol Behav 1:1–21
Thomas CD, Lennon JJ (1999) Birds extend their ranges northwards. Nature 399:213
Thomas CD, Blondel J, Perret P, Lambrechts MM, speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600
Utech FH (1999) Checklist of the vascular plants of Powdermill Nature Reserve, Westmoreland County, Pennsylvania. Carnegie Museum of Natural History Special Publication No. 20. Carnegie Museum, Pittsburgh
Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Lond B 265:1867–1870
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-C, Hoegh-Guldberg O, Bairlein B (2002) Ecological responses to recent climate change. Nature 416:389–395
Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:76–82
Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH (2003) Costs of migration in free-flying songbirds. Nature 423:704
Yong W, Moore FR (1993) Relation between migratory activity and energetic condition among thrushes (Turdinae) following passage across the Gulf of Mexico. Condor 95:934–943
Yong W, Moore FR (1997) Spring stopover of intercontinental migratory thrushes along the northern coast of the Gulf of Mexico. Auk 114:263–278
Acknowledgements
We wish to thank the legions of volunteers that have helped with ringing efforts at all of the stations and the folks who had the foresight to initiate these long-term ringing stations. We thank Bird Studies Canada for making Long Point Bird Observatory data available. Financial support for the field operations at Long Point was provided by the W. Garfield Weston Foundation, the Ontario Ministry of Natural Resources—Wildlife Assessment Program, the Federation of Ontario Naturalists, and donations from hundreds of individuals and organizations. We thank Robert C. Leberman for his key role in initiating and maintaining the continuity of the banding program at Powdermill Nature Reserve from 1961 to present. Operated by Carnegie Museum of Natural History, the Powdermill program has been generously funded through numerous grants from private individuals and corporate foundations. We also thank Marilyn Niedermeier, data entry operator at the Section of Birds of CMNH, for her diligent work entering and checking Powdermill’s daily banding records for more than 20 years, and for providing us with the Powdermill data used in this study. Mark Schwartz was kind enough to provide the lilac data. Nora Diggs helped develop the figures and Kevin Omland, Scott Sillett and Colin Studds made important suggestions to improve the manuscript.
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Marra, P.P., Francis, C.M., Mulvihill, R.S. et al. The influence of climate on the timing and rate of spring bird migration. Oecologia 142, 307–315 (2005). https://doi.org/10.1007/s00442-004-1725-x
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DOI: https://doi.org/10.1007/s00442-004-1725-x