Local temperature fine-tunes the timing of spring migration in birds.

Evidence for climate-driven phenological changes is rapidly increasing at all trophic levels. Our current poor knowledge of the detailed control of bird migration from the level of genes and hormonal control to direct physiological and behavioral responses hampers our ability to understand and predict consequences of climatic change for migratory birds. In order to better understand migration phenology and adaptation in environmental changes, we here assess the scale at which weather affects timing of spring migration in passerine birds. We use three commonly used proxies of spring-time climatic conditions: (1) vegetation "greenness" (NDVI) in Europe, (2) local spring temperatures in northern Europe, and (3) the North Atlantic Oscillation Index (NAO) as predictors of the phenology of avian migration as well as the strength of their effect on different subsets of populations and the dependence of correlations on species-specific migratory strategy. We analyze phenological patterns of the entire spring migration period in 12 Palaearctic passerine species, drawing on long-term data collected at three locations along a longitudinal gradient situated close to their northern European breeding area. Local temperature was the best single predictor of phenology with the highest explanatory power achieved in combination with NAO. Furthermore, early individuals are more affected by climatic variation compared to individuals on later passage, indicating that climatic change affects subsets of migratory populations differentially. Species wintering closer to the breeding areas were affected more than were those travelling longer distances and this pattern was strongest for the earliest subsets of the population. Overall, our results suggest that at least early subsets of the population are affected by local conditions and early birds use local conditions to fine-tune the date of their spring arrival while individuals arriving later are driven by other factors than local conditions e.g. endogenous control. Understanding what cues migratory organisms use to arrive at an optimum time is important for increasing our knowledge of fundamental issues like decision making in organisms during migration and is crucial for future protection of migratory organisms.

[1]  K. Thorup,et al.  Understanding the migratory orientation program of birds: extending laboratory studies to study free-flying migrants in a natural setting. , 2010, Integrative and comparative biology.

[2]  Timothy Coppack,et al.  Proximate control and adaptive potential of protandrous migration in birds. , 2009, Integrative and comparative biology.

[3]  C. Rahbek,et al.  Avian migrants adjust migration in response to environmental conditions en route , 2008, Biology Letters.

[4]  E. Gwinner,et al.  Circannual clocks in avian reproduction and migration , 2008 .

[5]  K. Thorup,et al.  Sex-differentiated migration patterns, protandry and phenology in North European songbird populations , 2008, Journal of Ornithology.

[6]  W. Bradshaw,et al.  Genetic response to rapid climate change: it's seasonal timing that matters , 2008, Molecular ecology.

[7]  O. Gordo Why are bird migration dates shifting? A review of weather and climate effects on avian migratory phenology , 2007 .

[8]  R. Leimu,et al.  Responses to climate change in avian migration time - microevolution versus phenotypic plasticity , 2007 .

[9]  F. Pulido,et al.  Phenotypic changes in spring arrival: evolution, phenotypic plasticity, effects of weather and condition , 2007 .

[10]  C. Both,et al.  Climate change and timing of avian breeding and migration throughout Europe , 2007 .

[11]  A. P. Tøttrup,et al.  Effects of climate change on the degree of protandry in migratory songbirds , 2007 .

[12]  C. Parmesan Influences of species, latitudes and methodologies on estimates of phenological response to global warming , 2007 .

[13]  Timothy Coppack Experimental determination of the photoperiodic basis for geographic variation in avian seasonality , 2007, Journal of Ornithology.

[14]  J. Lobo,et al.  Spatial patterns of white stork (Ciconia ciconia) migratory phenology in the Iberian Peninsula , 2007, Journal of Ornithology.

[15]  T. Sparks,et al.  Is earlier spring migration of Tatarstan warblers expected under climate warming? , 2007, International journal of biometeorology.

[16]  A. Hedenström,et al.  Climate change and the optimal arrival of migratory birds , 2007, Proceedings of the Royal Society B: Biological Sciences.

[17]  G. Swenson,et al.  Going wild: what a global small-animal tracking system could do for experimental biologists , 2007, Journal of Experimental Biology.

[18]  C. Parmesan Ecological and Evolutionary Responses to Recent Climate Change , 2006 .

[19]  E. Lehikoinen,et al.  Climatic responses in spring migration of boreal and arctic birds in relation to wintering area and taxonomy , 2006 .

[20]  L. Beaumont,et al.  A matter of timing: changes in the first date of arrival and last date of departure of Australian migratory birds , 2006 .

[21]  J. Vik,et al.  Rapid Advance of Spring Arrival Dates in Long-Distance Migratory Birds , 2006, Science.

[22]  C. Both,et al.  Climate change and population declines in a long-distance migratory bird , 2006, Nature.

[23]  O. Gordo,et al.  Phenology and climate change: a long-term study in a Mediterranean locality , 2005, Oecologia.

[24]  N. Pettorelli,et al.  Using the satellite-derived NDVI to assess ecological responses to environmental change. , 2005, Trends in ecology & evolution.

[25]  A. Mills Changes in the timing of spring and autumn migration in North American migrant passerines during a period of global warming , 2005 .

[26]  Markus Ahola,et al.  Variation in climate warming along the migration route uncouples arrival and breeding dates , 2004 .

[27]  R. Stöckli,et al.  European plant phenology and climate as seen in a 20-year AVHRR land-surface parameter dataset , 2004 .

[28]  Lars Gustafsson,et al.  Large–scale geographical variation confirms that climate change causes birds to lay earlier , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  T. H. Clutton-Brock,et al.  Why large-scale climate indices seem to predict ecological processes better than local weather , 2004, Nature.

[30]  A. Lehikoinen,et al.  Spring arrival of birds depends on the North Atlantic Oscillation , 2004 .

[31]  P. Marra,et al.  Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[32]  M. Kéry,et al.  Timing of autumn bird migration under climate change: advances in long–distance migrants, delays in short–distance migrants , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[34]  O. Hüppop,et al.  North Atlantic Oscillation and timing of spring migration in birds , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  S. Schneider,et al.  Fingerprints of global warming on wild animals and plants , 2003, Nature.

[36]  N. Stenseth,et al.  North Atlantic Oscillation timing of long‐ and short‐distance migration , 2002 .

[37]  O. Hoegh‐Guldberg,et al.  Ecological responses to recent climate change , 2002, Nature.

[38]  C. Rahbek,et al.  Population trends in Baltic passerine migrants, elucidated by a combination of ringing data and point- and summer-count indices , 2002 .

[39]  James W. Hurrell,et al.  The North Atlantic Oscillation: Past, present, and future , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  R T Holmes,et al.  Impacts of a global climate cycle on population dynamics of a migratory songbird. , 2000, Science.

[41]  R. Good,et al.  Long Term Effects on Immune Function of Early Nutritional Deprivation , 1973, Nature.

[42]  R. Greenberg Biometry , 1969, The Yale Journal of Biology and Medicine.

[43]  Melissa S. Bowlin,et al.  Frontiers inEcology and the Environment Integrating concepts and technologies to advance the study of bird migration , 2009 .

[44]  A. P. M A C M Y N O W S K I,et al.  Changes in spring arrival of Nearctic-Neotropical migrants attributed to multiscalar climate , 2007 .

[45]  JØrgen RabØl Population trends in Baltic passerine migrants, elucidated by a combination of ringing data and point- and summer-count indices , 2007 .

[46]  Carsten Rahbek,et al.  Patterns of change in timing of spring migration in North European songbird populations , 2006 .

[47]  C. Rahbek,et al.  Changes in timing of autumn migration in North European songbird populations , 2006 .

[48]  Charles M. Francis,et al.  The influence of climate on the timing and rate of spring bird migration , 2004, Oecologia.

[49]  T. Sparks,et al.  Arrival and Departure Dates , 2004 .

[50]  Timothy Coppack,et al.  Photoperiodic Response and the Adaptability of Avian Life Cycles to Environmental Change , 2004 .

[51]  P. Berthold Control of bird migration , 1996 .

[52]  P. Berthold Patterns of avian migration in light of current global "greenhouse" effects: A central European perspective , 1991 .

[53]  T. D. Pigott,et al.  Bird Migration , 1910, Nature.