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Science 2 February 2007:
Vol. 315. no. 5812, p. 598
DOI: 10.1126/science.1136920
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Technical Comments

Response to Comment on "Rapid Advance of Spring Arrival Dates in Long-Distance Migratory Birds"

Niclas Jonzén,1 Andreas Lindén,2 Torbjørn Ergon,4 Endre Knudsen,4 Jon Olav Vik,4 Diego Rubolini,5 Dario Piacentini,6 Christian Brinch,4 Fernando Spina,6 Lennart Karlsson,7 Martin Stervander,8 Arne Andersson,8 Jonas Waldenström,9 Aleksi Lehikoinen,3 Erik Edvardsen,10 Rune Solvang,10 Nils Chr. Stenseth4*

Both's comment questions our suggestion that the advanced spring arrival time of long-distance migratory birds in Scandinavia and the Mediterranean may reflect a climate-driven evolutionary change. We present additional arguments to support our hypothesis but underscore the importance of additional studies involving direct tests of evolutionary change.

1 Department of Theoretical Ecology, Ecology Building, Lund University, SE-22362 Lund, Sweden.
2 Department of Biological and Environmental Sciences, Integrative Ecology Unit, Post Office Box 65 (Viikinkaari 1), FIN-00014, Helsinki University, Finland.
3 Department of Biological and Environmental Sciences, Bird Ecology Unit, Post Office Box 65 (Viikinkaari 1), FIN-00014, Helsinki University, Finland.
4 Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, Post Office Box 1066, Blindern, N-0316 Oslo, Norway.
5 Dipartimento di Biologia Animale, Università degli Studi di Pavia, piazza Botta 9, I-27100 Pavia, Italy.
6 Istituto Nazionale per la Fauna Selvatica, via Ca' Fornacetta 9, I-40064 Ozzano Emilia (BO), Italy.
7 Falsterbo Bird Observatory, Fyren, SE-23940 Falsterbo, Sweden.
8 Ottenby Bird Observatory, Post Office Box 1500, SE-38065 Degerhamn, Sweden.
9 Section for Zoonotic Ecology and Epidemiology, Department of Environmental Sciences, Kalmar University, SE-39182 Kalmar, Sweden.
10 Jomfruland Bird Observatory, Post Office Box 1076, N-3704 Skien, Norway.

* To whom correspondence should be addressed. E-mail: n.c.stenseth{at}bio.uio.no.

Both (1) questions our suggestion that the advanced spring arrival time of long-distance migratory birds in Scandinavia and the Mediterranean may reflect a climate-driven evolutionary change (2). A key premise of our interpretation is that spring is arriving earlier in the breeding areas we considered and that most birds are laying eggs earlier than before. Yet Both argues that the species we studied breed mainly in Fennoscandia and northern Russia, where springs have not become warmer, nor has egg-laying advanced. However, recovery of birds banded at the Nordic observatories and at Capri clearly show that Scandinavia (and, to some extent, the Baltic) is where most individuals of the studied species breed (3–7). Overall, contrary to Both's assertions (1, 8), it is well documented that spring green-up advanced by about 0.5 days/year from 1982 to 2001 in most of Scandinavia and western Russia (9). This is likely to have contributed to earlier peak insect abundance for breeding migrants. Likewise, April and May were warmer between 1991 and 2005 than in the period 1961 to 1990 in Sweden (10). However, trends in spring timing do vary within regions, with spring coming later in snow-rich mountain areas, for example (9).

Both (1) suggests two alternative explanations for the observed change in migration timing of long-distance migrants, neither of which are supported by the available evidence. His first suggestion is that the sizes of populations arriving early might have increased relative to later-arriving populations of the same species. In general, the populations breeding farthest to the north are the last to migrate through our study sites (11). If such populations in most species were declining relative to earlier-arriving populations, this might explain our results. However, there is no evidence that this has generally occurred. In Finland, populations have increased in the south relative to the north only in two of the seven long-distance migrant species included in our study (12).

Both also suggests that spring migration could be faster as a result of improved ecological conditions en route (13), such as increased Sahel rainfall and North African spring temperatures (1, 13). However, a reanalysis of our data from Capri indicates that the observed advance in migration dates is unaffected by taking these seemingly favorable conditions into account (14). The possibility that some unmeasured environmental cue might have induced a phenotypic shift in the onset of migratory activity or speed of migration in Africa cannot be ruled out. Nevertheless, our result is suggestive, and the next step would be to search for direct evidence of microevolution. For instance, a comparison of individual- and population-level changes in phenotypic traits may quantify to what degree the observed changes in mean phenotypic traits are caused by plasticity or genetic adaptation (15).

Both (1) argues that our report suggests that the inadequate timing responses may only be transient and that rapid evolution may solve the birds' mismatch of arrival time and peak food availability (2). However, such perfect compensation is not to be expected. The optimal temporal shift in arrival date is always less than the shift in the food peak date because of the survival costs of early arrival (16). Hence, despite an evolutionary response, bird populations might still face a temporal mismatch of resources and breeding, which may cause population declines (17). In our view, phenotypic plasticity and evolutionary response are not mutually exclusive, and the latter remains a likely explanation for the general trend of earlier springtime arrival of long-distance migrant birds.


References and Notes

  • 1. C. Both, Science 315, 598 (2006); www.sciencemag.org/cgi/content/full/315/5812/598b.
  • 2. N. Jonzén et al., Science 312, 1959 (2006).[Abstract/Free Full Text]
  • 3. V. Bakken, O. Runde, E. Tjørve, Norwegian Bird Ringing Atlas, Vol. 2 (Stavanger Museum, Stavanger, Norway, 2006).
  • 4. Swedish Museum of Natural History, Bird Ringing Centre, www.nrm.se/rc.
  • 5. Finnish Museum of Natural History, Finnish Ringing Centre, www.fmnh.helsinki.fi/english/zoology/ringing.
  • 6. Italian Ringing Centre, Istituto Nazionale per la Fauna Selvatica, www.infs.it.
  • 7. N. Jonzén et al., Ornis Svecica 16, 27 (2006).
  • 8. C. Both et al., Proc. R. Soc. Ser. B 271, 1657 (2004). [Medline]
  • 9. R. Stöckli, P. L. Vidale, Int. J. Remote Sens. 25, 3303 (2004). [CrossRef]
  • 10. The Swedish Meteorological and Hydrological Institute, Fact sheet no. 29 (in Swedish) (2006).
  • 11. A. Hedenström, J. Pettersson, Vår Fågelvärld 43, 217 (1984).
  • 12. R. Väisänen, Linnut-vuosikirja 2005, 83 (2005).
  • 13. C. Both, R. G. Bijlsma, M. E. Visser, J. Avian Biol. 36, 368 (2005). [CrossRef]
  • 14. The linear trend in on the median arrival date, when taking into account the Sahel wet season (June to October) rainfall, the mean of February to April temperatures at Tunis, and the winter North Atlantic Oscillation (2), was –0.27 days/year (95% confidence interval, –0.40 to –0.15; the species set is considered as fixed, and the variance of the mean is calculated from the uncertainty of the species-specific effects), which is in line with the temporal trend reported in (2). Meteorological information was obtained from (18) and (19) for Sahel rainfall and Tunis temperature, respectively.
  • 15. A. P. Møller, J. Merilä, Adv. Ecol. Res. 35, 111 (2004). [CrossRef]
  • 16. N. Jonzén, A. Hedenström, P. Lundberg, Proc. R. Soc. Lond. B. Biol. Sci. 274, 269 (2007). [Medline]
  • 17. C. Both, S. Bouwhuis, A. Offermans, C. M. Lessells, M. E. Visser, Nature 441, 81 (2006). [CrossRef] [Medline]
  • 18. Joint Institute for the Study of the Atmosphere and Ocean, http://jisao.washington.edu/data_sets/sahel.
  • 19. National Oceanic and Atmospheric Administration, National Climate Data Center, Global Historical Climatology Network, version 2; http://iridl.ldeo.columbia.edu/SOURCES/.NOAA/.NCDC/.GHCN/.v2.
Received for publication 27 October 2006. Accepted for publication 29 December 2006.

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Science. ISSN 0036-8075 (print), 1095-9203 (online)