International Journal of Biometeorology

, Volume 51, Issue 6, pp 553–563 | Cite as

Long-term trends in first arrival and first egg laying dates of some migrant and resident bird species in northern Italy

  • Diego Rubolini
  • Roberto Ambrosini
  • Mario Caffi
  • Pierandrea Brichetti
  • Stefano Armiraglio
  • Nicola Saino
Original Paper


Climate change is affecting the phenology of seasonal events in Europe and the Northern Hemisphere, as shown by several studies of birds’ timing of migration and reproduction. Here, we analyse the long-term (1982–2006) trends of first arrival dates of four long-distance migratory birds [swift (Apus apus), nightingale (Luscinia megarhynchos), barn swallow (Hirundo rustica), and house martin (Delichon urbicum)] and first egg laying dates of two migrant (swift, barn swallow) and two resident species [starling (Sturnus vulgaris), Italian sparrow (Passer italiae)] at a study site in northern Italy. We also addressed the effects of local weather (temperature and precipitation) and a climate index (the North Atlantic Oscillation, NAO) on the interannual variability of phenological events. We found that the swift and the barn swallow significantly advanced both arrival and laying dates, whereas all other species did not show any significant temporal trend in either arrival or laying date. The earlier arrival of swifts was explained by increasing local temperatures in April, whereas this was not the case for arrival dates of swallows and first egg laying dates of both species. In addition, arrival dates of house martins were earlier following high NAO winters, while nightingale arrival was earlier when local spring rainfall was greater. Finally, Italian sparrow onset of reproduction was anticipated by greater spring rainfall, but delayed by high spring NAO anomalies, and swift’s onset of reproduction was anticipated by abundant rainfall prior to reproduction. There were no significant temporal trends in the interval between onset of laying and arrival in either the swift or the barn swallow. Our findings therefore indicate that birds may show idiosyncratic responses to climate variability at different spatial scales, though some species may be adjusting their calendar to rapidly changing climatic conditions.


Avian phenology Climate change First arrival date Italy North Atlantic Oscillation 



We thank two anonymous referees for constructive comments on an earlier version of the manuscript.


  1. Ahas R, Aasa A (2006) The effects of climate change on the phenology of selected Estonian plant, bird and fish populations. Int J Biometeorol 51:17–26CrossRefPubMedGoogle Scholar
  2. Barnston AG, Livezey RE (1987) Classification, seasonality and persistence of low-frequency atmospheric circulation patterns. Mon Weather Rev 115:1083–1126CrossRefGoogle Scholar
  3. Bellot MD, Dervieux A, Isenmann P (1991) Relationship between temperature and the timing of breeding of the blue tit (Parus caeruleus) in two Mediterranean oakwoods. J Ornithol 132:297–301CrossRefGoogle Scholar
  4. Bojariu R, Giorgi F (2005) The North Atlantic Oscillation signal in a regional climate simulation for the European region. Tellus 57A:641–653Google Scholar
  5. Both C, Artemyev AV, Blaauw B, Cowie RJ, Dekhuijzen AJ, Eeva T, Enemar A, Gustafsson L, Ivankina EV, Jarvinen A, Metcalfe NB, Nyholm NEI, Potti J, Ravussin PA, Sanz JJ, Silverin B, Slater FM, Sokolov LV, Torok J, Winkel W, Wright J, Zang H, Visser ME (2004) Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proc R Soc B 271:1657–1662CrossRefPubMedGoogle Scholar
  6. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83CrossRefPubMedGoogle Scholar
  7. Brunetti M, Maugeri M, Monti F, Nanni T (2006) Temperature and precipitation variability in Italy in the last two centuries from homogenised instrumental time series. Int J Climatol 26:345–381CrossRefGoogle Scholar
  8. Butler CJ (2003) The disproportionate effect of global warming on the arrival dates of short-distance migratory birds in North America. Ibis 145:484–495CrossRefGoogle Scholar
  9. Cotton PA (2003) Avian migration phenology and global climate change. Proc Natl Acad Sci USA 100:12219–12222CrossRefPubMedGoogle Scholar
  10. Cramp S (1998) The complete birds of the Western Palearctic on CD-ROM. Oxford University Press, OxfordGoogle Scholar
  11. Crick HQP, Sparks TH (1999) Climate change related to egg-laying trends. Nature 399:423–424CrossRefGoogle Scholar
  12. Crick HQP, Dudley C, Glue DE, Thomson DL (1997) UK birds are laying eggs earlier. Nature 388:526CrossRefGoogle Scholar
  13. Dunn PO (2004) Breeding dates and reproductive performance. Adv Ecol Res 35:67–85Google Scholar
  14. Forchhammer MC, Post E (2004) Using large-scale climate indices in climate change ecology studies. Popul Ecol 46:1–12CrossRefGoogle Scholar
  15. Forchhammer MC, Post E, Stenseth NC (1998) Breeding phenology and climate. Nature 391:29–30CrossRefGoogle Scholar
  16. Forchhammer MC, Post E, Stenseth NC (2002) North Atlantic Oscillation timing of long- and short-distance migration. J Anim Ecol 71:1002–1014CrossRefGoogle Scholar
  17. Frampton GK, Van Den Brink PJ, Gould PJL (2000) Effects of spring drought and irrigation on farmland arthropods in southern Britain. J Appl Ecol 37:865–883CrossRefGoogle Scholar
  18. Garson DG (2006) Multiple regression. (accessed 15 December 2006)
  19. Gordo O, Brotons LL, Ferrer X, Comas P (2005) Do changes in climate patterns in wintering areas affect the timing of the spring arrival of trans-Saharan migrant birds? Glob Chang Biol 11:12–21CrossRefGoogle Scholar
  20. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Natl Acad Sci USA 103:14288–14293CrossRefPubMedGoogle Scholar
  21. Huin N, Sparks TH (1998) Arrival and progression of the Swallow Hirundo rustica through Britain. Bird Study 45:361–370Google Scholar
  22. Huin N, Sparks TH (2000) Spring arrival patterns of the Cuckoo Cuculus canorus, Nightingale Luscinia megarhynchos and Spotted Flycatcher Muscicapa striata in Britain. Bird Study 47:22–31CrossRefGoogle Scholar
  23. Hulme M, Doherty R, Ngara T, New M, Lister D (2001) African climate change: 1900–2100. Clim Res 17:145–168Google Scholar
  24. Hüppop O, Hüppop K (2003) North Atlantic Oscillation and timing of spring migration in birds. Proc R Soc B 270:233–240CrossRefPubMedGoogle Scholar
  25. Hurrell JW (1995) Decadal trends in the North Atlantic Oscillation: regional temperatures and precipitation. Science 269:676–679CrossRefPubMedGoogle Scholar
  26. Jonzén N, Lindén A, Ergon T, Knudsen E, Vik JO, Rubolini D, Piacentini D, Brinch C, Spina F, Karlsson L, Stervander M, Andersson A, Waldenström J, Lehikoinen A, Edvardsen E, Solvang R, Stenseth NC (2006a) Rapid advance of spring arrival dates in long-distance migratory birds. Science 312:1959–1961CrossRefPubMedGoogle Scholar
  27. Jonzén N, Piacentini D, Andersson A, Montemaggiori A, Stervander M, Rubolini D, Waldenström J, Spina F (2006b) The timing of spring migration in trans-Saharan migrants: a comparison between Ottenby, Sweden, and the island of Capri, Italy. Ornis Svec 16:27–33Google Scholar
  28. Jonzén N, Hedenström A, Lundberg P (2007) Climate change and the optimal arrival of migratory birds. Proc R Soc B 274:269–274CrossRefPubMedGoogle Scholar
  29. Lehikoinen E, Sparks TH, Zalakevicius M (2004) Arrival and departure dates. Adv Ecol Res 35:1–31CrossRefGoogle Scholar
  30. Maranini N (1991) Quattordici anni di osservazioni sull’arrivo e sulla partenza del Rondone, Apus apus, a Genova. Riv Ital Ornitol 61:69–70Google Scholar
  31. McCleery RH, Perrins CM (1998) Temperature and egg-laying trends. Nature 391:30–31CrossRefGoogle Scholar
  32. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Aha R, Alm-Kubler K, Bissolli P, Braslavska O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A, Filella Y, Jatcza K, Mage F, Mestre A, Nordli O, Penuelas J, Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski FE, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976CrossRefGoogle Scholar
  33. Møller AP, Merilä J (2004) Analysis and interpretation of long-term studies investigating responses to climate change. Adv Ecol Res 35:11–130Google Scholar
  34. Moltoni E (1950) A Milano città i primi Rondoni (Micropus apus) arrivano prima delle Rondini (Hirundo rustica). Riv Ital Ornitol 20:50–57Google Scholar
  35. Oba G, Post E, Stenseth NC (2001) Sub-saharan desertification and productivity are linked to hemispheric climate variability. Glob Chang Biol 7:241–246CrossRefGoogle Scholar
  36. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  37. Peintinger M, Schuster S (2005) Veränderungen der Erstankünfte bei häufigen Zugvogelarten in Südwestdeutschland. Vogelwarte 43:161–169Google Scholar
  38. Post E, Forchhammer MC, Stenseth NC, Callaghan TV (2001) The timing of life-history events in a changing climate. Proc R Soc B 268:15–23CrossRefPubMedGoogle Scholar
  39. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60CrossRefPubMedGoogle Scholar
  40. Saino N, Szép T, Romano M, Rubolini D, Spina F, Møller AP (2004) Ecological conditions during winter predict arrival date at the breeding quarters in a trans-Saharan migratory bird. Ecol Lett 7:21–25CrossRefGoogle Scholar
  41. Sanz JJ (2003) Large-scale effect of climate change on breeding parameters of pied flycatchers in Western Europe. Ecography 26:45–50CrossRefGoogle Scholar
  42. Sanz JJ, Potti J, Moreno J, Merino S, Frias O (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Glob Chang Biol 9:461–472CrossRefGoogle Scholar
  43. Schmidli J, Schmutz C, Frei C, Wanner H, Schar C (2002) Mesoscale precipitation variability in the region of the European Alps during the 20th century. Int J Climatol 22:1049–1074CrossRefGoogle Scholar
  44. Schnoor JL (2005) Global warming: a consequence of human activities rivaling earth’s biogeochemical processes. Hum Ecol Risk Assess 11:105–1110CrossRefGoogle Scholar
  45. Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the Northern Hemisphere. Glob Chang Biol 12:343–351CrossRefGoogle Scholar
  46. Sparks TH, Braslavská O (2001) The effects of temperature, altitude and latitude on the arrival and departure dates of the swallow Hirundo rustica in the Slovak Republic. Int J Biometeorol 45:212–216CrossRefPubMedGoogle Scholar
  47. Sparks TH, Carey PD (1995) The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. J Ecol 83:321–329CrossRefGoogle Scholar
  48. Sparks TH, Roberts DR, Crick HQP (2001) What is the value of first arrival dates of spring migrants in phenology? Avian Ecol Behav 7:75–85Google Scholar
  49. Sparks TH, Bairlein F, Bojarinova JG, Hüppop H, Lehikoinen EA, Rainio K, Sokolov LV, Walker D (2005) Examining the total arrival distribution of migratory birds. Glob Chang Biol 11:22–30CrossRefGoogle Scholar
  50. Stenseth NC, Mysterud A, Ottersen G, Hurrell JW, Kung-Sik C, Lima M (2002) Ecological effects of climate fluctuations. Science 297:1292–1296CrossRefPubMedGoogle Scholar
  51. Stenseth NC, Ottersen G, Hurrell JW, Mysterud A, Lima M, Chan KS, Yoccoz NG, Ådlandsvik B (2003) Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proc R Soc B 270:2087–2096CrossRefPubMedGoogle Scholar
  52. Stephenson DB, Pavan V, Collins M, Junge MM, Quadrelli R (2006) North Atlantic Oscillation response to transient greenhouse gas forcing and the impact on European winter climate: a CMIP2 multi-model assessment. Clim Dyn 27:401–420CrossRefGoogle Scholar
  53. Stöckli R, Vidale PL (2004) European plant phenology and climate as seen in a 20-year AVHRR land-surface parameter dataset. Int J Remote Sens 25:3303–3330CrossRefGoogle Scholar
  54. Tomozeiu R, Lazzeri M, Cacciamani C (2002) Precipitation fluctuations during the winter season from 1960 to 1995 over Emilia-Romagna, Italy. Theor Appl Climatol 72:221–229CrossRefGoogle Scholar
  55. Töpfer T (2006) The taxonomic status of the Italian Sparrow—Passer italiae (Vieillot 1817): speciation by stabilised hybridisation? A critical analysis. Zootaxa 1325:117–145Google Scholar
  56. Visser ME, Adriaensen F, van Balen JH, Blondel J, Dhondt AA, van Dongen S, du Feu C, Ivankina EV, Kerimov AB, de Laet J, Matthysen E, McCleery R, Orell M, Thomson DL (2003) Variable responses to large-scale climate change in European Parus populations. Proc R Soc B 270:367–372CrossRefPubMedGoogle Scholar
  57. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefPubMedGoogle Scholar
  58. Winkler DW, Dunn PO, McCulloch CE (2002) Predicting the effects of climate change on avian life-history traits. Proc Natl Acad Sci USA 99:13595–13599CrossRefGoogle Scholar
  59. Zalakevicius M, Bartkeviciene G, Raudonikis L, Janulaitis J (2006) Spring arrival response to climate change in birds: a case study from eastern Europe. J Ornithol 147:326–343CrossRefGoogle Scholar

Copyright information

© ISB 2007

Authors and Affiliations

  • Diego Rubolini
    • 1
  • Roberto Ambrosini
    • 2
  • Mario Caffi
    • 3
  • Pierandrea Brichetti
    • 4
  • Stefano Armiraglio
    • 5
  • Nicola Saino
    • 6
  1. 1.Dipartimento di Biologia AnimaleUniversità degli Studi di PaviaPaviaItaly
  2. 2.Dipartimento di Biotecnologie e BioscienzeUniversità degli Studi di Milano-BicoccaMilanItaly
  3. 3.Osservatorio Ornitologico Pianura Bresciana “Padernello”Borgo S. GiacomoItaly
  4. 4.Centro Italiano Studi OrnitologiciVerolavecchiaItaly
  5. 5.Museo Civico di Scienze Naturali di BresciaBresciaItaly
  6. 6.Dipartimento di BiologiaUniversità degli Studi di MilanoMilanItaly

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