Oecologia

, Volume 178, Issue 4, pp 1227–1238 | Cite as

Detecting mismatches of bird migration stopover and tree phenology in response to changing climate

Community ecology - Original research

Abstract

Migratory birds exploit seasonal variation in resources across latitudes, timing migration to coincide with the phenology of food at stopover sites. Differential responses to climate in phenology across trophic levels can result in phenological mismatch; however, detecting mismatch is sensitive to methodology. We examined patterns of migrant abundance and tree flowering, phenological mismatch, and the influence of climate during spring migration from 2009 to 2011 across five habitat types of the Madrean Sky Islands in southeastern Arizona, USA. We used two metrics to assess phenological mismatch: synchrony and overlap. We also examined whether phenological overlap declined with increasing difference in mean event date of phenophases. Migrant abundance and tree flowering generally increased with minimum spring temperature but depended on annual climate by habitat interactions. Migrant abundance was lowest and flowering was highest under cold, snowy conditions in high elevation montane conifer habitat while bird abundance was greatest and flowering was lowest in low elevation riparian habitat under the driest conditions. Phenological synchrony and overlap were unique and complementary metrics and should both be used when assessing mismatch. Overlap declined due to asynchronous phenologies but also due to reduced migrant abundance or flowering when synchrony was actually maintained. Overlap declined with increasing difference in event date and this trend was strongest in riparian areas. Montane habitat specialists may be at greatest risk of mismatch while riparian habitat could provide refugia during dry years for phenotypically plastic species. Interannual climate patterns that we observed match climate change projections for the arid southwest, altering stopover habitat condition.

Keywords

Aridlands Flowering Gradients Madrean Stopover habitat Climate change 

References

  1. Allen CD, Breshears DD (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci USA 95:14839–14842PubMedCentralPubMedCrossRefGoogle Scholar
  2. Altermatt F (2012) Temperature-related shifts in butterfly phenology depend on the habitat. Glob Change Biol 18:2429–2438. doi:10.1111/j.1365-2486.2012.02727.x CrossRefGoogle Scholar
  3. Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20:243–248. doi:10.1016/j.cub.2009.11.074 PubMedCrossRefGoogle Scholar
  4. Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411: 296–298. doi:10.1038/35077063 PubMedCrossRefGoogle Scholar
  5. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83. doi:10.1038/nature04539 PubMedCrossRefGoogle Scholar
  6. Both C, Van Turnhout CA, Bijlsma RG, Siepel H, Van Strien AJ, Foppen RP (2009) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc Lond B. doi:10.1098/rspb.2009.1525 Google Scholar
  7. Brown JH, Valone TJ, Curtin CG (1997) Reorganization of an arid ecosystem in response to recent climate change. Proc Natl Acad Sci USA 94:9729–9733PubMedCentralPubMedCrossRefGoogle Scholar
  8. Buler JJ, Moore FR, Woltmann S (2007) A multi-scale examination of stopover habitat use by birds. Ecology 88:1789–1802. doi:10.1007/s10336-010-0640-7 PubMedCrossRefGoogle Scholar
  9. Carlisle JD, Olmstead KL, Richart CH, Swanson DL (2012) Food availability, foraging behavior, and diet of autumn migrant landbirds in the Boise Foothills of southwestern Idaho. Condor 114:449–461. doi:10.1525/cond.2012.100209 CrossRefGoogle Scholar
  10. Clavel J, Julliard R, Devictor V (2010) Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ 9:222–228. doi:10.1890/080216 CrossRefGoogle Scholar
  11. Coblentz DD, Riitters KH (2004) Topographic controls on the regional-scale biodiversity of the south-western USA. J Biogeog 31:1125–1138. doi:10.1111/j.1365-2699.2004.00981.x CrossRefGoogle Scholar
  12. Comer P, Faber-Langendoen D, Evans R, Gawler S, Josse C, Kittel G, Menard S, Pyne S, Reid M, Schulz K, Snowand K, Teague J (2003) Ecological systems of the United States: a working classification of US terrestrial systems. Nature Serve, Arlington. http://www.natureserve.org/library/usEcologicalsystems.pdf. Accessed Jan 2010
  13. Eis S (1973) Cone production of douglas-fir and grand fir and its climatic requirements. Can J For Res 3:61–70. doi:10.1139/x73-009 CrossRefGoogle Scholar
  14. Ellwood ER et al (2012) Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming? Oecologia 168:1161–1171. doi:10.1007/s00442-011-2160-4 PubMedCrossRefGoogle Scholar
  15. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439. doi:10.1016/j.tree.2007.05.006 PubMedCrossRefGoogle Scholar
  16. ESRI (Environmental Systems Resource Institute) (2009) ArcMap 9.3.1. ESRI, RedlandsGoogle Scholar
  17. Faaborg J et al (2010) Recent advances in understanding migration systems of New World land birds. Ecol Monogr 80:3–48. doi:10.1890/09-0397.1 CrossRefGoogle Scholar
  18. Fabina NS, Abbott KC, Gilman RT (2010) Sensitivity of plant-pollinator-herbivore communities to changes in phenology. Ecol Model 221:453–458. doi:10.1016/j.ecolmodel.2009.10.020 CrossRefGoogle Scholar
  19. Fontaine JJ, Decker KL, Skagen SK, van Riper C (2009) Spatial and temporal variation in climate change: a bird’s eye view. Clim Change 97:305–311. doi:10.1007/s10584-009-9644-9 CrossRefGoogle Scholar
  20. Forkner RE, Marquis RJ, Lill JT, Corff JL (2008) Timing is everything? Phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecol Entomol 33:276–285. doi:10.1111/j.1365-2311.2007.00976.x CrossRefGoogle Scholar
  21. Garfin G, Eischeid JK, Lenart M, Cole K, Ironside K, Cobb N (2010) Downscaling climate projections to model ecological change on topographically diverse landscapes of the arid southwestern US. In: van Riper IIIC, Wakeling BF, Sisk TD (eds) The Colorado Plateau IV. University of Arizona Press, Tucson, pp 21–44Google Scholar
  22. Garfin G, Jardine A, Merideth R, Black M, LeRoy S (eds) (2013) Assessment of Climate Change in the Southwest United States: A Report Prepared for the National Climate Assessment. A report by the Southwest Climate Alliance. Island Press, Washington, DCGoogle Scholar
  23. Gonzalez-Megias A, Menendez R (2012) Climate change effects on above- and below-ground interactions in a dryland ecosystem. Philos Trans R Soc Lond B 367:3115–3124. doi:10.1098/rstb.2011.0346 CrossRefGoogle Scholar
  24. Gullett P, Hatchwell BJ, Robinson RA, Evans KL (2013) Phenological indices of avian reproduction: cryptic shifts and prediction across large spatial and temporal scales. Ecol Evol 3:1864–1877. doi:10.1002/ece3.558 PubMedCentralPubMedCrossRefGoogle Scholar
  25. Hutto RL (1985) Seasonal changes in the habitat distribution of transient insectivorous birds in southeastern Arizona: competition mediated? Auk 102:120–132CrossRefGoogle Scholar
  26. Julliard R, Jiguet F, Couvet D (2004) Common birds facing global changes: what makes a species at risk? Glob Change Biol 10:148–154. doi:10.1111/j.1365-2486.2003.00723.x CrossRefGoogle Scholar
  27. Kellermann JL, van Riper IIIC (2015) Phenological synchrony of bird migration with tree flowering at desert riparian stopover sites. In: Wood EM, Kellermann JL (eds) Phenological synchrony and bird migration: changing climate and seasonal resources in North America. Studies in Avian Biology, vol 47. CRC, Boca Raton, pp 133–144Google Scholar
  28. Kelly AE, Goulden ML (2008) Rapid shifts in plant distribution with recent climate change. Proc Natl Acad Sci USA 33:11823–11826. doi:10.1073/pnas.0802891105 CrossRefGoogle Scholar
  29. La Sorte FA, Jetz W (2010) Projected range contractions of montane biodiversity under global warming. Proc R Soc Lond B. doi:10.1098/rspb.2010.0612 Google Scholar
  30. Lehikoinen E, Sparks TH, Zalakevicius M (2004) Arrival and departure dates. Birds Clim Change 35:1–31. doi:10.1016/S0065-2504(04)35001-4 CrossRefGoogle Scholar
  31. Lindroth A, Bath A (1999) Assessment of regional willow coppice yield in Sweden on basis of water availability. For Ecol Manag 121:57–65. doi:10.1016/S0378-1127(98)00556-8 CrossRefGoogle Scholar
  32. Lowry JH, Ramsey RD, Boykin K, Bradford D, Comer D, Falzarano S, Kepner W, Kirby JLangs L, Prior-Magee J, Manis G, O’Brien L, Sajwaj T, Thomas KA, Rieth W, Schrader S, Schrupp D, Schulz K, Thompson B, Velasquez C, Wallace C, Waller E, Wolk B (2005) Southwest Regional Gap Analysis Project: Final Report on Land Cover Mapping Methods. RS/GIS Laboratory, Utah State University, LoganGoogle Scholar
  33. MacMynowski DP, Root TL (2007) Climate and the complexity of migratory phenology: sexes, migratory distance, and arrival distributions. Int J Biometeorol 51:361–373. doi:10.1007/s00484-006-0084-1 PubMedCrossRefGoogle Scholar
  34. Marra PP, Francis CM, Mulvihill RS, Moore FR (2005) The influence of climate on the timing and rate of spring bird migration. Oecologia 142:307–315. doi:10.1007/s00442-004-1725-x PubMedCrossRefGoogle Scholar
  35. Martin TE (2007) Climate correlates of 20 years of trophic changes in a high-elevation riparian system. Ecology 88:367–380. doi:10.1890/0012-9658(2007)88[367:CCOYOT]2.0.CO;2PubMedCrossRefGoogle Scholar
  36. McGrath LJ, van Riper C, Fontaine JJ (2009) Flower power: tree flowering phenology as a settlement cue for migrating birds. J Anim Ecol 78:22–30. doi:10.1111/j.1365-2656.2008.01464.x PubMedCrossRefGoogle Scholar
  37. McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol A 128:579–593. doi:10.1016/S1095-6433(00)00336-6 CrossRefGoogle Scholar
  38. Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger P (2008) Bird migration times, climate change, and changing population sizes. Glob Change Biol 14:1959–1972. doi:10.1111/j.1365-2486.2008.01619.x CrossRefGoogle Scholar
  39. Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc Lond B Biol Sci 365:3177–3186. doi:10.1098/rstb.2010.0148   PubMedCentralPubMedCrossRefGoogle Scholar
  40. Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc Natl Acad Sci USA 105:16195–16200. doi:10.1073/pnas.0803825105 PubMedCentralPubMedCrossRefGoogle Scholar
  41. Moore F, Kerlinger P (1987) Stopover and fat deposition by North American wood-warbler (Parulinae) following spring migration over the Gulf of Mexico. Oecologia 74:47–54. doi:10.1007/BF00377344 CrossRefGoogle Scholar
  42. Moore FR, Yong W (1991) Evidence of food-based competition among passerine migrants during stopover. Behav Ecol Sociobiol 28:85–90. doi:10.1650/8350.1 CrossRefGoogle Scholar
  43. Moore FR, Gauthreaux SA Jr, Kerlinger PA, Simons TR (1995) Habitat requirements during migration: important link in conservation. In: Martin TE, Finch DM (eds) Ecology and management of neotropical migratory birds, a synthesis and review of critical issues. Oxford University Press, New York, pp 121–144Google Scholar
  44. NOAA (2013) National Oceanic and Atmospheric Administration, National Climate Data Center. http://www.ncdc.noaa.gov/data-access
  45. Norris DR, Marra PP (2007) Seasonal interactions, habitat quality, and population dynamics in migratory birds. Condor 109:535–547CrossRefGoogle Scholar
  46. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872. doi:10.1111/j.1365-2486.2007.01404.x CrossRefGoogle Scholar
  47. Paxton KL, Van Riper C, O’Brien C (2008) Movement patterns and stopover ecology of Wilson’s Warblers during spring migration on the lower Colorado River in southwestern Arizona. Condor 110:672–681. doi:10.1525/cond.2008.8602 CrossRefGoogle Scholar
  48. Poole A (ed) (2005) The Birds of North America Online. Cornell Laboratory of Ornithology, Ithaca. http://bna.birds.cornell.edu/BNA/
  49. Rangwala I, Miller JR (2012) Climate change in mountains: a review of elevation-dependent warming and its possible causes. Clim Change 114:527–547. doi:10.1007/s10584-012-0419-3 CrossRefGoogle Scholar
  50. Reynolds RT, Scott JM, Nussbaum RA (1980) A variable circular-plot method for estimating bird numbers. Condor 82:309–313. doi:10.2307/1367399 CrossRefGoogle Scholar
  51. 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. doi:10.1525/auk.2012.12003 CrossRefGoogle Scholar
  52. Rodewald PG, Brittingham MC (2007) Stopover habitat use by spring migrant landbirds: the roles of habitat structure, leaf development, and food availability. Auk 124:1063–1074. doi:10.1642/0004-8038(2007)124[1063:SHUBSM]2.0.CO;2CrossRefGoogle Scholar
  53. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  54. Seager R et al (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316:1181–1184. doi:10.1126/science.1139601 PubMedCrossRefGoogle Scholar
  55. Seewagen CL, Guglielmo CG (2010) Effects of fat and lean body mass on migratory landbird stopover duration. Wilson J Ornithol 122:82–87. doi:10.1676/09-088.1 CrossRefGoogle Scholar
  56. Şekercioğlu CH, Schneider SH, Fay JP, Loarie SR (2008) Climate change, elevational range shifts, and bird extinctions. Conserv Biol 22:140–150. doi:10.1111/j.1523-1739.2007.00852.x PubMedCrossRefGoogle Scholar
  57. Shochat E, Abramsky Z, Pinshow B, Whitehouse M (2002) Density-dependent habitat selection in migratory passerines during stopover: what causes the deviation from IFD? Evol Ecol 16:469–488. doi:10.1023/A:1020851801732 CrossRefGoogle Scholar
  58. Sillett TS, Holmes RT (2002) Variation in survivorship of a migratory songbird throughout its annual cycle. J Anim Ecol 71:296–308. doi:10.1046/j.1365-2656.2002.00599.x CrossRefGoogle Scholar
  59. Skagen SK et al (2005) Geography of spring landbird migration through riparian habitats in southwestern North America. Condor 107:212–227. doi:10.1650/7807 CrossRefGoogle Scholar
  60. Smallegange IM, Fiedler W, Köppen U, Geiter O, Bairlein F (2010) Tits on the move: exploring the impact of environmental change on blue tit and great tit migration distance. J Anim Ecol 79:350–357. doi:10.1111/j.1365-2656.2009.01643.x PubMedCrossRefGoogle Scholar
  61. Strode PK (2009) Spring tree species use by migrating Yellow-rumped Warblers in relation to phenology and food availability. Wilson J Ornithol 121:457–468. doi:10.1676/05-148.1 CrossRefGoogle Scholar
  62. Studds CE, Marra PP (2007) Linking fluctuations in rainfall to nonbreeding season performance in a long-distance migratory bird, Setophaga ruticilla. Clim Res 35:115–122. doi:10.3354/cr00718 CrossRefGoogle Scholar
  63. Studds CE, Marra PP (2011) Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird. Proc R Soc Lond B. doi:10.1098/rspb.2011.0332 Google Scholar
  64. Terrill SB, Ohmart RD (1984) Facultative extension of fall migration by Yellow-rumped Warblers (Dendroica coronata). Auk 101:427–438Google Scholar
  65. Thackeray SJ, Sparks TH, Frederiksen M, Burthe S, Bacon PJ, Bell JR, Botham MS, Brereton TM, Bright PW, Carvalho L, Cutton-Brock T, Dawson A, Edwards M, Elliot JM, Harrington R, Johns D, Jones ID, Jones JT, Di Leech, Roy DB, Scott WA, Smith M, Smithers RJ, Winfield IJ, Wanless S (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313. doi:10.1111/j.1365-2486.2010.02165.x CrossRefGoogle Scholar
  66. Tottrup AP, Rainio K, Coppack T, Lehikoinen E, Rahbek C, Thorup K (2010) Local temperature fine-tunes the timing of spring migration in birds. Integr Comp Biol 50:293–304. doi:10.1093/icb/icq028 PubMedCrossRefGoogle Scholar
  67. vanriper C (1980) The phenology of the dryland forest of Mauna Kea, Hawaii, and the impact of recent environmental perturbations. Biotropica 12:282–291. doi:10.2307/2387700 CrossRefGoogle Scholar
  68. Végvári Z, Bókony V, Barta Z, Kovács G (2010) Life history predicts advancement of avian spring migration in response to climate change. Glob Change Biol 16:1–11CrossRefGoogle Scholar
  69. Visser ME, Holleman LJM (2001) Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc R Soc Lond B 268:289–294. doi:10.1098/rspb.2000.1363 CrossRefGoogle Scholar
  70. Whittaker RH, Niering WA (1964) Vegetation of the Santa Catalina Mountains, Arizona. I. Ecological classification and distribution of species. J Arizona Acad Sci 3:9–34CrossRefGoogle Scholar
  71. Williams CM, Hellmann J, Sinclair BJ (2012) Lepidopteran species differ in susceptibility to winter warming. Clim Res 53:119–130. doi:10.3354/cr01100 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jherime L. Kellermann
    • 1
    • 2
    • 3
  • Charles van RiperIII
    • 1
    • 2
  1. 1.School of Natural Resources and EnvironmentUniversity of ArizonaTucsonUSA
  2. 2.Sonoran Desert Research Station, Southwest Biological Science Center, US Geological SurveyUniversity of ArizonaTucsonUSA
  3. 3.Natural Sciences DepartmentOregon Institute of TechnologyKlamath FallsUSA

Personalised recommendations