Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Advances in breeding phenology outpace latitudinal and elevational shifts for North American birds tracking temperature

Nature Ecology & Evolution (2024)Cite this article

Subjects

Abstract

Terrestrial species can respond to a warming climate in multiple ways, including shifting in space (via latitude or elevation) and time (via phenology). Evidence for such shifts is often assessed independent of other temperature-tracking mechanisms; critically, no study has compared shifts across all three spatiotemporal dimensions. Here we used two continental-scale monitoring databases to estimate trends in the breeding latitude (311 species), elevation (251 species) and phenology (111 species) of North American landbirds over 27 years, with a shared pool of 102 species. We measured the magnitude of shifts and compared them relative to average regional warming (that is, shift ratios). Species shifted poleward (1.1 km per year, mean shift ratio 11%) and to higher elevations (1.2 m per year, mean shift ratio 17%), while also shifting their breeding phenology earlier (0.08 days per year, mean shift ratio 28%). These general trends belied substantial variation among species, with some species shifting faster than climate, whereas others shifted more slowly or in the opposite direction. Across the three dimensions (n = 102), birds cumulatively tracked temperature at 33% of current warming rates, 64% of which was driven by advances in breeding phenology as opposed to geographical shifts. A narrow focus on spatial dimensions of climate tracking may underestimate the responses of birds to climate change; phenological shifts may offer an alternative for birds—and probably other organisms—to conserve their thermal niche in a warming world.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: North American landbirds are shifting poleward, upslope and earlier in their breeding phenology.
Fig. 2: Birds are cumulatively better able to track rising temperatures across multiple dimensions than through a single dimension alone.
Fig. 3: Combined shift ratios across three spatiotemporal dimensions generally fall short of needed temperature tracking.

Similar content being viewed by others

Data availability

Bird spatial data were extracted from the US Geological Survey Breeding Bird Survey (https://www.pwrc.usgs.gov/BBS/RawData/), whereas phenological data were extracted from the Monitoring Avian Productivity and Survivorship programme (https://www.birdpop.org/pages/maps.php). Temperature data were extracted from Daymet (https://daymet.ornl.gov/). All aggregated data and modelling code used in the analyses as well as derived results are available via Figshare at https://doi.org/10.6084/m9.figshare.26412718.v1 (ref. 72).

References

  1. Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).

    Article  CAS  PubMed  Google Scholar 

  2. Chen, I.-C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).

    Article  CAS  PubMed  Google Scholar 

  3. Lenoir, J. et al. Species better track climate warming in the oceans than on land. Nat. Ecol. Evol. 4, 1044–1059 (2020).

    Article  PubMed  Google Scholar 

  4. La Sorte, F. A. & Thompson, F. R. Poleward shifts in winter ranges of North American birds. Ecology 88, 1803–1812 (2007).

    Article  PubMed  Google Scholar 

  5. Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).

    Article  Google Scholar 

  6. Martins, P. M., Anderson, M. J., Sweatman, W. L. & Punnett, A. J. Significant shifts in latitudinal optima of North American birds. Proc. Natl Acad. Sci. USA 121,e2307525121 (2024).

    Article  CAS  PubMed  Google Scholar 

  7. Neate-Clegg, M. H. C. & Tingley, M. W. Building a mechanistic understanding of climate-driven elevational shifts in birds. PLoS Clim. 2, e0000174 (2023).

    Article  Google Scholar 

  8. Freeman, B. G., Song, Y., Feeley, K. J. & Zhu, K. Montane species track rising temperatures better in the tropics than in the temperate zone. Ecol. Lett. 24, 1697–1708 (2021).

    Article  PubMed  Google Scholar 

  9. Freeman, B. G. & Class Freeman, A. M. Rapid upslope shifts in New Guinean birds illustrate strong distributional responses of tropical montane species to global warming. Proc. Natl Acad. Sci. USA 111, 4490–4494 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Forero-Medina, G., Terborgh, J., Socolar, S. J. & Pimm, S. L. Elevational ranges of birds on a tropical montane gradient lag behind warming temperatures. PLoS ONE 6, e28535 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Massimino, D., Johnston, A. & Pearce-Higgins, J. W. The geographical range of British birds expands during 15 years of warming. Bird. Study 62, 523–534 (2015).

    Article  Google Scholar 

  12. Tingley, M. W., Koo, M. S., Moritz, C., Rush, A. C. & Beissinger, S. R. The push and pull of climate change causes heterogeneous shifts in avian elevational ranges. Glob. Chang. Biol. 18, 3279–3290 (2012).

    Article  Google Scholar 

  13. Paquette, A. & Hargreaves, A. L. Biotic interactions are more often important at species’ warm versus cool range edges. Ecol. Lett. 24, 2427–2438 (2021).

    Article  PubMed  Google Scholar 

  14. Freeman, B. G., Lee-Yaw, J. A., Sunday, J. M. & Hargreaves, A. L. Expanding, shifting and shrinking: the impact of global warming on species’ elevational distributions. Glob. Ecol. Biogeogr. 27, 1268–1276 (2018).

    Article  Google Scholar 

  15. Anderson, A. S. et al. Immigrants and refugees: the importance of dispersal in mediating biotic attrition under climate change. Glob. Chang. Biol. 18, 2126–2134 (2012).

    Article  Google Scholar 

  16. Guo, F., Lenoir, J. & Bonebrake, T. C. Land-use change interacts with climate to determine elevational species redistribution. Nat. Commun. 9, 1315 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Auer, S. K. & King, D. I. Ecological and life-history traits explain recent boundary shifts in elevation and latitude of western North American songbirds. Glob. Ecol. Biogeogr. 23, 867–875 (2014).

    Article  Google Scholar 

  18. Zuckerberg, B., Woods, A. M. & Porter, W. F. Poleward shifts in breeding bird distributions in New York State. Glob. Chang. Biol. 15, 1866–1883 (2009).

    Article  Google Scholar 

  19. Romano, A., Garamszegi, L. Z., Rubolini, D. & Ambrosini, R. Temporal shifts in avian phenology across the circannual cycle in a rapidly changing climate: a global meta-analysis.Ecol. Monogr. 93, e1552 (2023).

    Article  Google Scholar 

  20. Post, E., Steinman, B. A. & Mann, M. E. Acceleration of phenological advance and warming with latitude over the past century. Sci. Rep. 8, 3927 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Youngflesh, C. et al. Migratory strategy drives species-level variation in bird sensitivity to vegetation green-up. Nat. Ecol. Evol. 5, 987–994 (2021).

    Article  PubMed  Google Scholar 

  22. Neate-Clegg, M. H. C. & Tingley, M. W. Adult male birds advance spring migratory phenology faster than females and juveniles across North America. Glob. Chang. Biol. 29, 341–354 (2023).

    Article  CAS  PubMed  Google Scholar 

  23. Horton, K. G. et al. Phenology of nocturnal avian migration has shifted at the continental scale. Nat. Clim. Change 10, 63–68 (2020).

    Article  Google Scholar 

  24. Lehikoinen, A. et al. Phenology of the avian spring migratory passage in Europe and North America: asymmetric advancement in time and increase in duration. Ecol. Indic. 101, 985–991 (2019).

    Article  Google Scholar 

  25. Zettlemoyer, M. A. & Peterson, M. L. Does phenological plasticity help or hinder range shifts under climate change? Front. Ecol. Evol. 9, 689192 (2021).

    Article  Google Scholar 

  26. Hällfors, M. H. et al. Combining range and phenology shifts offers a winning strategy for boreal Lepidoptera. Ecol. Lett. 24, 1619–1632 (2021).

    Article  PubMed  Google Scholar 

  27. Marra, P. P., Francis, C. M., Mulvihill, R. S. & Moore, F. R. The influence of climate on the timing and rate of spring bird migration. Oecologia 142, 307–315 (2005).

    Article  PubMed  Google Scholar 

  28. Socolar, J. B., Epanchin, P. N., Beissinger, S. R. & Tingley, M. W. Phenological shifts conserve thermal niches in North American birds and reshape expectations for climate-driven range shifts. Proc. Natl Acad. Sci. USA 114, 12976–12981 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Youngflesh, C. et al. Demographic consequences of phenological asynchrony for North American songbirds. Proc. Natl Acad. Sci. USA 120, e2221961120 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Saino, N. et al. Climate warming, ecological mismatch at arrival and population decline in migratory birds.Proc. R. Soc. B 278, 835–842 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Møller, A. P., Rubolini, D. & Lehikoinen, E. 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 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Saracco, J. F., Siegel, R. B., Helton, L., Stock, S. L. & DeSante, D. F. Phenology and productivity in a montane bird assemblage: trends and responses to elevation and climate variation. Glob. Chang. Biol. 25, 985–996 (2019).

    Article  PubMed  Google Scholar 

  33. Rosenberg, K. V. et al. Decline of the North American avifauna. Science 366, 120–124 (2019).

    Article  CAS  PubMed  Google Scholar 

  34. Rushing, C. S., Royle, J. A., Ziolkowski, D. J. & Pardieck, K. L. Migratory behavior and winter geography drive differential range shifts of eastern birds in response to recent climate change. Proc. Natl Acad. Sci. USA 117, 12897–12903 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Angert, A. L. et al. Do species’ traits predict recent shifts at expanding range edges? Ecol. Lett. 14, 677–689 (2011).

    Article  PubMed  Google Scholar 

  36. Pounds, J., Fogden, M. & Campbell, J. Biological response to climate change on a tropical mountain. Nature 398, 611–615 (1999).

    Article  CAS  Google Scholar 

  37. Şekercioğlu, Ç. H., Schneider, S. H., Fay, J. P. & Loarie, S. R. Climate change, elevational range shifts, and bird extinctions. Conserv. Biol. 22, 140–150 (2008).

    Article  PubMed  Google Scholar 

  38. Colwell, R. K., Brehm, G., Cardelús, C. L., Gilman, A. C. & Longino, J. T. Global warming, elevational range shifts, and lowland biotic attrition in the Wet Tropics. Science 322, 258–261 (2008).

    Article  CAS  PubMed  Google Scholar 

  39. Wright, S. J., Muller-Landau, H. C. & Schipper, J. The future of tropical species on a warmer planet. Conserv. Biol. 23, 1418–1426 (2009).

    Article  PubMed  Google Scholar 

  40. Neate-Clegg, M. H. C., Jones, S. E. I., Tobias, J. A., Newmark, W. D. & Şekercioǧlu, Ç. H. Ecological correlates of elevational range shifts in tropical birds. Front. Ecol. Evol. 9, 621749 (2021).

    Article  Google Scholar 

  41. Spence, A. R. & Tingley, M. W. The challenge of novel abiotic conditions for species undergoing climate-induced range shifts. Ecography 43, 1571–1590 (2020).

    Article  Google Scholar 

  42. Sparks, T. H. Phenology and the changing pattern of bird migration in Britain. Int. J. Biometeorol. 42, 134–138 (1999).

    Article  Google Scholar 

  43. Bradley, N. L., Leopold, A. C., Ross, J. & Huffaker, W. Phenological changes reflect climate change in Wisconsin. Proc. Natl Acad. Sci. USA 96, 9701–9704 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hällfors, M. H. et al. Shifts in timing and duration of breeding for 73 boreal bird species over four decades.Proc. Natl Acad. Sci. USA 117, 18557–18565 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zimova, M., Willard, D. E., Winger, B. M. & Weeks, B. C. Widespread shifts in bird migration phenology are decoupled from parallel shifts in morphology.J. Anim. Ecol. 90, 2348–2361 (2021).

    Article  PubMed  Google Scholar 

  46. Albright, T. P. et al. Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc. Natl Acad. Sci. USA 114, 2283–2288 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Araújo, M. B. et al. Heat freezes niche evolution. Ecol. Lett. 16, 1206–1219 (2013).

    Article  PubMed  Google Scholar 

  48. Price, T., Kirkpatrick, M. & Arnold, S. J. Directional selection and the evolution of breeding date in birds. Science 240, 798–799 (1988).

    Article  CAS  PubMed  Google Scholar 

  49. Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 26, 285–291 (2011).

    Article  PubMed  Google Scholar 

  50. Jankowski, J. E., Londoño, G. A., Robinson, S. K. & Chappell, M. A. Exploring the role of physiology and biotic interactions in determining elevational ranges of tropical animals. Ecography 36, 1–12 (2012).

    Article  Google Scholar 

  51. Greig, E. I., Wood, E. M. & Bonter, D. N. Winter range expansion of a hummingbird is associated with urbanization and supplementary feeding.Proc. Biol. Sci. 284, 20170256 (2017).

    PubMed  PubMed Central  Google Scholar 

  52. Hallman, T. A., Guélat, J., Antoniazza, S., Kéry, M. & Sattler, T. Rapid elevational shifts of Switzerland’s avifauna and associated species traits. Ecosphere 13, e4194 (2022).

    Article  Google Scholar 

  53. Grier, J. W. Ban of DDT and subsequent recovery of reproduction in bald eagles. Science 218, 1232–1235 (1982).

    Article  CAS  PubMed  Google Scholar 

  54. Voogt, J. A. & Oke, T. R. Thermal remote sensing of urban climates.Remote Sens. Environ. 86, 370–384 (2003).

    Article  Google Scholar 

  55. Lavergne, S., Mouquet, N., Thuiller, W. & Ronce, O. Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Annu. Rev. Ecol. Evol. Syst. 41, 321–350 (2010).

    Article  Google Scholar 

  56. Wiens, J. J. et al. Niche conservatism as an emerging principle in ecology and conservation biology. Ecol. Lett. 13, 1310–1324 (2010).

    Article  PubMed  Google Scholar 

  57. Linck, E. B., Freeman, B. G., Cadena, C. D. & Ghalambor, C. K. Evolutionary conservatism will limit responses to climate change in the tropics. Biol. Lett. 17, 20210363 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Tingley, M. W., Monahan, W. B., Beissinger, S. R. & Moritz, C. Birds track their Grinnellian niche through a century of climate change. Proc. Natl Acad. Sci. USA 106, 19637–19643 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Pollock, H. S., Brawn, J. D. & Cheviron, Z. A. Heat tolerances of temperate and tropical birds and their implications for susceptibility to climate warming. Funct. Ecol. 35, 93–104 (2021).

    Article  Google Scholar 

  60. Maclean, I. M. D. & Early, R. Macroclimate data overestimate range shifts of plants in response to climate change. Nat. Clim. Chang. 13, 484–490 (2023).

    Article  Google Scholar 

  61. Youngflesh, C., Saracco, J. F., Siegel, R. B. & Tingley, M. W. Abiotic conditions shape spatial and temporal morphological variation in North American birds. Nat. Ecol. Evol. 6, 1860–1870 (2022).

    Article  PubMed  Google Scholar 

  62. Sauer, J. R. et al. The North American Breeding Bird Survey, Results and Analysis 1966–2015. Version 2.07.2019 (USGS Patuxent Wildlife Resarch Center, 2017).

  63. Terry Chesser, R. et al. Sixty-second supplement to the American Ornithological Society’s check-list of North American birds. Ornithology 140, ukab037 (2023).

    Google Scholar 

  64. Danielson, J. J. & Gesch, D. B. Global Multi-resolution Terrain Elevation Data 2010 (GMTED2010). Open-File Rep. 2011-1073 (USGS, 2011).

  65. Desante, D. F. et al. MAPS Manual 2016 Protocol, The Institute for Bird Populations, Point Reyes Station, California. (2016).

  66. Desante, D. F., Williams, O. E. & Burton, K. M. The Monitoring Avian Productivity and Survivorship (MAPS) Program: overview and progress. USDA For. Serv. Gen. Tech. Rep. 208–222 (USDA, 1993).

  67. Plummer, M. JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In Proc. 3rd International Workshop on Distributed Statistical Computing (DSC 2003) 1–10 (2003).

  68. Su, Y.-S. & Yajima, M. R2jags: Using R to Run ‘JAGS’, Version 0.7-1 https://cran.r-project.org/web/packages/R2jags (2021).

  69. Thornton, M. M. et al. Daymet: Daily Surface Weather Data on a 1-km Grid for North America, Version 4 https://doi.org/10.3334/ORNLDAAC/2129 (2020).

  70. Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

    Article  CAS  PubMed  Google Scholar 

  71. Revell, L. J. phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  72. Neate-Clegg, M. Latitudinal, elevational, and phenological shifts for North American birds. Figshare https://doi.org/10.6084/m9.figshare.26412718.v1 (2024).

Download references

Acknowledgements

We thank the thousands of volunteers who participate in the BBS and the organizers at the US Geological Survey. In addition, we thank the many dedicated volunteers who have collected and donated data to the MAPS programme, as well as The Institute for Bird Populations for developing and curating the MAPS programme. Data used in this analysis were made available via funding from the National Science Foundation (grant no. EF 1703048). B.A.T. was supported by the National Aeronautics and Space Administration under the FINESST grant no. 80NSSC22K1530.

Author information

Authors and Affiliations

  1. Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA

    Montague H. C. Neate-Clegg, Benjamin A. Tonelli & Morgan W. Tingley

Authors
  1. Montague H. C. Neate-Clegg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benjamin A. Tonelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Morgan W. Tingley
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.H.C.N.-C. and M.W.T. developed an analytical and inferential framework based on an initial conceptualization by M.W.T. M.H.C.N.-C. led formal analysis, assisted by B.A.T. and M.W.T. M.H.C.N.-C. wrote a first draft with review and editing contributed by B.A.T. and M.W.T.

Corresponding authors

Correspondence to Montague H. C. Neate-Clegg or Morgan W. Tingley.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Maria Hällfors and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Maps showing the distribution of (A) Breeding Bird Survey routes and (B) Monitoring Avian Productivity and Survivorship banding stations.

Sites are colored by elevation (m). Maps were created using the package rnaturalearth (v. 1.0.1, https://docs.ropensci.org/rnaturalearth/).

Extended Data Fig. 2 The spatial coverage of survey sites.

The latitudinal and elevational distribution of (A–B) Breeding Bird Survey routes and (C–D) Monitoring Avian Productivity and Survivorship banding stations are displayed as histograms.

Extended Data Fig. 3 Latitudinal shift rates for 311 North American landbird species over 27 years.

Points show the mean shift rate and bars the 95% Bayesian credible intervals. Points and bars are purple when not overlapping 0. Sample sizes (number of annual latitudinal estimates) are also shown for each species.

Extended Data Fig. 4 The relationship between shift rates and mean position for North American landbirds.

Across species, (a) latitudinal shifts are greater for more southerly species while (b) elevational shifts are greater for high-elevation species, but (c) phenological shift rates are not associated with mean capture day. Each point represents a species while the colored lines show the mean relationships plus 95% Bayesian credible intervals.

Extended Data Fig. 5 Elevational shift rates for 251 North American landbird species over 27 years.

Points show the mean shift rate and bars the 95% Bayesian credible intervals. Points and bars are green when not overlapping 0. Sample sizes (number of annual elevational estimates) are also shown for each species.

Extended Data Fig. 6 Phenological shift rates for 111 North American landbird species over 27 years.

Points show the mean shift rate and bars the 95% Bayesian credible intervals. Points and bars are orange when not overlapping 0. Sample sizes (number of year-by-station phenological estimates) are also shown for each species.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Neate-Clegg, M.H.C., Tonelli, B.A. & Tingley, M.W. Advances in breeding phenology outpace latitudinal and elevational shifts for North American birds tracking temperature. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02536-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41559-024-02536-z

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing