Abstract
Animals and plants are shifting the timing of key life events in response to climate change, yet despite recent documentation of escalating phenological change, scientists lack a full understanding of how and why phenological responses vary across space and among species. Here, we used over 7 million community-contributed bird observations to derive species-specific, spatially explicit estimates of annual spring migration phenology for 56 bird species across eastern North America. We show that changes in the spring arrival of migratory birds are coarsely synchronized with fluctuations in vegetation green-up and that the sensitivity of birds to plant phenology varied extensively. Bird arrival responded more synchronously with vegetation green-up at higher latitudes, where phenological shifts over time are also greater. Critically, species’ migratory traits explained variation in sensitivity to green-up, with species that migrate more slowly, arrive earlier and overwinter further north showing greater responsiveness to earlier springs. Identifying how and why species vary in their ability to shift phenological events is fundamental to predicting species’ vulnerability to climate change. Such variation in sensitivity across taxa, with long-distance neotropical migrants exhibiting reduced synchrony, may help to explain substantial declines in these species over the last several decades.
Similar content being viewed by others
Data availability
Bird occurrence data are available through eBird (https://ebird.org). Green-up (MCD12Q2) and land cover (MCD12Q1) data are available through the NASA/USGS Land Processes Distributed Active Archive Center (https://lpdaac.usgs.gov/). Interactive visualizations of all major analyses, as well as download capabilities of data products, are viewable on our R Shiny site at https://migratory-sensitivity.shinyapps.io/MigSen-app/ which is also available on Github (https://github.com/br-amaral/MigratorySensitivity_ShinyApp) and archived on Zenodo (https://doi.org/10.5281/zenodo.4549910).
Code availability
Code used to derive the arrival estimates and conduct the analyses of phenological sensitivity are available on Github (https://github.com/phenomismatch/Bird_Phenology; https://github.com/caseyyoungflesh/Pheno_sensitivity) and archived on Zenodo (https://doi.org/10.5281/zenodo.4532885; https://doi.org/10.5281/zenodo.4532799).
References
Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).
Cohen, J. M., Lajeunesse, M. J. & Rohr, J. R. A global synthesis of animal phenological responses to climate change. Nat. Clim. Change 8, 224–228 (2018).
Thackeray, S. J. et al. Phenological sensitivity to climate across taxa and trophic levels. Nature 535, 241–245 (2016).
Both, C., van Asch, M., Bijlsma, R. G., van den Burg, A. B. & Visser, M. E. Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J. Anim. Ecol. 78, 73–83 (2009).
Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M. & Lessells, C. M. Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. B 265, 1867–1870 (1998).
Stenseth, N. C. & Mysterud, A. Climate, changing phenology, and other life history traits: nonlinearity and match–mismatch to the environment. Proc. Natl Acad. Sci. USA 99, 13379–13381 (2002).
Blackford, C., Germain, R. M. & Gilbert, B. Species differences in phenology shape coexistence. Am. Nat. 195, E168–E180 (2020).
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).
Rudolf, V. H. W. The role of seasonal timing and phenological shifts for species coexistence. Ecol. Lett. 22, 1324–1338 (2019).
Mynott, J. Birds in the Ancient World: Winged Words (Oxford Univ. Press, 2018).
Hurlbert, A. H. & Liang, Z. Spatiotemporal variation in avian migration phenology: citizen science reveals effects of climate change. PLoS ONE 7, e31662 (2012).
Mayor, S. J. et al. Increasing phenological asynchrony between spring green-up and arrival of migratory birds. Sci. Rep. 7, 1902 (2017).
Horton, K. G. et al. Phenology of nocturnal avian migration has shifted at the continental scale. Nat. Clim. Change 10, 63–68 (2020).
Rosenberg, K. V. et al. Decline of the North American avifauna. Science 366, 120–124 (2019).
Sullivan, B. L. et al. The eBird enterprise: an integrated approach to development and application of citizen science. Biol. Conserv. 169, 31–40 (2014).
Friedl, M., Gray, J. & Sulla-Menashe, D. MCD12Q2 MODIS/Terra+Aqua Land Cover Dynamics Yearly L3 Global 500m SIN Grid v.6 (NASA EOSDIS Land Processes DAAC, accessed 26 March 2020); https://doi.org/10.5067/MODIS/MCD12Q2.006
Richardson, A. D., Hufkens, K., Milliman, T. & Frolking, S. Intercomparison of phenological transition dates derived from the PhenoCam Dataset V1.0 and MODIS satellite remote sensing. Sci. Rep. 8, 5679 (2018).
Cole, E. F., Long, P. R., Zelazowski, P., Szulkin, M. & Sheldon, B. C. Predicting bird phenology from space: satellite-derived vegetation green-up signal uncovers spatial variation in phenological synchrony between birds and their environment. Ecol. Evol. 5, 5057–5074 (2015).
Pettorelli, N. et al. The normalized difference vegetation index (NDVI): unforeseen successes in animal ecology. Clim. Res. 46, 15–27 (2011).
Winger, B. M., Auteri, G. G., Pegan, T. M. & Weeks, B. C. A long winter for the Red Queen: rethinking the evolution of seasonal migration. Biol. Rev. 94, 737–752 (2019).
Åkesson, S. et al. Timing avian long-distance migration: from internal clock mechanisms to global flights. Philos. Trans. R. Soc. B 372, 20160252 (2017).
Helm, B. et al. Two sides of a coin: ecological and chronobiological perspectives of timing in the wild. Philos. Trans. R. Soc. B 372, 20160246 (2017).
Haest, B., Hüppop, O. & Bairlein, F. The influence of weather on avian spring migration phenology: what, where and when? Glob. Change Biol. 24, 5769–5788 (2018).
Studds, C. E. & Marra, P. P. Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird. Proc. R. Soc. B 278, 3437–3443 (2011).
Thorup, K. et al. Resource tracking within and across continents in long-distance bird migrants. Sci. Adv. 3, e1601360 (2017).
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).
Van der Graaf, A., Stahl, J., Klimkowska, A., Bakker, J. P. & Drent, R. H. Surfing on a green wave—how plant growth drives spring migration in the Barnacle Goose Branta leucopsis. Ardea Wagening. 94, 567 (2006).
Schmaljohann, H. & Both, C. The limits of modifying migration speed to adjust to climate change. Nat. Clim. Change 7, 573–576 (2017).
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).
Zurell, D., Gallien, L., Graham, C. H. & Zimmermann, N. E. Do long-distance migratory birds track their niche through seasons? J. Biogeogr. 45, 1459–1468 (2018).
Horton, K. G. et al. Holding steady: little change in intensity or timing of bird migration over the Gulf of Mexico. Glob. Change Biol. 25, 1106–1118 (2019).
Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008).
Curley, S. R., Manne, L. L. & Veit, R. R. Differential winter and breeding range shifts: implications for avian migration distances. Divers. Distrib. 26, 415–425 (2020).
Root, T. Energy constraints on avian distributions and abundances. Ecology 69, 330–339 (1988).
La Sorte, F. A., Fink, D., Hochachka, W. M., DeLong, J. P. & Kelling, S. Population-level scaling of avian migration speed with body size and migration distance for powered fliers. Ecology 94, 1839–1847 (2013).
Somveille, M., Manica, A. & Rodrigues, A. S. L. Where the wild birds go: explaining the differences in migratory destinations across terrestrial bird species. Ecography 42, 225–236 (2019).
Knudsen, E. et al. Challenging claims in the study of migratory birds and climate change. Biol. Rev. 86, 928–946 (2011).
Allstadt, A. J. et al. Spring plant phenology and false springs in the conterminous US during the 21st century. Environ. Res. Lett. 10, 104008 (2015).
Franks, S. E. et al. The sensitivity of breeding songbirds to changes in seasonal timing is linked to population change but cannot be directly attributed to the effects of trophic asynchrony on productivity. Glob. Change Biol. 24, 957–971 (2018).
Both, C., Bouwhuis, S., Lessells, C. M. & Visser, M. E. Climate change and population declines in a long-distance migratory bird. Nature 441, 81–83 (2006).
Kharouba, H. M. & Wolkovich, E. M. Disconnects between ecological theory and data in phenological mismatch research. Nat. Clim. Change 10, 406–415 (2020).
Samplonius, J. M. et al. Strengthening the evidence base for temperature-mediated phenological asynchrony and its impacts. Nat. Ecol. Evol. 5, 155–164 (2021).
Abdala‐Roberts, L. et al. Tri‐trophic interactions: bridging species, communities and ecosystems. Ecol. Lett. 22, 2151–2167 (2019).
Burgess, M. D. et al. Tritrophic phenological match–mismatch in space and time. Nat. Ecol. Evol. 2, 970–975 (2018).
Helm, B., Van Doren, B. M., Hoffmann, D. & Hoffmann, U. Evolutionary response to climate change in migratory pied flycatchers. Curr. Biol. 29, 3714–3719 (2019).
Newson, S. E. et al. Long-term changes in the migration phenology of UK breeding birds detected by large-scale citizen science recording schemes. Ibis 158, 481–495 (2016).
Townsend, A. K. et al. The interacting effects of food, spring temperature, and global climate cycles on population dynamics of a migratory songbird. Glob. Change Biol. 22, 544–555 (2016).
Grüebler, M. U. & Naef-Daenzer, B. Fitness consequences of pre- and post-fledging timing decisions in a double-brooded passerine. Ecology 89, 2736–2745 (2008).
Lany, N. K. et al. Breeding timed to maximumimize reproductive success for a migratory songbird: the importance of phenological asynchrony. Oikos 125, 656–666 (2016).
Samplonius, J. M. & Both, C. Climate change may affect fatal competition between two bird species. Curr. Biol. 29, 327–331 (2019).
Potvin, D. A., Välimäki, K. & Lehikoinen, A. Differences in shifts of wintering and breeding ranges lead to changing migration distances in European birds. J. Avian Biol. 47, 619–628 (2016).
Bassett, F. & Cubie, D. Wintering hummingbirds in Alabama and Florida: species diversity, sex and age ratios, and site fidelity. J. Field Ornithol. 80, 154–162 (2009).
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).
Chmura, H. E. et al. The mechanisms of phenology: the patterns and processes of phenological shifts. Ecol. Monogr. 89, e01337 (2019).
Kharouba, H. M. et al. Global shifts in the phenological synchrony of species interactions over recent decades. Proc. Natl Acad. Sci. USA 115, 5211–5216 (2018).
Cressie, N., Calder, C. A., Clark, J. S., Hoef, J. M. V. & Wikle, C. K. Accounting for uncertainty in ecological analysis: the strengths and limitations of hierarchical statistical modeling. Ecol. Appl. 19, 553–570 (2009).
Miller-Rushing, A. J., Inouye, D. W. & Primack, R. B. How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. J. Ecol. 96, 1289–1296 (2008).
Miller-Rushing, A. J., Lloyd-Evans, T. L., Primack, R. B. & Satzinger, P. Bird migration times, climate change, and changing population sizes. Glob. Change Biol. 14, 1959–1972 (2008).
Barnes, R. dggridR: Discrete global grids for R. R package version 0.1.12 https://github.com/r-barnes/dggri (2017).
Data Zone (BirdLife International, 2019); http://datazone.birdlife.org/species/requestdis
Sulla-Menashe, D. et al. Hierarchical mapping of Northern Eurasian land cover using MODIS data. Remote Sens. Environ. 115, 392–403 (2011).
Friedl, M. & Sulla-Menashe, D. MCD12Q1 MODIS/Terra+Aqua Land Cover Type Yearly L3 Global 500m SIN Grid v.6 (NASA EOSDIS Land Processes DAAC, accessed 26 February 2020); https://doi.org/10.5067/MODIS/MCD12Q2.006
Wood, S. N. & Augustin, N. H. GAMs with integrated model selection using penalized regression splines and applications to environmental modelling. Ecol. Model. 157, 157–177 (2002).
Fink, D. et al. Spatiotemporal exploratory models for broad-scale survey data. Ecol. Appl. 20, 2131–2147 (2010).
Wood, S. N. Thin plate regression splines. J. R. Stat. Soc. B 65, 95–114 (2003).
Lindén, A., Meller, K. & Knape, J. An empirical comparison of models for the phenology of bird migration. J. Avian Biol. 48, 255–265 (2017).
Goodrich, B., Gabry, J., Ali, I. & Brilleman, S. rstanarm: Bayesian applied regression modeling via Stan. R package version 2.21.1 https://mc-stan.org/rstanarm (2020).
Carpenter, B. et al. Stan: a probabilistic programming language. J. Stat. Softw. https://www.jstatsoft.org/v076/i01 (2017).
Brooks, S. P. & Gelman, A. General methods for monitoring convergence of iterative simulations. J. Comput. Graph. Stat. 7, 434 (1998).
Besag, J. & Kooperberg, C. On conditional and intrinsic autoregression. Biometrika 82, 733 (1995).
Banerjee, S., Carlin, B. P. & Gelfand, A. E. Hierarchical Modeling and Analysis for Spatial Data (Chapman & Hall/CRC, 2004).
Morris, M. et al. Bayesian hierarchical spatial models: implementing the Besag York Mollié model in stan. Spat. Spatiotemporal Epidemiol. 31, 100301 (2019).
Stan Development Team. RStan: the R interface to Stan. R package version 2.17.3 http://mc-stan.org (2018).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
Monnahan, C. C., Thorson, J. T. & Branch, T. A. Faster estimation of Bayesian models in ecology using Hamiltonian Monte Carlo. Methods Ecol. Evol. 8, 339–348 (2017).
Gabry, J., Simpson, D., Vehtari, A., Betancourt, M. & Gelman, A. Visualization in Bayesian workflow. J. R. Stat. Soc. A 182, 389–402 (2019).
Gelman, A., Carlin, J. B, Stern, H. S. & Rubin, D. B. Bayesian Data Analysis (Chapman & Hall/CRC, 2014).
Finley, A. O. Comparing spatially-varying coefficients models for analysis of ecological data with non-stationary and anisotropic residual dependence: spatially-varying coefficients models. Methods Ecol. Evol. 2, 143–154 (2011).
Stan Modeling Language Users Guide and Reference Manual v. 2.18.0 (Stan Development Team, 2018).
Menzel, A., von Vopelius, J., Estrella, N., Schleip, C. & Dose, V. Farmers’ annual activities are not tracking the speed of climate change. Clim. Res. 32, 201–207 (2006).
Acknowledgements
Funding for this project was provided by the National Science Foundation (grant nos. EF 1703048 to M.W.T., 1702708 to A.H.H. and 2033263 to M.W.T.). M. Belitz, G. Di Cecco, E. Larsen, N. Neupane, L. Ries and J. Withey provided assistance and made suggestions that improved the paper. S. MacLean provided bird illustrations. We are grateful to the tens of thousands of eBird users who submit data each year.
Author information
Authors and Affiliations
Contributions
C.Y., J.S. and M.W.T. led conceptualization, formal analysis and writing of the original draft, with methodological, investigative and data curation support from A.A., R.P.G., A.H.H., R.L., S.J.M. and D.A.W.M. B.R.A. provided software and visualization support. The research project and supportive funding is administered by M.W.T. and A.H.H. All authors contributed to review and editing of drafts.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature Ecology & Evolution thanks Adriaan Dokter, Albert Phillimore and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 Study area of interest over North America.
Data were aggregated within each cell to calculate phenological measures and to characterize phenological change and sensitivity. Yellow cells represent the full extent of the study area. Cells were selected based on data density for both bird and green-up phenology (see Methods). Cell centres ranged from approximately 95° W to 54° W longitude and 26° N to 59° N latitude.
Extended Data Fig. 2 Derivation of the half-maximum from GAM results for each species–cell-year.
Circles at the top of each plot represent checklists where the species of interest was recorded, while circles at the bottom of each plot represent checklists where the species of interest was not recorded. Left panel: the green line represents the first detection of a given species in a given cell-year; the red line represents the first local maximum for the modelled probability of occurrence in an eBird checklist to come after the first detection; the gold line represents the probability of occurrence at that local maximum; the purple line represents Δp, the difference between the minimum modelled probability of occurrence prior to the first local maximum and the probability of occurrence at the local maximum (the minimum reporting probability here is 0); the dark blue line represents the probability of occurrence at \(\frac{1}{2}{{{\Delta}}}_p\), half the difference between the maximum and minimum probabilities plus the minimum reporting probability; the light blue line represents the half-maximum date, the ordinal date (day-of-year) at which the modelled probability of occurrence equals \(\frac{1}{2}{{{\Delta}}}_p\). Right panel: black lines represent posterior realizations of the GAM model fit for a single species–cell-year (500 realizations shown for clarity). The red lines represent the derived half-maximum date at each realization of the GAM model fit and were used to calculate the mean and 95% credible intervals for this metric.
Extended Data Fig. 3 Data processing pipeline using red-eyed vireo (Vireo olivaceus) as an example.
Estimates of arrival (half-maximum) were derived from generalized additive models (GAMs), which were then used as input for the intrinsic autoregressive (IAR) model to produce spatially smoothed estimates of arrival. The plot at the far left shows GAM results for a single cell-year for this species. Circles at the top of the plot represent eBird checklists in which red-eyed vireo was recorded, while circles at the bottom of the plot represent eBird checklists in which red-eyed vireo was not recorded. The black line represents the mean GAM fit, while the dashed red lines represent the 95% credible intervals. The solid blue and dashed blue lines represent the mean estimate and 95% credible intervals for the half-maximum, respectively. The plots in the centre column of the figure represent the estimated arrival date of this species over the study area for 2006. The plot at top centre represents the GAM-derived arrival estimates, while the plot at bottom centre represents the IAR-derived arrival estimates. Blue hues represent later arrival dates while pink hues represent earlier arrival dates for a given cell. The plots at far right represent a subset (the region bounded by the black box) of the maps in the centre column of the figure. Numbers in black represent the posterior mean of the arrival day (ordinal date), while the white numbers represent the posterior standard deviation of the arrival day.
Extended Data Fig. 4 Number of cells across the study area that met data requirements for each species and year.
Red hues represent more cells while white hues represent fewer cells. Only species that met minimum data requirements are shown. Since species-years with fewer than 3 valid cells were not run as a part of the IAR model (see Methods), each species–year has either 0 or 3 or greater valid cells.
Extended Data Fig. 5 Posterior estimates for a) ξAPG (the species-specific phenological sensitivities; equation 11) and b) γAPG (the species-specific effect of latitude on phenological sensitivities; equation 11).
Points represent posterior medians, thick lines represent 50% credible intervals, thin lines represent 95% credible intervals. The dashed grey line represents zero in each case.
Extended Data Fig. 6 Rate of change in green-up from 2002–2017 over the study area for (a) forest land cover types, and (b) all land cover types.
Colours for (a) and (b) represent the cell-specific posterior mean estimates of the rate of change in green-up over time (days change per year) with red hues representing more negative trends over time (earlier green-up) and yellow hues representing no trend over time. c, Posterior estimates for cell-specific rate of change in green-up for forest land cover types (black) and all land cover types (red). Points represent the posterior median estimates for the rate of change of each cell (ordered by latitude), thick lines represent 50% credible intervals, thin lines represent 95% credible intervals. The dashed grey line represents zero.
Extended Data Fig. 7 Directed acyclic graphs (DAGs) outlining the hierarchical models used in this study.
Boxes represent variables that were provided to the model, while ovals represent parameters estimated by the model. Corresponding equation numbers for each DAG given in lower right of each bounded box. Lettering corresponds to that shown in Supplementary Table 2, which provides descriptions of each variable represented in the DAGs.
Extended Data Fig. 8 Density plots for observed response variable data (y; corresponding to IAR-derived arrival dates for (a) and green-up dates for (b) and (c)) and response variable data simulated from the posterior predictive distribution (yrep).
These plots were used for graphical posterior predictive checks, to ensure that data simulated from the model were similar to the observed data for models examining (a) the sensitivity of bird arrival to vegetation phenology (Eqs. 9–14), (b) trends in green-up over time for forest land cover types (Eqs. 19–21), and (c) trends in green-up over time for all land cover types (Eqs. 19–21). Curves in red are a representation of the density of all response data used to fit each model. Curves in black are a representation of the density of data simulated from the posterior predictive distribution. Each iteration of the posterior chain yields a simulated dataset. Here 250 datasets simulated from the posterior predictive distribution are displayed (250 separate black lines). The general similarities between the red lines and black lines demonstrate that the models simulate data similar to the observed data.
Supplementary information
Supplementary Information
Supplementary Methods, References and Tables 1–3.
Rights and permissions
About this article
Cite this article
Youngflesh, C., Socolar, J., Amaral, B.R. et al. Migratory strategy drives species-level variation in bird sensitivity to vegetation green-up. Nat Ecol Evol 5, 987–994 (2021). https://doi.org/10.1038/s41559-021-01442-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-021-01442-y
- Springer Nature Limited
This article is cited by
-
Avian migration clocks in a changing world
Journal of Comparative Physiology A (2024)
-
Experimental warming causes mismatches in alpine plant-microbe-fauna phenology
Nature Communications (2023)
-
Adaptation to climate change through dispersal and inherited timing in an avian migrant
Nature Ecology & Evolution (2023)
-
Artificial light at night is a top predictor of bird migration stopover density
Nature Communications (2023)
-
Inconsistent shifts in warming and temperature variability are linked to reduced avian fitness
Nature Communications (2023)