Longer-lived tropical songbirds reduce breeding activity as they buffer impacts of drought

Abstract

Droughts are expected to increase in frequency and severity with climate change. Population impacts of such harsh environmental events are theorized to vary with life history strategies among species. However, existing demographic models generally do not consider behavioural plasticity that may modify the impact of harsh events. Here we show that tropical songbirds in the New and Old Worlds reduced reproduction during drought, with greater reductions in species with higher average long-term survival. Large reductions in reproduction by longer-lived species were associated with higher survival during drought than predrought years in Malaysia, whereas shorter-lived species maintained reproduction and survival decreased. Behavioural strategies of longer-lived, but not shorter-lived, species mitigated the effect of increasing drought frequency on long-term population growth. Behavioural plasticity can buffer the impact of climate change on populations of some species and differences in plasticity among species related to their life histories are critical for predicting population trajectories.

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Fig. 1: Possible demographic consequences of drought in tropical rainforest for songbirds.
Fig. 2: Tropical songbirds reduce breeding activity in drought years on two continents.
Fig. 3: Relationships of reproductive activity and survival across Malaysian species.
Fig. 4: General demographic consequences of drought.
Fig. 5: Population elasticity and simulated population growth under historic frequencies of drought.
Fig. 6: Drought frequency and simulated population growth under alternative climate change scenarios for the future.

Data availability

Life history data are available in Dryad (https://doi.org/10.5061/dryad.gf1vhhmm8). Source data are provided with this paper.

Code availability

R code for population models are available in Dryad (https://doi.org/10.5061/dryad.gf1vhhmm8).

References

  1. 1.

    Dai, A. Increasing drought under global warming in observations and models. Nat. Clim. Change 3, 52–58 (2013).

    Google Scholar 

  2. 2.

    Cook, B. I., Smerdon, J. E., Seager, R. & Coats, S. Global warming and 21st century drying. Clim. Dynam. 43, 2607–2627 (2014).

    Google Scholar 

  3. 3.

    Trenberth, K. E. et al. Global warming and changes in drought. Nat. Clim. Change 4, 17–22 (2014).

    Google Scholar 

  4. 4.

    Webb, J. K., Brook, B. W. & Shine, R. What makes a species vulnerable to extinction? Comparative life‐history traits of two sympatric snakes. Ecol. Res. 17, 59–67 (2002).

    Google Scholar 

  5. 5.

    Clark, M. E. & Martin, T. E. Modeling tradeoffs in avian life history traits and consequences for population growth. Ecol. Model. 209, 110–120 (2007).

    Google Scholar 

  6. 6.

    MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967).

  7. 7.

    Bennett, P. M. & Owens, I. P. F. Variation in extinction risk among birds: chance or evolutionary predisposition? Proc. R. Soc. Lond. B 264, 401–408 (1997).

    Google Scholar 

  8. 8.

    Pfister, C. A. Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. Proc. Natl Acad. Sci. USA 95, 213–218 (1998).

    CAS  Google Scholar 

  9. 9.

    Nelson, R. J. Simulated drought affect male reproductive function in deer mice (Permoyscus maniculatus bairdii). Phys. Zool. 66, 99–114 (1993).

    Google Scholar 

  10. 10.

    Winne, C. T., Willson, J. D. & Gibbons, J. W. Income breeding allows an aquatic snake Seminatrix pygaea to reproduce normally following prolonged drought-induced aestivation. J. Anim. Ecol. 75, 1352–1360 (2006).

    Google Scholar 

  11. 11.

    Boag, P. T. & Grant, P. R. Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Galapagos. Science 214, 82–85 (1981).

    CAS  Google Scholar 

  12. 12.

    Grant, P. R., Grant, B. R., Keller, L. F. & Petren, K. Effect of El Niño events on Darwin’s finch productivity. Ecology 81, 2442–2457 (2000).

    Google Scholar 

  13. 13.

    Cruz-McDonnell, K. K. & Wolf, B. O. Rapid warming and drought negatively impact population size and reproductive dynamics of an avian predator in the arid southwest. Glob. Change Biol. 22, 237–253 (2016).

    Google Scholar 

  14. 14.

    Sperry, J. H. & Weatherhead, P. J. Prey-mediated effects of drought on condition and survival in a terrestrial snake. Ecology 89, 2770–2776 (2008).

    Google Scholar 

  15. 15.

    Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manage. 259, 660–684 (2010).

    Google Scholar 

  16. 16.

    Calow, P. The cost of reproduction—a physiological approach. Biol. Rev. 54, 23–40 (1979).

    CAS  Google Scholar 

  17. 17.

    Reznick, D. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44, 257–267 (1985).

    Google Scholar 

  18. 18.

    Flatt, T. Survival costs of reproduction in Drosophila. Exp. Geron. 46, 369–375 (2011).

    Google Scholar 

  19. 19.

    Forbes, M. R. L., Clark, R. G., Weatherhead, P. J. & Armstrong, T. Risk-taking by female ducks: intra- and interspecific tests of nest defense theory. Behav. Ecol. Sociobiol. 34, 79–85 (1994).

    Google Scholar 

  20. 20.

    Ghalambor, C. K. & Martin, T. E. Fecundity-survival trade-offs and parental risk-taking in birds. Science 292, 494–497 (2001).

    CAS  Google Scholar 

  21. 21.

    Møller, A. P. & Liang, W. Tropical birds take small risks. Behav. Ecol. 24, 267–272 (2012).

    Google Scholar 

  22. 22.

    Deutsch, C. A. et al. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl Acad. Sci. USA 105, 6668–6672 (2008).

    CAS  Google Scholar 

  23. 23.

    Tewksbury, J. J., Huey, R. B. & Deutsch, C. A. Putting the heat on tropical animals. Science 320, 1296–1297 (2008).

    CAS  Google Scholar 

  24. 24.

    Martin, T. E., Riordan, M. M., Repin, R., Mouton, J. C. & Blake, W. M. Apparent annual survival estimates of tropical songbirds better reflect life history variation when based on intensive field methods. Glob. Ecol. Biogeogr. 26, 1386–1397 (2017).

    Google Scholar 

  25. 25.

    Martin, T. E. Age-related mortality explains life history strategies of tropical and temperate songbirds. Science 349, 966–970 (2015).

    CAS  Google Scholar 

  26. 26.

    Martin, T. E., Oteyza, J. C., Boyce, A. J., Lloyd, P. & Ton, R. Adult mortality probability and nest predation rates explain parental effort in warming eggs with consequences for embryonic development time. Am. Nat. 186, 223–236 (2015).

    Google Scholar 

  27. 27.

    Arslan, N. Ş. & Martin, T. E. Reproductive biology of Grey-breasted Wood-Wren (Henicorhina leucophrys): a comparative study of tropical and temperate wrens. Wilson J. Ornithol. 131, 1–11 (2019).

    Google Scholar 

  28. 28.

    Stutchbury, B. J. & Morton, E. S. Behavioral Ecology of Tropical Birds Ch. 5 (Academic Press, 2001).

  29. 29.

    Collar, N. in Handbook of the Birds of the World Alive (eds del Hoyo, J. et al.) (Lynx Edicions, 2019); https://doi.org/10.2173/bow.borwht1.01

  30. 30.

    Caswell, H. Matrix Population Models: Construction, Analysis, and Interpretation (Sinauer, 2001).

  31. 31.

    Wisdom, M. J., Mills, L. S. & Doak, D. F. Life stage simulation analysis: estimating vital-rate effects on population growth for conservation. Ecology 81, 628–641 (2000).

    Google Scholar 

  32. 32.

    Muñoz, A. P., Kéry, M., Martins, P. V. & Ferraz, G. Age effects on survival of Amazon forest birds and the latitudinal gradient in bird survival. Auk 135, 299–313 (2018).

    Google Scholar 

  33. 33.

    Lloyd, P. & Martin, T. E. Fledgling survival increases with development time and adult survival across north and south temperate zones. Ibis 158, 135–143 (2016).

    Google Scholar 

  34. 34.

    Ropelewski, C. F. & Jones, P. D. An extension of the Tahiti-Darwin Southern Oscillation Index. Mon. Weather Rev. 115, 2161–2165 (1987).

    Google Scholar 

  35. 35.

    Aiba, S. I. & Kitayama, K. Effects of the 1997–98 El Nino drought on rain forests of Mount Kinabalu, Borneo. J. Trop. Ecol. 18, 215–230 (2002).

    Google Scholar 

  36. 36.

    Hirshfield, M. F. & Tinkle, D. W. Natural selection and the evolution of reproductive effort. Proc. Natl Acad. Sci. USA 72, 2227–2231 (1975).

    CAS  Google Scholar 

  37. 37.

    Martin, T. E., Ton, R. & Oteyza, J. C. Adaptive influence of extrinsic and intrinsic factors on variation of incubation periods among tropical and temperate passerines. Auk 135, 101–113 (2018).

    Google Scholar 

  38. 38.

    Wilmers, C. C. & Post, E. Predicting the influence of wolf-provided carrion on scavenger community dynamics under climate change scenarios. Glob. Change Biol. 12, 403–409 (2006).

    Google Scholar 

  39. 39.

    Lenssen, N. et al. Improvements in the GISTEMP uncertainty model. J. Geophys. Res. Atmos. 124, 6307–6326 (2019).

    Google Scholar 

  40. 40.

    IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) 1311–1393 (Cambridge Univ. Press, 2013).

  41. 41.

    Taylor, I. H. et al. The impact of climate mitigation on projections of future drought. Hydrol. Earth Syst. Sci. 17, 2339–2358 (2013).

    Google Scholar 

  42. 42.

    Kitayama, K. An altitudinal transect study of the vegetation on Mount Kinabalu, Borneo. Vegetation 102, 149–171 (1992).

    Google Scholar 

  43. 43.

    Blake, J. G. & Loiselle, B. A. Enigmatic declines in bird numbers in lowland forest of eastern Ecuador may be a consequence of climate change. Peer J. 3, e1177 (2015).

    Google Scholar 

  44. 44.

    Mitchell, A. E., Tuh, F. & Martin, T. E. Breeding biology of an endemic Bornean turdid, the Fruithunter (Chlamydochaera jefferyi), and life history comparisons with Turdus species of the world. Wilson J. Ornithol. 129, 36–45 (2017).

    Google Scholar 

  45. 45.

    White, G. C. & Burnham, K. P. Program MARK: survival estimation from populations of marked animals. Bird Study 46, 120–139 (1999).

    Google Scholar 

  46. 46.

    Shaffer, T. L. A unified approach to analyzing nest success. Auk 121, 526–540 (2004).

    Google Scholar 

  47. 47.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information–Theoretic Approach (Springer-Verlag, 2002).

  48. 48.

    Pradel, R., Hines, J. E., Lebreton, J. D. & Nichols, J. D. Capture–recapture survival models taking account of transients. Biometrics 53, 60–72 (1997).

    Google Scholar 

  49. 49.

    Burnham, K. P., Anderson, D. R., White, G. C., Brownie, C. & Pollock, K. H. Design and Analysis Methods for Fish Survival Experiments Based on Release–recapture (Amer Fisheries Society, 1987).

  50. 50.

    Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 125, 1–15 (1985).

    Google Scholar 

  51. 51.

    Orme, D. The caper package: comparative analysis of phylogenetics and evolution in R. R package version 3.5.0 http://cran.r-project.org/web/packages/caper/vignettes/caper.pdf (2013).

  52. 52.

    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).

    CAS  Google Scholar 

  53. 53.

    Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008).

    CAS  Google Scholar 

  54. 54.

    Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. R package version 2.75 http://mesquiteproject.org (2011).

  55. 55.

    Pagel, M. D. A method for the analysis of comparative data. J. Theor. Biol. 156, 431–442 (1992).

    Google Scholar 

  56. 56.

    Symonds, M. R. & Blomberg, S. P. in Modern Phylogenetic Comparative Methods and their Application in Evolutionary Biology (eds Garamszegi, L. Z.) Ch. 5 (Springer, 2014).

  57. 57.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Google Scholar 

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Acknowledgements

We appreciate helpful comments from J. Brodie, C. Conway, B. Heidinger, L. S. Mills and our laboratory on the manuscript. We are grateful to C. Armstad and numerous field assistants for help collecting data for this study. We are grateful to S. Williams for advice on survival analyses and to Sabah Parks and the Sabah Biodiversity Centre in Malaysia and C. Bosque, INPARQUES and Fonacit in Venezuela for logistical support. This work was supported by the National Science Foundation (Graduate Research Fellowship and grant nos. DEB-1701672 to J.C.M.; DEB-1241041, DEB-1651283 and IOS-1656120 to T.E.M.) and the Drollinger Family Charitable Foundation. This work was conducted under University of Montana IACUC no. 059-10TMMCWRU. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the US Government.

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Authors

Contributions

T.E.M. designed the study, analysed the field data and obtained funding. J.C.M. conducted all climate and demographic modelling. Both authors collected data and contributed to writing and revising the manuscript.

Corresponding author

Correspondence to Thomas E. Martin.

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The authors declare no competing interests.

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Peer review information Nature Climate Change thanks Peter Grant and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Extended data

Extended Data Fig. 1 Phylogenetic relationships of all study species from birdtree.org.

Species from the Venezuela site are depicted blue and species from the Malaysia site are depicted in orange. Abbreviations based on scientific names in parentheses are the eight species used for population simulation analyses, and include long-lived in red, short-lived in blue, and wet-habitat species in yellow-green. Source data

Extended Data Fig. 2 Linear mixed model analyses of reproductive output in drought versus non-drought years.

Differences in clutch size and number of young that fledged (left the nest) were compared between drought versus non-drought years, while including species and year as random factors.

Supplementary information

Source data

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Source data for Fig. 1.

Source Data Fig. 2

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Source Data Fig. 3

Source data for Fig. 3.

Source Data Fig. 5

Source data for Fig. 5.

Source Data Fig. 6

Source data for Fig. 6.

Source Data Extended Data Fig. 1

Source data for Extended Data Fig. 1.

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Martin, T.E., Mouton, J.C. Longer-lived tropical songbirds reduce breeding activity as they buffer impacts of drought. Nat. Clim. Chang. 10, 953–958 (2020). https://doi.org/10.1038/s41558-020-0864-3

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