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  • Brief Communication
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Behavioural plasticity is associated with reduced extinction risk in birds

Abstract

Behavioural plasticity is believed to reduce species vulnerability to extinction, yet global evidence supporting this hypothesis is lacking. We address this gap by quantifying the extent to which birds are observed behaving in novel ways to obtain food in the wild; based on a unique dataset of >3,800 novel behaviours, we show that species with a higher propensity to innovate are at a lower risk of global extinction and are more likely to have increasing or stable populations than less innovative birds. These results mainly reflect a higher tolerance of innovative species to habitat destruction, the main threat for birds.

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Fig. 1: Behavioural plasticity is associated with extinction risk.
Fig. 2: Coefficient estimates of models predicting extinction risk and population trends.

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Data availability

The dataset used in this study is available from Dryad (https://doi.org/10.5061/dryad.sf7m0cg2k).

Code availability

The R code used in this study is available from Dryad (https://doi.org/10.5061/dryad.sf7m0cg2k).

References

  1. Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014).

    Article  CAS  PubMed  Google Scholar 

  2. IUCN. The IUCN Red List of Threatened Species Version 2019-1. IUCN Red List of Threatened Species https://www.iucnredlist.org/en (2019).

  3. 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).

    Article  Google Scholar 

  4. Purvis, A., Gittleman, J. L., Cowlishaw, G. & Mace, G. M. Predicting extinction risk in declining species. Proc. R. Soc. Lond. B 267, 1947–1952 (2000).

    Article  CAS  Google Scholar 

  5. Reed, J. M. The role of behavior in recent avian extinctions and endangerments. Conserv. Biol. 13, 232–241 (1999).

    Article  Google Scholar 

  6. Sol, D. in Animal Innovation (eds Reader, S. M. & Laland, K. N.) Ch. 3 (Oxford Univ. Press, 2003).

  7. Sih, A. Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim. Behav. 85, 1077–1088 (2013).

    Article  Google Scholar 

  8. Maspons, J., Molowny-Horas, R. & Sol, D. Behaviour, life history and persistence in novel environments. Phil. Trans. R. Soc. B 374, 20180056 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Barrett, B., Zepeda, E., Pollack, L., Munson, A. & Sih, A. Counter-culture: does social learning help or hinder adaptive response to human-induced rapid environmental change?. Front. Ecol. Evol. 7, 183 (2019).

    Article  Google Scholar 

  10. Lefebvre, L., Reader, S. M. & Sol, D. Brains, innovations and evolution in birds and primates. Brain. Behav. Evol. 63, 233–246 (2004).

    Article  PubMed  Google Scholar 

  11. Dukas, R. Evolutionary biology of insect learning. Annu. Rev. Entomol. 53, 145–160 (2008).

    Article  CAS  PubMed  Google Scholar 

  12. Sol, D. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 5, 130–133 (2009).

    Article  PubMed  Google Scholar 

  13. Ricklefs, R. E. The cognitive face of avian life histories. Wilson J. Ornithol. 116, 119–133 (2004).

    Google Scholar 

  14. Godfrey-Smith, P. in The Evolution of Intelligence (eds Sternberg, I. R. & Kaufman, J.) 233–249 (Lawrence Erlbaum Associates, 2002).

  15. Sayol, F. et al. Environmental variation and the evolution of large brains in birds. Nat. Commun. 7, 13971 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Owens, I. P. & Bennett, P. M. Ecological basis of extinction risk in birds: habitat loss versus human persecution and introduced predators. Proc. Natl Acad. Sci. USA 97, 12144–12148 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gonzalez-Voyer, A., González-Suárez, M., Vilà, C. & Revilla, E. Larger brain size indirectly increases vulnerability to extinction in mammals. Evolution 70, 1364–1375 (2016).

    Article  PubMed  Google Scholar 

  18. Fristoe, T. S., Iwaniuk, A. N. & Botero, C. A. Big brains stabilize populations and facilitate colonization of variable habitats in birds. Nat. Ecol. Evol. 1, 1706–1715 (2017).

    Article  PubMed  Google Scholar 

  19. Lefebvre, L., Whittle, P., Lascaris, E. & Finkelstein, A. Feeding innovations and forebrain size in birds. Anim. Behav. 53, 549–560 (1997).

    Article  Google Scholar 

  20. Reader, S. M. & Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436–4441 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sol, D., Sayol, F., Ducatez, S. & Lefebvre, L. The life-history basis of behavioural innovations. Phil. Trans. R. Soc. B 371, 20150187 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Sol, D., Duncan, R. P., Blackburn, T. M., Cassey, P. & Lefebvre, L. Big brains, enhanced cognition, and response of birds to novel environments. Proc. Natl Acad. Sci. USA 102, 5460–5465 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hobbs, J. Use of tools by the White-winged chough. Emu 71, 84–85 (1971).

    Article  Google Scholar 

  24. Overington, S. E., Morand-Ferron, J., Boogert, N. J. & Lefebvre, L. Technical innovations drive the relationship between innovativeness and residual brain size in birds. Anim. Behav. 78, 1001–1010 (2009).

    Article  Google Scholar 

  25. Ducatez, S. & Shine, R. Drivers of extinction risk in terrestrial vertebrates. Conserv. Lett. 10, 186–194 (2017).

    Article  Google Scholar 

  26. Berkunsky, I. et al. Current threats faced by Neotropical parrot populations. Biol. Conserv. 214, 278–287 (2017).

    Article  Google Scholar 

  27. Tulloch, V. J. D., Plagányi, É. E., Matear, R., Brown, C. J. & Richardson, A. J. Ecosystem modelling to quantify the impact of historical whaling on Southern Hemisphere baleen whales. Fish Fish. 19, 117–137 (2018).

    Article  Google Scholar 

  28. Cowlishaw, G. & Dunbar, R. Primate Conservation Biology (Univ. of Chicago Press, 2000).

  29. Nicolakakis, N., Sol, D. & Lefebvre, L. Behavioural flexibility predicts species richness in birds, but not extinction risk. Anim. Behav. 65, 445–452 (2003).

    Article  Google Scholar 

  30. Rodrigues, A. S. L., Pilgrim, J. D., Lamoreux, J. F., Hoffmann, M. & Brooks, T. M. The value of the IUCN Red List for conservation. Trends Ecol. Evol. 21, 71–76 (2006).

    Article  PubMed  Google Scholar 

  31. Mace, G. M. et al. Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv. Biol. 22, 1424–1442 (2008).

    Article  PubMed  Google Scholar 

  32. Cooper, N., Bielby, J., Thomas, G. H. & Purvis, A. Macroecology and extinction risk correlates of frogs. Glob. Ecol. Biogeogr. 17, 211–221 (2008).

    Article  Google Scholar 

  33. Davidson, A. D., Hamilton, M. J., Boyer, A. G., Brown, J. H. & Ceballos, G. Multiple ecological pathways to extinction in mammals. Proc. Natl Acad. Sci. USA 106, 10702–10705 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Siliceo, I. & Díaz, J. A. A comparative study of clutch size, range size, and the conservation status of island vs. mainland lacertid lizards. Biol. Conserv. 143, 2601–2608 (2010).

    Article  Google Scholar 

  35. Schaefer, H.-C., Jetz, W. & Böhning-Gaese, K. Impact of climate change on migratory birds: community reassembly versus adaptation. Glob. Ecol. Biogeogr. 17, 38–49 (2008).

    Google Scholar 

  36. Lee, T. M. & Jetz, W. Unravelling the structure of species extinction risk for predictive conservation science. Proc. R. Soc. Lond. B 278, 1329–1338 (2011).

    Article  Google Scholar 

  37. Overington, S. E., Griffin, A. S., Sol, D. & Lefebvre, L. Are innovative species ecological generalists? A test in North American birds. Behav. Ecol. 22, 1286–1293 (2011).

    Article  Google Scholar 

  38. Lefebvre, L., Juretic, N., Nicolakakis, N. & Timmermans, S. Is the link between forebrain size and feeding innovations caused by confounding variables? A study of Australian and North American birds. Anim. Cogn. 4, 91–97 (2001).

    Article  Google Scholar 

  39. Lefebvre, L. et al. Feeding innovations and forebrain size in Australasian birds. Behaviour 135, 1077–1097 (1998).

    Article  Google Scholar 

  40. Timmermans, S., Lefebvre, L., Boire, D. & Basu, P. Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain. Behav. Evol. 56, 196–203 (2000).

    Article  CAS  PubMed  Google Scholar 

  41. de Oliveira Casadei, L. & Plácido Guimarães, J. Registros fotográficos da Garça-branca, Ardea alba, predando outras espécies de aves na cidade de Praia Grande/SP. Atual. Ornitológicas 196, 26 (2017).

    Google Scholar 

  42. Baglione, V. & Canestrari, D. Kleptoparasitism and temporal segregation of sympatric corvids foraging in a refuse dump. Auk 126, 566–578 (2009).

    Article  Google Scholar 

  43. Atkore, V. M. & Dasgupta, S. Himalayan Griffon Gyps himalayensis feeding on chir pine Pinus roxburghii needles. Indian Birds 2, 172 (2006).

    Google Scholar 

  44. Bondo, K. J. & Brigham, R. M. Plasticity by migrant yellow-rumped warblers: foraging indoors during unseasonable cold weather. Northwest. Nat. 97, 139–143 (2016).

    Article  Google Scholar 

  45. Lock, J. Behavioral exploitation of human maritime activities by the great cormorant Phalacrocorax carbo. Mar. Ornithol. 41, 79–81 (2013).

    Google Scholar 

  46. Ducatez, S., Clavel, J. & Lefebvre, L. Ecological generalism and behavioural innovation in birds: technical intelligence or the simple incorporation of new foods? J. Anim. Ecol. 84, 79–89 (2015).

    Article  PubMed  Google Scholar 

  47. Navarrete, A. F., Reader, S. M., Street, S. E., Whalen, A. & Laland, K. N. The coevolution of innovation and technical intelligence in primates. Phil. Trans. R. Soc. B 371, 20150186 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Arbilly, M. & Laland, K. N. The magnitude of innovation and its evolution in social animals. Proc. R. Soc. B 284, 20162385 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Lefebvre, L. Taxonomic counts of cognition in the wild. Biol. Lett. 7, 631–633 (2011).

    Article  PubMed  Google Scholar 

  50. Nicolakakis, N. & Lefebvre, L. Forebrain size and innovation rate in european birds: feeding, nesting and confounding variables. Behaviour 137, 1415–1429 (2000).

    Article  Google Scholar 

  51. Ducatez, S. & Lefebvre, L. Patterns of research effort in birds. PLoS ONE 9, e89955 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Sol, D., Lefebvre, L. & Rodríguez-Teijeiro, J. D. Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Proc. R. Soc. B 272, 1433–1441 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Data Zone (Birdlife International, 2019); http://datazone.birdlife.org/home

  54. Dunning, J. B. CRC Handbook of Avian Body Masses (CRC Press, 2007).

  55. del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & de Juana, E. Handbook of the Birds of the World Alive (Lynx Edicions, 2017); http://www.hbw.com

  56. Ducatez, S., Tingley, R. & Shine, R. Using species co-occurrence patterns to quantify relative habitat breadth in terrestrial vertebrates. Ecosphere 5, art152 (2014).

    Article  Google Scholar 

  57. Bennett, P. M. & Owens, I. P. F. Evolutionary Ecology of Birds: Life Histories, Mating Systems and Extinction (Oxford Univ. Press, 2002).

  58. Wilman, H. et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027–2027 (2014).

    Article  Google Scholar 

  59. Hayward, M. W. The need to rationalize and prioritize threatening processes used to determine threat status in the IUCN red list. Conserv. Biol. 23, 1568–1576 (2009).

    Article  PubMed  Google Scholar 

  60. 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 

  61. Ericson, P. G. P. et al. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol. Lett. 2, 543–547 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  63. Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  64. Wild, S. et al. Long-term decline in survival and reproduction of dolphins following a marine heatwave. Curr. Biol. 29, R239–R240 (2019).

    Article  CAS  PubMed  Google Scholar 

  65. Yeh, P. J., Hauber, M. E. & Price, T. D. Alternative nesting behaviours following colonisation of a novel environment by a passerine bird. Oikos 116, 1473–1480 (2007).

    Article  Google Scholar 

  66. Lapiedra, O., Schoener, T. W., Leal, M., Losos, J. B. & Kolbe, J. J. Predator-driven natural selection on risk-taking behavior in anole lizards. Science 360, 1017–1020 (2018).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported by funds from the Spanish government (grant no. CGL2017-90033-P) to D.S. and a Discovery grant from NSERC Canada to L.L. We are grateful to J. DeVore for discussion and for her comments on a previous version of the manuscript, to J.-N. Audet and the Sol laboratory for discussions, and to O. Lapiedra and S. Bressler for providing photos included in Fig. 1.

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Authors and Affiliations

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Contributions

S.D. and L.L. initiated the project. L.L. compiled the innovation dataset. S.D., D.S. and F.S. compiled the remaining data. S.D. designed the analyses with the help of D.S. and F.S., and ran the analyses. S.D. wrote a first draft of the manuscript. All authors edited and approved the manuscript.

Corresponding author

Correspondence to Simon Ducatez.

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Extended data

Extended Data Fig. 1 Effect size of the regression coefficients of technical innovativeness (a), technical innovation rate (b), consumer innovativeness (c) or consumer innovation rate (d) and covariables on bird extinction risk and population trend estimated with Bayesian phylogenetic mixed models.

The effect is considered significant when its credibility interval (CI) does not overlap zero. Extinction risk (ordinal, from 1 = LC to 5 = CR) was modelled so that a negative effect of, for example, innovativeness, means that innovative species have a lower risk of extinction, and population trend (ordinal, from 1 = decreasing to 3 = increasing) was modelled so that a positive effect of, for example, innovativeness, means that innovative species are more likely to have increasing populations. All parameters are in the same model which also includes phylogeny and geographic region as random factors. Error bars are the 95% CIs estimated by MCMCglmm.

Extended Data Fig. 2 Coefficient estimates of models predicting extinction risk as a function of innovativeness (left panel) or innovation rate (right panel) according to the type of threat. Most endangered birds are exposed to more than one threat, making isolating species responses to a specific threat difficult.

We therefore compared the effect of innovation propensity on extinction risk in subsets of species exposed vs. not exposed to each threat. If innovation propensity limits the effects of a specific threat on extinction risk, it should decrease extinction risk in species exposed to the threat, but not in species that are not exposed. If innovation propensity does not buffer the effect of a certain threat, its effect on extinction risk should not differ between exposed and non-exposed species. Posterior effect size means, credibility intervals and species numbers are shown.

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Ducatez, S., Sol, D., Sayol, F. et al. Behavioural plasticity is associated with reduced extinction risk in birds. Nat Ecol Evol 4, 788–793 (2020). https://doi.org/10.1038/s41559-020-1168-8

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