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.
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
The dataset used in this study is available from Dryad (https://doi.org/10.5061/dryad.sf7m0cg2k).
The R code used in this study is available from Dryad (https://doi.org/10.5061/dryad.sf7m0cg2k).
Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014).
IUCN. The IUCN Red List of Threatened Species Version 2019-1. IUCN Red List of Threatened Species https://www.iucnredlist.org/en (2019).
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).
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).
Reed, J. M. The role of behavior in recent avian extinctions and endangerments. Conserv. Biol. 13, 232–241 (1999).
Sol, D. in Animal Innovation (eds Reader, S. M. & Laland, K. N.) Ch. 3 (Oxford Univ. Press, 2003).
Sih, A. Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim. Behav. 85, 1077–1088 (2013).
Maspons, J., Molowny-Horas, R. & Sol, D. Behaviour, life history and persistence in novel environments. Phil. Trans. R. Soc. B 374, 20180056 (2019).
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).
Lefebvre, L., Reader, S. M. & Sol, D. Brains, innovations and evolution in birds and primates. Brain. Behav. Evol. 63, 233–246 (2004).
Dukas, R. Evolutionary biology of insect learning. Annu. Rev. Entomol. 53, 145–160 (2008).
Sol, D. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 5, 130–133 (2009).
Ricklefs, R. E. The cognitive face of avian life histories. Wilson J. Ornithol. 116, 119–133 (2004).
Godfrey-Smith, P. in The Evolution of Intelligence (eds Sternberg, I. R. & Kaufman, J.) 233–249 (Lawrence Erlbaum Associates, 2002).
Sayol, F. et al. Environmental variation and the evolution of large brains in birds. Nat. Commun. 7, 13971 (2016).
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).
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).
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).
Lefebvre, L., Whittle, P., Lascaris, E. & Finkelstein, A. Feeding innovations and forebrain size in birds. Anim. Behav. 53, 549–560 (1997).
Reader, S. M. & Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436–4441 (2002).
Sol, D., Sayol, F., Ducatez, S. & Lefebvre, L. The life-history basis of behavioural innovations. Phil. Trans. R. Soc. B 371, 20150187 (2016).
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).
Hobbs, J. Use of tools by the White-winged chough. Emu 71, 84–85 (1971).
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).
Ducatez, S. & Shine, R. Drivers of extinction risk in terrestrial vertebrates. Conserv. Lett. 10, 186–194 (2017).
Berkunsky, I. et al. Current threats faced by Neotropical parrot populations. Biol. Conserv. 214, 278–287 (2017).
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).
Cowlishaw, G. & Dunbar, R. Primate Conservation Biology (Univ. of Chicago Press, 2000).
Nicolakakis, N., Sol, D. & Lefebvre, L. Behavioural flexibility predicts species richness in birds, but not extinction risk. Anim. Behav. 65, 445–452 (2003).
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).
Mace, G. M. et al. Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv. Biol. 22, 1424–1442 (2008).
Cooper, N., Bielby, J., Thomas, G. H. & Purvis, A. Macroecology and extinction risk correlates of frogs. Glob. Ecol. Biogeogr. 17, 211–221 (2008).
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).
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).
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).
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).
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).
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).
Lefebvre, L. et al. Feeding innovations and forebrain size in Australasian birds. Behaviour 135, 1077–1097 (1998).
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).
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).
Baglione, V. & Canestrari, D. Kleptoparasitism and temporal segregation of sympatric corvids foraging in a refuse dump. Auk 126, 566–578 (2009).
Atkore, V. M. & Dasgupta, S. Himalayan Griffon Gyps himalayensis feeding on chir pine Pinus roxburghii needles. Indian Birds 2, 172 (2006).
Bondo, K. J. & Brigham, R. M. Plasticity by migrant yellow-rumped warblers: foraging indoors during unseasonable cold weather. Northwest. Nat. 97, 139–143 (2016).
Lock, J. Behavioral exploitation of human maritime activities by the great cormorant Phalacrocorax carbo. Mar. Ornithol. 41, 79–81 (2013).
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).
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).
Arbilly, M. & Laland, K. N. The magnitude of innovation and its evolution in social animals. Proc. R. Soc. B 284, 20162385 (2017).
Lefebvre, L. Taxonomic counts of cognition in the wild. Biol. Lett. 7, 631–633 (2011).
Nicolakakis, N. & Lefebvre, L. Forebrain size and innovation rate in european birds: feeding, nesting and confounding variables. Behaviour 137, 1415–1429 (2000).
Ducatez, S. & Lefebvre, L. Patterns of research effort in birds. PLoS ONE 9, e89955 (2014).
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).
Data Zone (Birdlife International, 2019); http://datazone.birdlife.org/home
Dunning, J. B. CRC Handbook of Avian Body Masses (CRC Press, 2007).
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
Ducatez, S., Tingley, R. & Shine, R. Using species co-occurrence patterns to quantify relative habitat breadth in terrestrial vertebrates. Ecosphere 5, art152 (2014).
Bennett, P. M. & Owens, I. P. F. Evolutionary Ecology of Birds: Life Histories, Mating Systems and Extinction (Oxford Univ. Press, 2002).
Wilman, H. et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027–2027 (2014).
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).
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).
Ericson, P. G. P. et al. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol. Lett. 2, 543–547 (2006).
Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008).
Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).
Wild, S. et al. Long-term decline in survival and reproduction of dolphins following a marine heatwave. Curr. Biol. 29, R239–R240 (2019).
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).
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).
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.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
About this article
Cite this article
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
Evolution & Development (2021)
Frontiers in Ecology and Evolution (2021)
Ornithological Applications (2021)
Conservation Letters (2021)
Proceedings of the Royal Society B: Biological Sciences (2021)