Animal tolerance towards humans can be a key factor facilitating wildlife-human coexistence, yet traits predicting its direction and magnitude across tropical animals are poorly known. Using 10,249 observations for 842 bird species inhabiting open tropical ecosystems in Africa, South America, and Australia, we find that avian tolerance towards humans was lower (i.e., escape distance was longer) in rural rather than urban populations and in populations exposed to lower human disturbance (measured as human footprint index). In addition, larger species and species with larger clutches and enhanced flight ability are less tolerant to human approaches and escape distances increase when birds were approached during the wet season compared to the dry season and from longer starting distances. Identification of key factors affecting animal tolerance towards humans across large spatial and taxonomic scales may help us to better understand and predict the patterns of species distributions in the Anthropocene.

Africa Conservation Programme World Parrot Trust Glanmor House Hayle TR27 4HB UK

AP Leventis Ornithological Research Institute University of Jos Jos Nigeria

BirdLife South Africa Isdell House 17 Hume Road Dunkeld West 2196 Gauteng South Africa

British Trust for Ornithology University of Stirling Stirling FK9 4LA UK

C4 EcoSolutions Tokai 7966 Cape Town South Africa

Centre for Biological Diversity University of St Andrews St Andrews Fife KY16 9TH UK

Centre for Statistics in Ecology Environment and Conservation Department of Statistical Sciences University of Cape Town Rondebosch 7700 South Africa

Colecciones Biológicas Instituto de Investigación de Recursos Biológicos Alexander von Humboldt Villa de Leyva Boyacá Colombia

Departamento de Ciências Ambientais Universidade Federal de São Carlos Rodovia João Leme dos Santos km 110 18086 330 Sorocaba SP Brazil

Department of Biodiversity Conservation and Management University for Development Studies P O Box TL 1882 Tamale Ghana

Department of Biological Sciences University of Cape Town Cape Town South Africa

Department of Biology and Ecology University of Ostrava Chittussiho 10 710 00 Ostrava Czech Republic

Department of Biology Norwegian University of Science and Technology NTNU NO 7091 Trondheim Norway

Department of Biology Vrije Universiteit Brussel Pleinlaan 2 1050 Brussels Belgium

Department of Computer Science Aalto University PO Box 15400 00076 Aalto Finland

Department of Ecology and Evolutionary Biology University of California 621 Young Drive South Los Angeles CA 90095 1606 USA

Department of Ecology and Natural Resource Management Norwegian University of Life Sciences P O Box 5003 Norwegian 1432 Ås Norway

Department of Environmental Sciences College of Agriculture and Environmental Sciences University of South Africa PO Box 392 Pretoria 0003 South Africa

Department of Genetics Ecology and Evolution Federal University of Minas Gerais Presidente Antônio Carlos avenue 6627 31270 901 Belo Horizonte Brazil

Department of Physical Geography and Geoecology Faculty of Science Charles University Albertov 6 128 43 Prague 2 Czech Republic

Department of Wildlife Ecology and Conservation Chinhoyi University of Technology P Bag 7724 Chinhoyi Zimbabwe

Department of Zoology and Wildlife Conservation University of Dar es Salaam P O Box 35064 Dar es Salaam Tanzania

Department of Zoology Faculty of Science Charles University Viničná 7 128 44 Praha 2 Czech Republic

Department of Zoology Faculty of Science University of Lagos Akoka Yaba Nigeria

Department of Zoology Poznań University of Life Sciences Wojska Polskiego 71c 60 625 Poznań Poland

Faculty of Biological Sciences University of Zielona Góra Prof Z Szafrana 1 65 516 Zielona Góra Poland

Faculty of Environmental Sciences Czech University of Life Sciences Prague Kamýcká 129 165 00 Prague Czech Republic

FitzPatrick Institute of African Ornithology DSI NRF Centre of Excellence University of Cape Town Rondebosch 7701 South Africa

Grupo de investigación ECOTONOS Facultad de Ciencias Básicas e Ingeniería Universidad de Los Llanos Villavicencio Colombia

Grupo de Pesquisa e Conservação da Arara azul de lear Bahia Brazil

Institute for Advanced Study Technical University of Munich 85748 Garching Germany

Institute of Agricultural Research for Development 1st Main road Nkolbisson Yaoundé Yaoundé Cameroon

Institute of Vertebrate Biology Czech Academy of Sciences Květná 8 603 65 Brno Czech Republic

International Crane Foundation Endangered Wildlife Trust P O Box 33944 Lusaka Zambia

International Fund for Animal Welfare 22 Airdrie Road Estlea Harare Zimbabwe

Laboratorio de Biología Evolutiva de Vertebrados Departamento de Ciencias Biológicas Universidad de los Andes Bogotá Colombia

Laboratory and Museum of Evolutionary Ecology Department of Ecology Faculty of Humanities and Natural Sciences University of Prešov 17 novembra 1 081 16 Prešov Slovakia

Organisation for Tropical Studies PO Box 33 Skukuza 1350 South Africa

Programa de Biología Universidad Distrital Francisco José de Caldas Bogotá Colombia

Programa de Pós Graduação em Ecologia Instituto Nacional de Pesquisas da Amazônia Avenida André Araújo 69067 375 Manaus AM Brazil

Research and Education for Sustainable Actions 9934 Katanda Chinhoyi Zimbabwe

Research Institute for the Environment and Livelihoods Charles Darwin University Darwin NT 0909 Australia

School of Animal Plant and Environmental Sciences University of the Witwatersrand Private Bag 3 Wits 2050 Johannesburg South Africa

School of Life and Environmental Sciences Faculty of Science Engineering and the Built Environment Deakin University 221 Burwood Hwy Burwood VIC 3125 Australia

School of Medicine Institute of Life Course and Medical Sciences Faculty of Health and Life Sciences University of Liverpool Ashton Street L69 3GS Liverpool UK

TETFUND Centre of Excellence in Biodiversity Conservation and Ecosystem Management University of Lagos Lagos Nigeria

TUM School of Life Sciences Ecoclimatology Technical University of Munich 85354 Freising Germany

Zoology Department National Museums of Kenya Museum Hill Rd P O BOX 40658 00100 Nairobi Kenya

Zobrazit více v PubMed

Shorrocks, B. & Bates, W. The Biology of African Savannahs (Oxford University Press, 2015).

Parr CL, Lehmann CER, Bond WJ, Hoffmann WA, Andersen AN. Tropical grassy biomes: misunderstood, neglected, and under threat. Trends Ecol. Evol. 2014;29:205–213. doi: 10.1016/j.tree.2014.02.004. PubMed DOI

Beaumont LJ, et al. Impacts of climate change on the world’s most exceptional ecoregions. Proc. Natl Acad. Sci. USA. 2011;108:2306–2311. doi: 10.1073/pnas.1007217108. PubMed DOI PMC

Ripple WJ, et al. Extinction risk is most acute for the world’s largest and smallest vertebrates. Proc. Natl Acad. Sci. USA. 2017;114:10678–10683. doi: 10.1073/pnas.1702078114. PubMed DOI PMC

Ducatez S, Sol D, Sayol F, Lefebvre L. Behavioural plasticity is associated with reduced extinction risk in birds. Nat. Ecol. Evol. 2020;4:788–793. doi: 10.1038/s41559-020-1168-8. PubMed DOI

Lima SL, Dill LM. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 1990;68:619–640. doi: 10.1139/z90-092. DOI

Frid A, Dill L. Human-caused disturbance stimuli as a form of predation risk. Conserv. Ecol. 2002;6:11.

Steven R, Pickering C, Guy Castley J. A review of the impacts of nature based recreation on birds. J. Environ. Manag. 2011;92:2287–2294. doi: 10.1016/j.jenvman.2011.05.005. PubMed DOI

Navarro C, de Lope F, Marzal A, Møller AP. Predation risk, host immune response, and parasitism. Behav. Ecol. 2004;15:629–635. doi: 10.1093/beheco/arh054. DOI

Møller AP, Samia DSM, Weston MA, Guay P-J, Blumstein DT. American exceptionalism: population trends and flight initiation distances in birds from three continents. PLoS ONE. 2014;9:e107883. doi: 10.1371/journal.pone.0107883. PubMed DOI PMC

Samia DSM, Nakagawa S, Nomura F, Rangel TF, Blumstein DT. Increased tolerance to humans among disturbed wildlife. Nat. Commun. 2015;6:8877. doi: 10.1038/ncomms9877. PubMed DOI PMC

Díaz M, et al. The geography of fear: a latitudinal gradient in anti-predator escape distances of birds across Europe. PLoS ONE. 2013;8:e64634. doi: 10.1371/journal.pone.0064634. PubMed DOI PMC

Ghalambor CK, Martin TE. Fecundity-survival trade-offs and parental risk-taking in birds. Science. 2001;292:494–497. doi: 10.1126/science.1059379. PubMed DOI

Ripple WJ, et al. Bushmeat hunting and extinction risk to the world’s mammals. R. Soc. Open Sci. 2016;3:160498. doi: 10.1098/rsos.160498. PubMed DOI PMC

Jetz W, Sekercioglu CH, Böhning-Gaese K, Burgess N, Powell G. The worldwide variation in avian clutch size across species and space. PLoS Biol. 2008;6:e303. doi: 10.1371/journal.pbio.0060303. PubMed DOI PMC

Møller AP, Liang W. Tropical birds take small risks. Behav. Ecol. 2013;24:267–272. doi: 10.1093/beheco/ars163. DOI

Valcu M, Dale J, Griesser M, Nakagawa S, Kempenaers B. Global gradients of avian longevity support the classic evolutionary theory of ageing. Ecography. 2014;37:930–938. doi: 10.1111/ecog.00929. DOI

Stankowich T, Blumstein DT. Fear in animals: a meta-analysis and review of risk assessment. Proc. R. Soc. Lond. B: Biol. Sci. 2005;272:2627–2634. PubMed PMC

Blumstein DT. Developing an evolutionary ecology of fear: how life history and natural history traits affect disturbance tolerance in birds. Anim. Behav. 2006;71:389–399. doi: 10.1016/j.anbehav.2005.05.010. DOI

Guay PJ, van Dongen WFD, Robinson RW, Blumstein DT, Weston MA. AvianBuffer: an interactive tool for characterising and managing wildlife fear responses. Ambio. 2016;45:841–851. doi: 10.1007/s13280-016-0779-4. PubMed DOI PMC

Livezey KB, Fernández-Juricic E, Blumstein DT. Database of bird flight initiation distances to assist in estimating effects from human disturbance and delineating buffer areas. J. Fish. Wildl. Manag. 2016;7:181–191. doi: 10.3996/082015-JFWM-078. DOI

Ekanayake, K. E. et al. Ecological and environmental predictors of escape among birds on a large tropical island. Behav. Ecol. Sociobiol. 76, 31 (2022).

Mikula P, et al. Adjusting risk-taking to the annual cycle of long-distance migratory birds. Sci. Rep. 2018;8:13989. doi: 10.1038/s41598-018-32252-1. PubMed DOI PMC

Mikula P, et al. Face mask-wear did not affect large-scale patterns in escape and alertness of urban and rural birds during the COVID-19 pandemic. Sci. Total Environ. 2021;793:148672. doi: 10.1016/j.scitotenv.2021.148672. PubMed DOI PMC

Carrete M, Tella JL. High individual consistency in fear of humans throughout the adult lifespan of rural and urban burrowing owls. Sci. Rep. 2013;3:1–7. doi: 10.1038/srep03524. PubMed DOI PMC

Carrete M, et al. Heritability of fear of humans in urban and rural populations of a bird species. Sci. Rep. 2016;6:31060. doi: 10.1038/srep31060. PubMed DOI PMC

Symonds MRE, et al. Time since urbanization but not encephalisation is associated with increased tolerance of human proximity in birds. Front Ecol. Evol. 2016;4:117. doi: 10.3389/fevo.2016.00117. DOI

McKinney ML. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 2006;127:247–260. doi: 10.1016/j.biocon.2005.09.005. DOI

Croci S, Butet A, Cleargeau P. Does urbanization filter birds on the basis of their biological traits. Condor. 2008;110:223–240. doi: 10.1525/cond.2008.8409. DOI

Ferenc M, et al. Large-scale commonness is the best predictor of bird species presence in European cities. Urban Ecosyst. 2017;21:369–377.

Sol D, González-Lagos C, Moreira D, Maspons J, Lapiedra O. Urbanisation tolerance and the loss of avian diversity. Ecol. Lett. 2014;17:942–950. doi: 10.1111/ele.12297. PubMed DOI

Maklakov AA, Immler S, Gonzalez-Voyer A, Rönn J, Kolm N. Brains and the city: big-brained passerine birds succeed in urban environments. Biol. Lett. 2011;7:730–732. doi: 10.1098/rsbl.2011.0341. PubMed DOI PMC

Sayol F, Sol D, Pigot AL. Brain size and life history interact to predict urban tolerance in birds. Front. Ecol. Evol. 2020;8:58. doi: 10.3389/fevo.2020.00058. DOI

Blumstein DT. Flight-initiation distance in birds is dependent on intruder starting distance. J. Wildl. Manag. 2003;67:852–857. doi: 10.2307/3802692. DOI

Weston MA, McLeod EM, Blumstein DT, Guay P-J. A review of flight-initiation distances and their application to managing disturbance to Australian birds. Emu. 2012;112:269–286. doi: 10.1071/MU12026. DOI

Blumstein DT. Flush early and avoid the rush: a general rule of antipredator behavior? Behav. Ecol. 2010;21:440–442. doi: 10.1093/beheco/arq030. DOI

Samia DSM, Nomura F, Blumstein DT. Do animals generally flush early and avoid the rush? a meta-analysis. Biol. Lett. 2013;9:20130016. doi: 10.1098/rsbl.2013.0016. PubMed DOI PMC

Mayer M, Natusch D, Frank S. Water body type and group size affect the flight initiation distance of European waterbirds. PLoS ONE. 2019;14:e0219845. doi: 10.1371/journal.pone.0219845. PubMed DOI PMC

Samia DSM, Blumstein DT, Stankowich T, Cooper WE. Fifty years of chasing lizards: new insights advance optimal escape theory. Biol. Rev. 2016;91:349–366. doi: 10.1111/brv.12173. PubMed DOI

Kozłowski J, Konarzewski M, Czarnoleski M. Coevolution of body size and metabolic rate in vertebrates: a life-history perspective. Biol. Rev. 2020;95:1393–1417. doi: 10.1111/brv.12615. PubMed DOI PMC

Ricklefs RE, Wikelski M. The physiology/life-history nexus. Trends Ecol. Evol. 2002;17:462–468. doi: 10.1016/S0169-5347(02)02578-8. DOI

Guay PJ, Weston MA, Symonds MRE, Glover HK. Brains and bravery: little evidence of a relationship between brain size and flightiness in shorebirds. Austral Ecol. 2013;38:516–522. doi: 10.1111/j.1442-9993.2012.02441.x. DOI

Weston MA, et al. Differences in flight initiation distances between African and Australian birds. Anim. Behav. 2021;179:235–245. doi: 10.1016/j.anbehav.2021.07.008. DOI

Norberg, U. M. Vertebrate Flight: Mechanisms, Physiology, Morphology, Ecology and Evolution (Springer, 1990).

Sheard C, et al. Ecological drivers of global gradients in avian dispersal inferred from wing morphology. Nat. Commun. 2020;11:2463. doi: 10.1038/s41467-020-16313-6. PubMed DOI PMC

Mikula P, et al. Migratory and resident waders differ in risk taking on the wintering grounds. Behav. Process. 2018;157:309–314. doi: 10.1016/j.beproc.2018.07.020. PubMed DOI

Hau M. Timing of breeding in variable environments: tropical birds as model systems. Horm. Behav. 2001;40:281–290. doi: 10.1006/hbeh.2001.1673. PubMed DOI

Wyndham E. Length of birds’ breeding seasons. Am. Naturalist. 1986;128:155–164. doi: 10.1086/284551. DOI

Tablado Z, et al. Factors modulating the behavioral and physiological stress responses: do they modify the relationship between flight initiation distance and corticosterone reactivity? Horm. Behav. 2021;132:104979. doi: 10.1016/j.yhbeh.2021.104979. PubMed DOI

Romero LM. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol. 2002;128:1–24. doi: 10.1016/S0016-6480(02)00064-3. PubMed DOI

Silverin B. The stress response and autumn dispersal behaviour in willow tits. Anim. Behav. 1997;53:451–459. doi: 10.1006/anbe.1996.0295. DOI

Samia DSM, Møller AP, Blumstein DT. Brain size as a driver of avian escape strategy. Sci. Rep. 2015;5:11913. doi: 10.1038/srep11913. PubMed DOI PMC

Martin TE, Martin PR, Olson CR, Heidinger BJ, Fontaine JJ. Parental care and clutch sizes in North and South American birds. Science. 2000;287:1482–1485. doi: 10.1126/science.287.5457.1482. PubMed DOI

Runyan AM, Blumstein DT. Do individual differences influence flight initiation distance? J. Wildl. Manag. 2004;68:1124–1129. doi: 10.2193/0022-541X(2004)068[1124:DIDIFI]2.0.CO;2. DOI

Guay P-J, et al. Observer effects occur when estimating alert but not flight-initiation distances. Wildl. Res. 2013;40:289. doi: 10.1071/WR13013. DOI

Wilman H, et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology. 2014;95:2027–2027. doi: 10.1890/13-1917.1. DOI

del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & Kirwan, G. Handbook of the Birds of the World Alive (Lynx Edicions, 2020).

Birdlife International. Data Zone. http://datazone.birdlife.org/home (2020).

Global Forest Watch. Global Forest Change. https://data.globalforestwatch.org/ (2020).

Venter, O. et al. Sixteen years of change in the global terrestrial human footprint and implications for biodiversity conservation. Nat. Commun.7, 12558 (2016). PubMed PMC

Venter O, et al. Last of the Wild Project, Version 3 (LWP-3): 2009 Human Footprint, 2018 Release. Palisades,: NASA Socioeconomic Data and Applications Center (SEDAC); 2018.

Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO. The global diversity of birds in space and time. Nature. 2012;491:444–448. doi: 10.1038/nature11631. PubMed DOI

Schliep K. P. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27:592–593. doi: 10.1093/bioinformatics/btq706. PubMed DOI PMC

Gabry, J. & Češnovar, R. cmdstanr: R Interface to “CmdStan”. https://mc-stan.org/cmdstanr, https://discourse.mc-stan.org (2021).

R Development Core Team. A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).

Vehtari A, Gelman A, Simpson D, Carpenter B, Bürkner PC. Rank-normalization, folding, and localization: an improved R̂ for assessing convergence of MCMC (with discussion) Bayesian Anal. 2021;16:667–718. doi: 10.1214/20-BA1221. DOI

Jones, N. S. & Moriarty, J. Evolutionary inference for function-valued traits: Gaussian process regression on phylogenies. J. R. Soc. Interface10, 20120616 (2013). PubMed PMC

Schielzeth H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 2010;1:103–113. doi: 10.1111/j.2041-210X.2010.00012.x. DOI

Gelman A. Scaling regression inputs by dividing by two standard deviations. Stat. Med. 2008;27:2865–2873. doi: 10.1002/sim.3107. PubMed DOI

Gelman A, Rubin DB. Inference from iterative simulation using multiple sequences. Stat. Sci. 1992;7:457–472. doi: 10.1214/ss/1177011136. DOI

Leveraging social media and other online data to study animal behavior

Urban birds' tolerance towards humans was largely unaffected by COVID-19 shutdown-induced variation in human presence