Abstract
Anti-predator behavior and personality have important consequences for the survival of captive-bred animals after reintroduction in the wild. The personality of an animal can be defined as low within-individual variation in behavior relative to between-individual variation in behavior. Mortality caused by predation is the main reason for reintroduction failure, and training captive-born animals to avoid predators can solve this problem. However, how anti-predator training affects the personality of animals is uncertain. The objective of this study was to test the behavioral responses of captive Amazon Parrots (Amazona aestiva, Psittacidae) submitted to an anti-predator conditioning protocol, and to evaluate if anti-predator training affects parrot personalities. Twenty-six parrots were trained against predators using taxidermized models; their personalities were evaluated by calculating boldness scores before and after anti-predator training sessions. Parrots increased the expression of anti-predator behaviors when tested with all models; control groups behaved in a more relaxed way. The anti-predator responses persisted for 60 days after the end of the training sessions. Boldness scores increased in 50% of cases after anti-predator training sessions, and in only 33% of cases did parrots become shyer after anti-predator training. The tendency of parrots to exhibit bold behaviors in the personality tests, even after the training sessions, may be explained by their early experiences, low behavioral plasticity or high cognitive ability. Training naive parrots was an effective tool to enhance behavioral responses against predators before reintroduction. The study of personality is of great importance in reintroduction and translocation programs to determine the position of each individual in the shy-bold continuum and to help select individuals more suited for reintroduction.
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References
Alcock J. 2013. Animal behavior, an evolutionary approach, 10th Edition. Ann Arbor: Sinauer Associates.
Alonso R., Orejas P., Lopes F. & Sanz C. 2011. Pre-release training of juvenile Little Owls Athene noctua to avoid predation. Animal Biodiversity and Conservation 34: 389–393.
Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour 49: 227–267.
Andrade AA. & Azevedo C.S. 2011. Efeitos do enriquecimento ambiental na diminuição de comportamentos anormais exibidos por Papagaios-verdadeiros (Amazona aestiva, Psittacidae) cativos. Revista Brasileira de Ornitologia 19: 56–62.
Azevedo C.S. & Young RJ. 2006. Behavioural responses of captiveborn Greater Rheas Rhea americana Linnaeus (Rheiformes, Rheidae) submitted to antipredator training. Revista Brasileira de Zoologia 23: 186–193
Azevedo CS., Young R.J. & Rodrigues M. 2012. Failure of captive-born Greater Rheas (Rhea americana, Rheidae, Aves) to discriminate between predator and nonpredator models. Acta Ethologica 15: 179–185.
Beck B.B., Kleiman D.G., Dietz J.M., Castro I., Carvalho C., Martins A. & Rettberg-Beck B. 1991. Losses and reproduction in reintroduced Golden Lion Tamarins Leontopithecus rosalia. Dodo 27:50–61.
Begon M., Townsend C.R. & Harper J.L. 2006. Ecology: from individuals to ecosystems, 4th Edition. Oxford: Blackwell Publishing.
Beissinger S.R. & Bucher E.H. 1992. Sustainable harvesting of parrots for conservation, p. 73–115. In: Beissinger S.R. & Snyder N.F.R (eds.). New World parrots in crisis, solutions from conservation biology. Washington: Smithsonian Institution Press.
Béjcek V. & Stastny K. 2002. Enciclopédia das Aves: as várias espécies e seus habitats. Lisboa: Livros Livros.
Bell A.M. & Stamps JA. 2004. Development of behavioural differences between individuals and populations of Sticklebacks, Gasterosteus aculeatus Animal Behaviour 68: 1339–1348.
Biro PA. & Stamps JA. 2008. Are animal personality traits linked to life-history productivity? Trends in Ecology and Evolution 23: 361–368
Bremner-Harrison S. Prodohl PA. & Elwood RW. 2004. Behavioural trait assessment as a release criterion: boldness predicts early death in a reintroduction programme of captive-bred Swift Fox (Vulpes velox). Animal Conservation 7: 313–320.
Cade T.J. 1988. Using science and technology to reestablish species lost in nature, p. 279–288. In: Wilson E.O. & Peter F.M. (eds.). Biodiversity. Washington: National Academic Press.
Carere C., Drent P.J., Privitera L., Koolhaas J.M. & Groothuis T.G.G. 2005. Personalities in Great Tits, Parus major: stability and consistency. Animal Behaviour 70: 795–805.
Carlstead K. 1999. Constructing behavioural profiles for zoo animals: incorporating behavioral information into captive population management. Oregon: AZA Behaviour and Husbandry Advisory Group and Oregon Zoo.
Carter A.J. & Feeney W.E. 2012. Taking a comparative approach: analysing personality as a multivariate behavioural response across species. PLoS ONE 7: e42440.
Collar N.J. 1997. Family Psittacidae (parrots), p. 280–479. In: del Hoyo J., Elliot A. & Sargatal J. (eds.). Handbook of the Birds of the World, v. 4 (sandgrouse to cuckoos). Barcelona: Lynx Editions.
Curio E. 1988. Cultural transmission of enemy recognition by birds, p. 75–97. In: Zental T.R. & Galef-Jr. B.G. (eds.). Social learning, psychological and biological perspectives. New Jersey: Hilldalf.
Curio E., Ernst U. & Vieth W 1978. The adaptive significance of avian mobbing: II. Cultural transmission of enemy recognition in Blackbirds: effectiveness and some constraints. Ethology 48: 184–202.
Dingemanse N.J. & Réale D. 2005. Natural selection and animal personality. Behaviour 142: 1159–1184.
Eilam D. 2005. Die hard: a blend of freezing and fleeing as a dynamic defense-implications for the control of defensive behavior. Neuroscience and Biobehavioral Reviews 29: 1181–1191.
Emery N.J. 2006. Cognitive ornithology: the evolution of avian intelligence. Philosophical Transactions of the Royal Society of London B: Biological Sciences 361: 23–43.
Feenders G., Klaus K. & Bateson M. 2011. Fear and exploration in European Starlings (Sturnus vulgaris): a comparison of hand-reared and wild-caught birds. PLoS ONE 6: el 9074.
Foose T.J. 1986. Riders of the lost ark: the role of captive breeding in conservation strategies, p. 141–165. In: Kaufman L. & Mallory D. (eds.). The last extinction. Cambridge: The Mit Press.
Fox R.A. & Millam J.R. 2004. The effect of early environment on neophobia in Orange-winged Amazon Parrots (Amazona amazonica). Applied Animal Behaviour Science 89: 117–129.
Fox R.A. & Millam J.R. 2007. Novelty and individual differences influence neophobia in Orange-winged Amazon Parrots (Amazona amazonica). Applied Animal Behaviour Science 104: 107–115.
Frid A. & Dill L.M. 2002. Human-caused disturbance stimuli as a form of predation risk. Ecology and Society 6:11.
Frost A.J., Winrow-Giffen A., Ashley P.J. & Sneddon L.U. 2007. Plasticity in animal personality traits: does prior experience alter the degree of boldness? Proceedings of the Royal Society of London B: Biological Sciences 274: 333–339.
Gilardi J.D. & Munn CA. 1998. Patterns of activity, flocking, and habitat use in parrots of the Peruvian Amazon. Condor 100: 641–653.
Griffin A.S., Blumstein D.T. & Evans CS. 2000. Training captive-bred or translocated animals to avoid predators. Conservation Biology 14: 1317–1326.
Griffin A.S., Evans C.S. & Blumstein D.T. 2001. Learning specificity in acquired predator recognition. Animal Behaviour 62: 577–589.
Groothuis T.G.G. & Carere C. 2005. Avian personalities: characterization and epigenesis. Neuroscience & Biobehavioral Reviews 29: 137–150.
Hemmi J.M. & Merkle T. 2009. High stimulus specificity characterizes anti-predator habituation under natural conditions. Proceedings of the Royal Society B: Biological Sciences 276: 4381–4388.
IUCN (International Union for the Conservation of Nature). 2015. The LUCN red list of threatened species, Version 2015.1. http://www.iucnredlist.org. (access on 12 May 2016).
Kurvers R.H.J.M., Prins H.H.T., van Wieren S.E., van Oers K, Nolet BA. & Ydenberg R.C. 2010. The effect of personality on social foraging: shy Barnacle Geese scrounge more. Proceedings of the Royal Society of London B: Biological Sciences 277: 601–608.
Lendvai A.Z., Bókony V. & Chastel O. 2011. Coping with novelty and stress in free-living House Sparrows. Journal of Experimental Biology 214: 821–828.
Levine S., Atha K. & Wiener S.G. 1993. Early experience effects on the development of fear in the Squirrel Monkey. Behavioral and Neural Biology 60: 225–233.
Macias C., Parás A., González J.J., Enkerlin E., Ritchie B., Stone E., Lamberski N. & Ciembor D. 2003. Release of confiscated Amazon parrots in Mexico. Psittascene 15: 2–4.
Maloney RF. & McLean I.G. 1995. Historical and experimental learned predator recognition in free-living New Zealand Robins. Animal Behaviour 50: 1193–1201.
Martin, P. & Bateson, P. 2007. Measuring behaviour: an introductory guide, 3rd Edition. Cambridge University Press: Cambridge.
McDougall PT., Réale D., Sol D. & Reader S.M. 2006. Wildlife conservation and animal temperament: causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Animal Conservation 9: 39–48.
McLean I.G. 1996. Teaching an endangered mammal to recognize predators. Biological Conservation 75: 51–62.
McLean I.G. & Rhodes G. 1991. Enemy recognition and response in birds, p. 173–211. In: Power D.M. (ed.). Current Ornithology v. 8, Santa Barbara: Plenum Press.
McLean I.G., Hölzer C. & Studholme B.J.S. 1999. Teaching predator- recognition to a naive bird: implications for management. Biological Conservation 87: 123–130.
Meehan C.L., Millam J.R. & Mench J.A. 2003. Foraging opportunity and increased physical complexity both prevent and reduce psychogenic feather picking by young Amazon Parrots. Applied Animal Behaviour Science 80: 71–85.
Miles W.T.S., Parsons M., Close A.J., Luxmoore R. & Furness RW 2013. Predator-avoidance behaviour in a nocturnal petrel exposed to a novel predator. Lbis 155: 16–31.
Miller B., Biggins D., Hanebury L. & Vargas A. 1994. Reintroduction of the Black-footed Ferret (Mustela nigripes), p. 455–464. In: Olney P.J.S., Mace G.M. & Feistner A.T.C. (eds.). Creative conservation, interactive management of wild and captive animals. London: Chapman and Hall.
MMA (Ministério do Meio Ambiente). 2014. Portaria No 444, de 17 de dezembro de 2014. Brasilia: Ministério do Meio Ambiente.
Pitter E. & Christiansen M.B. 1997. Behavior of individuals and social interactions of the Red-fronted Macaw Ara rubrogenys in the wild during the midday rest. Ornitologia Neotropical 8: 133–143.
Prestes N.P 2000. Descrição e análise quantitativa do etograma de Amazona pretrei em cativeiro. Ararajuba 8: 25–42.
Ribeiro L.B. & Silva M.G. 2007. O comércio ilegal põe em risco a diversidade das aves no Brasil. Ciência e Cultura 59: 4–5.
Richards J. 1998. Return of the natives. Australian Geographic 50: 82.
Rosier R.L. & Langkilde T. 2011. Behavior under risk: how animals avoid becoming dinner. Nature Education Knowledge 2: 8.
Ryer C.H. & Olla B.L. 1998. Shifting the balance between foraging and predator avoidance: the importance of food distribution for a schooling pelagic forager. Environmental Biology of Fishes 52: 467–475.
Sanz V. & Grajal A. 1998. Successful reintroduction of captive-raised Yellow-shouldered Amazon Parrots on Margarita Island, Venezuela. Conservation Biology 12: 430–441.
Schunk F., Somenzari M., Lugarini C. & Soares E.S. 2011. Plano de ação nacional para a conservação dos papagaios da Mata Atlântica. Brasília: Ministério do Meio Ambiente.
Seixas G.H.F. & Mourão G.M. 2002. Nesting success and hatching survival of the Blue-fronted Amazon (Amazona aestiva) in the Pantanal of Mato Grosso do Sul, Brazil. Journal of Field Ornithology 73: 399–409.
Short J., Bradshaw S.D., Giles J., Prince R.I.T. & Wilson G.R. 1992. Reintroduction of macropods (Marsupialia: Macropodoidea) in Australia - a review. Biological Conservation 62: 189–204.
Sih A., Bell A. & Johnson J.C 2004. Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology and Evolution 19:372–378.
Smith B.R. & Blumstein D.T. 2012. Structural consistency of behavioural syndromes: does predator training lead to multi-contextual behavioural changes? Behaviour 149: 187–213.
Smith B.R. & Blumstein D.T. 2013. Animal personality and conservation biology: the importance of behavioral diversity, p. 381–413. In: Carere C. & Maestripieri D. (eds.). Animal personalities: behavior, physiology, and evolution. Chicago: The University of Chicago Press.
Specht G.V.A. 2007. Treinamento antipredação em Corujinha-do-mato (Megascops [Otus] choliba, (Vieillot, 1817) - Strigiformes - Aves) para programa de translocação. MSc. Dissertation. Belo Horizonte: Pontifícia Universidade Católica de Minas Gerais.
Stamps J. & Groothuis T.G.G. 2010. The development of animal personality: relevance, concepts and perspectives. Biological Reviews 85: 301–325.
Stankowich T. & Blumstein D.T. 2005. Fear in animals: a metaanalysis and review of risk assessment. Proceedings of the Royal Society of London B: Biological Sciences 272: 2627–2634.
Taylor R.W, Boon A.K, Dantzer B., Réale D., Humphries M.M., Boutin S., Gorrell J.C., Coltman D.W & McAdam A.G. 2012. Low heritabilities, but genetic and maternal correlations between Red Squirrel behaviours. Journal of Evolutionary Biology 25: 614–624.
Toms C.N., Echevarria D.J. & Jouandot D.J. 2010. A methodological review of personality-related studies in fish: focus on the shy-bold axis of behavior. International Journal of Comparative Psychology 23: 1–25.
Valle A.L., Silva C.W., Teixeira R.A., Batista L.P. & Ramos B.C. 2010. Comparativo entre duas metodologias de soltura para Amazona aestiva observando-se poucos critérios de soft-release. Reintrodução de Psitacídeos 1: 48–50.
van Heezik Y., Seddon P.J. & Maloney RR 1999. Helping reintroduced Houbara Bustards avoid predation: effective anti-predator training and the predictive value of pre-release behaviour. Animal Conservation 2: 155–163.
van Oers K., Drent P.J., de Goed P. & van Noordwijk A.J. 2004. Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proceedings of the Royal Society of London B: Biological Sciences 271: 65–73.
van Oers K., de Jong G., van Noordwijk A.J., Kempenaers B. & Drent P.J. 2005. Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142: 1185–1206.
van Oers K.V. & Naguib M. 2013. Avian personality, p. 66–95. In: Carere C. & Maestripieri D. (eds.). Animal personalities: behavior, physiology, and evolution. Chicago: The University of Chicago Press.
Veloso-Júnior, RR, Sousa L.C. & Brito M.L.O. 2010. Soltura e monitoramento de Jandaia verdadeira na Ilha de São Luís. Reintrodução de Psitacídeos 1: 40–43.
Verbeek M.E.M., Drent P.J. & Wiepkema RR 1994. Consistent individual differences in early exploratory behaviour of male Great Tits. Animal Behaviour 48: 1113–1121.
Waiters J.V. & Powell D.M. 2012. Measuring animal personality for use in population management in zoos: suggested methods and rationale. Zoo Biology 31: 1–12.
White-Jr. T.H., Collazo JA. & Vilella RJ. 2005. Survival of captive-reared Puerto Rican Parrots released in the Caribbean National Forest. Condor 107: 424–432.
Wilson D.S. 1998. Adaptive individual differences within single populations. Philosophical Transactions of the Royal Society of London B: Biological Sciences 353: 199–205.
Wilson D.S., Clark A.B., Coleman K. & Dearstyne T 1994. Shyness and boldness in humans and other animals. Trends in Ecology and Evolution 9: 442–446.
Wolf M. & Weissing RJ. 2012. Animal personalities: consequences for ecology and evolution. Trends in Ecology and Evolution 27: 452–461.
Yorzinski J.L. & Platt M.L. 2012. The difference between night and day: anti-predator behavior in birds. Journal of Ethology 30: 211–218
Zaccaroni M., Ciuffreda M., Paganin M. & Beani L. 2007. Does an early aversive experience to humans modify anti-predator behaviour in adult Rock Partridges? Ethology, Ecology & Evolution 19: 193–200.
Zar J.H. 1998. Biostatistical analysis, 4th fidition. New Jersey: Prentice Hall.
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de Azevedo, C.S., Rodrigues, L.S.F. & Fontenelle, J.C.R. Important tools for Amazon Parrot reintroduction programs. Rev. Bras. Ornitol. 25, 1–11 (2017). https://doi.org/10.1007/BF03544370
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DOI: https://doi.org/10.1007/BF03544370