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First record of death-feigning in Black Vultures (Coragyps atratus) (Cathartidae)

First record of death-feigning in Black Vultures (Coragyps atratus) (Cathartidae) Revista Brasileira de Ornitologia 27(4): 242–244. SHORT-COMMUNIC ARA TICLE TION December 2019 First record of death-feigning in Black Vultures (Coragyps atratus) (Cathartidae) 1,2,3 1,2 Marjory Auad Spina & Luís Fábio Silveira Programa de Pós-Graduação em Conservação da Fauna, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos – UFSCar, São Carlos, SP, Brazil. Seção de Aves, Museu de Zoologia da Universidade de São Paulo – MZUSP, São Paulo, SP, Brazil. Corresponding author: marjoryspina@gmail.com Received on 23 June 2019. Accepted on 18 November 2019. ABSTRACT: Death-feigning is a behavior ability with the purpose of allowing prey to evade from predators. Despite death-feigning is recorded on a wide variety of bird species, it has been recorded only once in vultures, more specifically on a Turkey Vulture (Cathartes aura) nest. In addition to this record, we report this behavior while manipulating an individual of Black Vulture (Coragyps atratus) in Brazil. This behavior is not usual in Cathartidae since adult vultures do not have a known natural predator. KEY-WORDS: anti-predator behavior, Brazil, physical contact, thanatosis. Although Black Vultures (Coragyps atratus) are considered reported thanatosis in predators, for example, Vogel-Jr. gregarious and group-forming species that can reach (1950) recorded thanatosis in a wild adult Turkey Vulture hundreds of individuals that feed, soar and roost together, (Cathartes aura) in Indiana, USA, when the vulture they do not breed in colonies. They are not territorialists was nesting in a Sycamore Tree, with two white downy and fly large areas in sear ch of food and shelter, considered chicks. Due to the human presence looking at the nest, rapid colonists, mainly in newly-opened anthropic-formed the adult remained completely motionless, remaining in a areas. Since individuals fly widely, t hey are considered as prone position with its wings opened and its head down. partially migratory birds, keeping longer periods of time Although it had been prodded with a stick and lifted in areas where a higher amount of resources is available off the ground, one could only notice eye movements (Mundy 1985, Souto 2008, Ribeiro et al. 2010). On the (Vogel-Jr. 1950). On another occasion, Martin-Jurado et other hand, they have a strong agonistic behavior when al. (2011) reported thanatosis in an adult individual of it comes to a resource dispute, due to food competition. Red Kite (Milvus milvus) after anesthesia for a surgical Among age-groups there are different behavioral features, procedure aiming for sex determination. This behavior such as juveniles being more submissive to the elders, as was confirmed t hrough the bispectral index, which reported by Kruuk (1967), Houston (1975) and Ribeiro evaluates the electrical activity of the brain of the bird. et al. (2010). After finishing the surgery, followe d by extubation, the Aggregation in American Black Vultures brings Red Kite remained immobile and unresponsive, despite about advantages, such as increased social interactions. the bispectral index corresponded to a full awake bird. Individuals may also benefit by being close to one another, In this report, we characterized thanatosis in one mainly through thermoregulation mechanisms by using Black Vulture individual, recorded in 2018 during the communal perches in trees, rocks or urban infrastructure removal from a handling-net (Fig. 1). (Campbell 2015, Ballejo 2016). The individual was captured at the Fundação Parque Thanatosis (or death-feigning) frequently occurs in Zoológico de São Paulo. The survey comprised biological response to the presence of predators, generating a state of sample collections such as feces, regurgitates as well as immobility by the prey (Miyatake et al. 2004, Humphreys any ectoparasite encountered during the procedure. This & Ruxton 2018). Although thanatosis has been described individual was captured, quickly pulled out of the trap in many groups, such as mammals, birds, fish, reptiles, with a handling net and immediately released afterward. amphibians, arachnids and insects (Miyatake et al. 2004, However, when released, the Black Vulture remained Humphreys & Ruxton 2018), it is more frequently found lying in the dorsal position. We could even lift the in prey than predators, like vultures. Few studies have individual off the ground by holding it only by its legs. Revista Brasileira de Ornitologia 27(4): 2019 Death-feigning in American Black Vultures Spina & Silveira Figure 1. Picture description showing thanatosis in a Black Vulture captured at the Fundação Parque Zoológico de São Paulo. (1) Individual lying down in dorsal decubitus; (2) touched without showing any response; (3) pushed out of the handling net without showing any response; (4) sideway-fallen Black Vulture seconds before rising. After realizing that either it was expressing thanatosis or helping with the capture of the Black Vultures and to an having a health issue, we placed the individual back on anonymous reviewer that contributed to improve the the handling net, in which it remained for a few seconds manuscript. and it stood and flew away. Thanatosis is an anti-predatory strategy frequently adopted by prey after physical contact by predator REFERENCES (Humphreys & Ruxton 2018). However, such behavior is Ballejo F. 2016. Ecología trófica y tafonomía del Jote de Cabeza uncertain in this particular situation described here. Even Negra, Coragyps atratus (Cathartidae) y su comparación con otros though vultures are vulnerable to predation by terrestrial Cathartidae en el noroeste de la Patagonia. Ph.D. Thesis. La P lata: carnivores when they are fledglings and juveniles, few Facultad de Ciencias Naturales y Museo, Universidad Nacional reports of adults being predated are known (Houston de La Plata. 1994, T eixeira et al. 2019). In spite of being quite common Campbell M.O. 2015. Systematic list of New World vultures, p. 71– 112. In: Campbell M.O. (ed.). Vultures: their evolution, ecology in several taxa, the adaptive significance of thanatosis is and conservation. Boca Raton: CRC Press. still uncertain. Lack of studies may be attributed to the Honma A., Oku S. & Nishida T. 2006. Adaptive significance of death fact that the usual consequence of thanatosis may be feigning posture as a specialized inducible defence against gape- predation, being less likely to be seen or tested in the field limited predators. Proceedings of the Royal Society of London B: and laboratory due to ethical reasons. Besides that, the Biological Sciences 273: 1631–1636. Houston D. 1975. Ecological isolation of African scavenging birds. success or failure of death feigning depends largely on Ardea 63: 55–64. the foraging techniques adopted by the predator. More Houston D.C. 1994. Family Cathartidae (New World vultures), p. studies are needed with regards to the predator-prey 24–41. In: del Hoyo J., Elliot A. & Sargatal J. (eds.). Handbook dynamics of vultures, in order to fully understand the of the birds of the world, v. 2 (New World vultures to guineafowl). predator-avoidance tactics involved within this species Barcelona: Lynx Editions. Humphreys R.K. & Ruxton G.D. 2018. A review of thanatosis (death (Honma et al. 2006, Humphreys & Ruxton 2018). feigning) as an anti-predator behaviour. Behavioral Ecology and Sociobiology 72: 22. Kruuk H. 1967. Competition for food between vultures in east Africa. ACKNOWLEDGEMENTS Ardea 55: 171–193. Martin-Jurado O., Simova-Curd S., Bettschart-Wolfensberger R. & Hatt J.-M. 2011. Bispectral index reveals death-feigning behavior We thank Fundação Parque Zoológico de São Paulo for the in a Red Kite (Milvus milvus). Journal of Avian Medicine and grant and support, Universidade Federal de São Carlos, Surgery 25: 132–135. Animal Ethics Committee (CEUA-UFSCar) and Instituto Miyatake T., Katayama K., Takeda Y., Nakashima A., Sugita A. & Chico Mendes de Conservação da Biodiversidade (ICMBio) Mizumoto M. 2004. Is death-feigning adaptative? Heritable for the licenses. We also thank Eli Carlos dos Santos for variation in fitness difference of death-feigning behaviour. Revista Brasileira de Ornitologia 27(4): 2019 Death-feigning in American Black Vultures Spina & Silveira Proceedings of the Royal Society of London B: Biological Sciences 271: município de Uberlândia (MG). M.Sc. Dissertation. Uberlândia: 2293–2296. Universidade Federal de Uberlândia. Mundy P.J. 1985. The biology of vultures: a summary of the workshop Teixeira F.D., Mesquita E.P., Ferreira M.A. & Araújo F.C. 2019. Diet proceedings. ICBP Technical Publication 5: 457–482. of Ornate Hawk-Eagle (Spizaetus ornatus). Revista Brasileira de Ribeiro L.B., Lima D.G. & Melo S.B.F. 2010. Interação competitiva de Ornitologia 27: 31–39. Coragyps atratus (Bechstein, 1793) (Cathartiformes, Cathartidae) Vogel-Jr. H.H. 1950. Observations on social behavior in Turkey no uso de um recurso limitado. Revista de Etologia 9: 34–39. Vultures. Auk 67: 210–216. Souto H.N. 2008. Ecologia de interações entre Coragyps atratus (Bechstein, 1793) e Caracara plancus (Miller, JF, 1777) no Associate Editor: Lilian T. Manica. Revista Brasileira de Ornitologia 27(4): 2019 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

First record of death-feigning in Black Vultures (Coragyps atratus) (Cathartidae)

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Abstract

Revista Brasileira de Ornitologia 27(4): 242–244. SHORT-COMMUNIC ARA TICLE TION December 2019 First record of death-feigning in Black Vultures (Coragyps atratus) (Cathartidae) 1,2,3 1,2 Marjory Auad Spina & Luís Fábio Silveira Programa de Pós-Graduação em Conservação da Fauna, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos – UFSCar, São Carlos, SP, Brazil. Seção de Aves, Museu de Zoologia da Universidade de São Paulo – MZUSP, São Paulo, SP, Brazil. Corresponding author: marjoryspina@gmail.com Received on 23 June 2019. Accepted on 18 November 2019. ABSTRACT: Death-feigning is a behavior ability with the purpose of allowing prey to evade from predators. Despite death-feigning is recorded on a wide variety of bird species, it has been recorded only once in vultures, more specifically on a Turkey Vulture (Cathartes aura) nest. In addition to this record, we report this behavior while manipulating an individual of Black Vulture (Coragyps atratus) in Brazil. This behavior is not usual in Cathartidae since adult vultures do not have a known natural predator. KEY-WORDS: anti-predator behavior, Brazil, physical contact, thanatosis. Although Black Vultures (Coragyps atratus) are considered reported thanatosis in predators, for example, Vogel-Jr. gregarious and group-forming species that can reach (1950) recorded thanatosis in a wild adult Turkey Vulture hundreds of individuals that feed, soar and roost together, (Cathartes aura) in Indiana, USA, when the vulture they do not breed in colonies. They are not territorialists was nesting in a Sycamore Tree, with two white downy and fly large areas in sear ch of food and shelter, considered chicks. Due to the human presence looking at the nest, rapid colonists, mainly in newly-opened anthropic-formed the adult remained completely motionless, remaining in a areas. Since individuals fly widely, t hey are considered as prone position with its wings opened and its head down. partially migratory birds, keeping longer periods of time Although it had been prodded with a stick and lifted in areas where a higher amount of resources is available off the ground, one could only notice eye movements (Mundy 1985, Souto 2008, Ribeiro et al. 2010). On the (Vogel-Jr. 1950). On another occasion, Martin-Jurado et other hand, they have a strong agonistic behavior when al. (2011) reported thanatosis in an adult individual of it comes to a resource dispute, due to food competition. Red Kite (Milvus milvus) after anesthesia for a surgical Among age-groups there are different behavioral features, procedure aiming for sex determination. This behavior such as juveniles being more submissive to the elders, as was confirmed t hrough the bispectral index, which reported by Kruuk (1967), Houston (1975) and Ribeiro evaluates the electrical activity of the brain of the bird. et al. (2010). After finishing the surgery, followe d by extubation, the Aggregation in American Black Vultures brings Red Kite remained immobile and unresponsive, despite about advantages, such as increased social interactions. the bispectral index corresponded to a full awake bird. Individuals may also benefit by being close to one another, In this report, we characterized thanatosis in one mainly through thermoregulation mechanisms by using Black Vulture individual, recorded in 2018 during the communal perches in trees, rocks or urban infrastructure removal from a handling-net (Fig. 1). (Campbell 2015, Ballejo 2016). The individual was captured at the Fundação Parque Thanatosis (or death-feigning) frequently occurs in Zoológico de São Paulo. The survey comprised biological response to the presence of predators, generating a state of sample collections such as feces, regurgitates as well as immobility by the prey (Miyatake et al. 2004, Humphreys any ectoparasite encountered during the procedure. This & Ruxton 2018). Although thanatosis has been described individual was captured, quickly pulled out of the trap in many groups, such as mammals, birds, fish, reptiles, with a handling net and immediately released afterward. amphibians, arachnids and insects (Miyatake et al. 2004, However, when released, the Black Vulture remained Humphreys & Ruxton 2018), it is more frequently found lying in the dorsal position. We could even lift the in prey than predators, like vultures. Few studies have individual off the ground by holding it only by its legs. Revista Brasileira de Ornitologia 27(4): 2019 Death-feigning in American Black Vultures Spina & Silveira Figure 1. Picture description showing thanatosis in a Black Vulture captured at the Fundação Parque Zoológico de São Paulo. (1) Individual lying down in dorsal decubitus; (2) touched without showing any response; (3) pushed out of the handling net without showing any response; (4) sideway-fallen Black Vulture seconds before rising. After realizing that either it was expressing thanatosis or helping with the capture of the Black Vultures and to an having a health issue, we placed the individual back on anonymous reviewer that contributed to improve the the handling net, in which it remained for a few seconds manuscript. and it stood and flew away. Thanatosis is an anti-predatory strategy frequently adopted by prey after physical contact by predator REFERENCES (Humphreys & Ruxton 2018). However, such behavior is Ballejo F. 2016. Ecología trófica y tafonomía del Jote de Cabeza uncertain in this particular situation described here. Even Negra, Coragyps atratus (Cathartidae) y su comparación con otros though vultures are vulnerable to predation by terrestrial Cathartidae en el noroeste de la Patagonia. Ph.D. Thesis. La P lata: carnivores when they are fledglings and juveniles, few Facultad de Ciencias Naturales y Museo, Universidad Nacional reports of adults being predated are known (Houston de La Plata. 1994, T eixeira et al. 2019). In spite of being quite common Campbell M.O. 2015. Systematic list of New World vultures, p. 71– 112. In: Campbell M.O. (ed.). Vultures: their evolution, ecology in several taxa, the adaptive significance of thanatosis is and conservation. Boca Raton: CRC Press. still uncertain. Lack of studies may be attributed to the Honma A., Oku S. & Nishida T. 2006. Adaptive significance of death fact that the usual consequence of thanatosis may be feigning posture as a specialized inducible defence against gape- predation, being less likely to be seen or tested in the field limited predators. Proceedings of the Royal Society of London B: and laboratory due to ethical reasons. Besides that, the Biological Sciences 273: 1631–1636. Houston D. 1975. Ecological isolation of African scavenging birds. success or failure of death feigning depends largely on Ardea 63: 55–64. the foraging techniques adopted by the predator. More Houston D.C. 1994. Family Cathartidae (New World vultures), p. studies are needed with regards to the predator-prey 24–41. In: del Hoyo J., Elliot A. & Sargatal J. (eds.). Handbook dynamics of vultures, in order to fully understand the of the birds of the world, v. 2 (New World vultures to guineafowl). predator-avoidance tactics involved within this species Barcelona: Lynx Editions. Humphreys R.K. & Ruxton G.D. 2018. A review of thanatosis (death (Honma et al. 2006, Humphreys & Ruxton 2018). feigning) as an anti-predator behaviour. Behavioral Ecology and Sociobiology 72: 22. Kruuk H. 1967. Competition for food between vultures in east Africa. ACKNOWLEDGEMENTS Ardea 55: 171–193. Martin-Jurado O., Simova-Curd S., Bettschart-Wolfensberger R. & Hatt J.-M. 2011. Bispectral index reveals death-feigning behavior We thank Fundação Parque Zoológico de São Paulo for the in a Red Kite (Milvus milvus). Journal of Avian Medicine and grant and support, Universidade Federal de São Carlos, Surgery 25: 132–135. Animal Ethics Committee (CEUA-UFSCar) and Instituto Miyatake T., Katayama K., Takeda Y., Nakashima A., Sugita A. & Chico Mendes de Conservação da Biodiversidade (ICMBio) Mizumoto M. 2004. Is death-feigning adaptative? Heritable for the licenses. We also thank Eli Carlos dos Santos for variation in fitness difference of death-feigning behaviour. Revista Brasileira de Ornitologia 27(4): 2019 Death-feigning in American Black Vultures Spina & Silveira Proceedings of the Royal Society of London B: Biological Sciences 271: município de Uberlândia (MG). M.Sc. Dissertation. Uberlândia: 2293–2296. Universidade Federal de Uberlândia. Mundy P.J. 1985. The biology of vultures: a summary of the workshop Teixeira F.D., Mesquita E.P., Ferreira M.A. & Araújo F.C. 2019. Diet proceedings. ICBP Technical Publication 5: 457–482. of Ornate Hawk-Eagle (Spizaetus ornatus). Revista Brasileira de Ribeiro L.B., Lima D.G. & Melo S.B.F. 2010. Interação competitiva de Ornitologia 27: 31–39. Coragyps atratus (Bechstein, 1793) (Cathartiformes, Cathartidae) Vogel-Jr. H.H. 1950. Observations on social behavior in Turkey no uso de um recurso limitado. Revista de Etologia 9: 34–39. Vultures. Auk 67: 210–216. Souto H.N. 2008. Ecologia de interações entre Coragyps atratus (Bechstein, 1793) e Caracara plancus (Miller, JF, 1777) no Associate Editor: Lilian T. Manica. Revista Brasileira de Ornitologia 27(4): 2019

Journal

Ornithology ResearchSpringer Journals

Published: Dec 1, 2019

Keywords: anti-predator behavior; Brazil; physical contact; thanatosis

References