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Actualidades Biológicas

Print version ISSN 0304-3584

Actu Biol vol.43 no.115 Medellín July/Dec. 2021  Epub Jan 25, 2022

https://doi.org/10.17533/udea.acbi/v43n115a01 

Nota corta

Consumption of Melopsittacus undulatus (Shaw, 1805) (Psittaciformes, Psittacidae) by Sapajus cay Illiger, 1815 (Primates, Cebidae) in Midwest region of Brazil

Consumo de Melopsittacus undulatus (Shaw, 1805) (Psittaciformes, Psittacidae) por Sapajus cay Illiger, 1815 (Primates, Cebidae) en la región del Centro-Oeste de Brasil

Rodney Murillo Peixoto Couto1  * 

Vanderley Pereira dos Santos2 

Fernanda Dias Silva3  4  5 

¹ Faculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Dourados, Brazil.

² Universidade Estadual de Mato Grosso do Sul, Dourados, Brazil.

³ Programa de Pós-Graduação em Ciências Biológicas (Biodiversidade Neotropical), Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brasil.

4 Laboratório de Biossistemática de Anfíbios, Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brasil.

5 Departamento de Vertebrados, Setor de Herpetologia, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil.


Abstract

The interaction between native and exotic species can cause changes both in the food-chain and in aspects of competition for trophic resources, such as predation. Predatory events are common in nature, but difficult and usually recorded opportunistically. Here we present the first report of trophic interaction involving a species of exotic bird (Melopsittacus undulatus) and a species of native primate (Sapajus cay). Capuchin monkeys have already been recorded feeding on a wide variety of vertebrates, including frogs, lizards, birds, mammals, and even other species of primates. Although the record of the non-native M. undulatus in the state of Mato Grosso do Sul indicates a possible domestic escape, the record of predation may represent a beneficial trophic interaction for the ecosystem, preventing M. undulatus from becoming an invasive alien species. Studies are needed to assess what risks are posed by domestic species being preyed upon by native species.

Keywords: Bird; primates; trophic interactions; interspecific interactions

Resumen

La interacción entre especies nativas y exóticas puede provocar cambios en la cadena trófica tanto en aspectos de competencia por recursos alimenticios, como en depredación. Los eventos depredadores son de naturaleza común, pero difíciles y oportunistas de registrar. Aquí presentamos el primer informe de interacción trófica que involucra una especie de ave exótica (Melopsittacus undulatus) y una especie de primate nativo (Sapajus cay). Ya se ha registrado que los monos capuchinos se alimentan de una amplia variedad de vertebrados, incluidas ranas, lagartos, aves, mamíferos e incluso otras especies de monos. Aunque el registro de M. undulatus en el estado de Mato Grosso do Sul indica una posible fuga doméstica, el registro de depredación puede representar una interacción trófica beneficiosa para el ecosistema, evitando que M. undulatus se convierta en una especie exótica invasora. Se necesitan estudios para evaluar qué riesgos plantean las especies domésticas que son depredadas por especies nativas.

Palabras claves: aves; primates; interacción trófica; interacciones interespecíficas

Sapajus cay is a species of capuchin monkey which is distributed across South America, occurring in northern Argentina, south-eastern Bolivia, eastern Paraguay, and Brazil (Júnior et al., 2020). In Brazil, Azara’s capuchin is distributed from the southwest of the Amazon, south to the states of Mato Grosso and Mato Grosso do Sul and to the southeast of Goiás state (Júnior et al., 2020). This species has diurnal habits, and it is considered vulnerable to extinction in Brazil due to habitat loss and fragmentation of habitat (ICMBio and Ministério do Meio Ambiente, 2018). Azara’s capuchinmoves in groups, and the alpha male is usually responsible for locating food resources (Júnior et al., 2020). The species is considered omnivorous and opportunistic; feeding on fruits, invertebrates, seeds, parts of plants and vertebrates (Fragaszy et al., 2004; Júnior et al., 2020; Pinto, 2006).

Birds represent one of the groups of vertebrates with the greatest game importance worldwide (Bezerra et al., 2012), while parrots (Psittacidae) are among the birds that show the highest environmental plasticity, as they are normally able to establish at least one reproductive population outside their range of natural distribution (Menchetti and Mori 2014). Psittaciforms are known to potentially affect the economy and human well-being (e.g., damage to croplands, electrical infrastructure, noise pollution and transmission of pathogens), as well as population dynamics of native species (e.g., transmission of pathogens, direct competition and indirect in nesting, and changes in the food chain) (Menchetti and Mori, 2014; Vitousek, 1990). The budgerigar, Melopsittacus undulatus (Shaw, 1805) (Psittaciformes, Psittacidae), is a parrot of Australian origin (Wydham, 1980), whose introduction as a captive species is known along several countries worldwide, such as South Africa, Brazil, United States of America, Japan, New Zealand, Puerto Rico, and Switzerland (Binks, 2006; Juniper, 1998). In Brazil, this species was introduced in captivity in 1850, and since 1998 it has been recognized as a domestic bird (IBAMA, 1998). Melopsittacus undulatus is a very popular small pet parrot (18-20 cm long), which exhibits diurnal activity. In the wild, this species exhibits gregarious behaviour, in addition to being considered a potential explorer of ground food resources (e.g., seeds) and water resources, being able to compete with native species (Wydham, 1980).

The establishment of populations of exotic species can causes several impacts to the ecosystems being the second main factor promoting the loss of biodiversity (Menchetti and Mori, 2014; Paz et al., 2013). The replacement of native species and the generation of hybrids (Crooks, 1998; Huxel, 1999) in principle, is one of the major concerns of the existence of an exotic species. The interaction between native and exotic species can also cause a reduction in the diversity of species existing in the environment (Lodge, 1993), alteration of habitat (Castilla et al., 2004; Crooks, 1998), parasitism and changes in the food chain (e.g., competition and predation) (Vitousek, 1990). Although predatory events are common in nature, the records of these events are generally casual, and can provide essential data on the trophic interaction of the species involved (Fadel et al., 2019). Here we present the first report of trophic interaction between a species of exotic parrot, M. undulatus and a species of native primate, S. cay.

The event was observed during a daytime field activity in the reserve of the Centro Educacional e Social Marista (22°13’58.95”S and 54°46’00.89”W) in the municipality of Dourados, state of Mato Grosso do Sul, Brazil (Figure 1). The reserve has an area of ​​approximately 1.2 ha of Atlantic Forest with formation of the Submontana Semideciduous Seasonal Forest type (Bosa and Aderlan, 2011). The Centro Educacional e Social Marista is located within the urban area. There are residences around the reserve and some countryside areas with some trees. The primate population resides in the reserve, but eventually moves around the reserve. People visit the reserve frequently, with environmental education work on the reserve's grounds. The observation was carried out from distance the 10 m to do not interfere the predatory behavior, while also being recorded through a digital camera.

Figure 1 Forest reserve of Centro Educacional e Social Marista, Dourados, state of Mato Grosso do Sul, mid-west region of Brazil. Image: google earth for Alex Sandro Vergino Lima. 

On February 16th, 2020 at 11:00 am, we observed an individual adult female Azara's capuchin monkey feeding on an adult individual of budgerigar on a branch of a tree within the reserve (22°13’58.95”S and 54°46’00.89”W) (Figure 2). Away from the group, the adult female was seen pulling out the feathers of the budgerigar M. undulatus. We approached the animal to observe its predatory behaviour and the monkey appeared unperturbed. The Azara's capuchin monkey continued to pluck out the budgerigar feathers, and then began to tear its prey apart, feeding on the meat and offal. The observation lasted 10 minutes, after which which the monkey began to move back into the woods, carrying the prey and alternatively gripping M. undulatus in the hand or mouth while moving through the bush. We do not know whether Azara’s capuchin captured budgerigar or had found the budgerigar dead already. The image of this event was deposited in the UFMS Collection at ZUFMS (ZUFMS-MNV00150). Capuchin monkeys of the Sapajus genus are known to have a generalist diet (Costa et al., 2020). Behavioural and ecological flexibility allows species of capuchin monkeys to exploit a wide range of food items (Júnior et al., 2020), and at the same time they manage to select their prey according to size and age (e.g.,Rose et al., 2003; Sampaio and Ferrari, 2005). Opportunistic predation is also common, and they can feed on injured or dead animals regardless of their size and age (e.g.,Carretero-Pinzón et al., 2008). According to research by Resende et al (2003) predation of vertebrates by monkeys generally occurs when there is a scarcity of food or as the result of intraspecific social learning. Capuchin monkeys have been recorded feeding on a wide variety of vertebrates including frogs (Izawa, 1978), lizards (Canale et al., 2013), birds (Canale and Bernardo, 2016; Rose et al., 2003), small mammals (Milano et al., 2009; Palmeira and Pianca 2012; Resende et al., 2003; Rose et al., 2003) and even other species of monkeys (Albuquerque et al., 2014; Costa et al., 2020; Sampaio and Ferrari, 2005). The predation of vertebrates by capuchin monkeys is attributed to males when there is a shortage of food and/or because of intraspecific social learning (Júnior et al., 2020; Resende et al., 2003). The same occurs with the species Azara’s capuchin, where the diet of the females consists basically of fruits and invertebrates, while dominant males consume fruits, invertebrates, and vertebrates as food items (Júnior et al., 2020).

Figure 2 Sapajus cay predating Melopsittacus undulatus in the forest reserve of Centro Educacional e Social Marista, Dourados, state of Mato Grosso do Sul, mid-west region of Brazil. Photography: Vanderley Pereira dos Santos. 

Despite not appearing on the list of invasive alien species in Brazil, M. undulatus has populations established in Curitiba, Paraíba and São Paulo, and in these states, it is considered as a species of invasive exotic bird (Fontoura et al., 2013; Paz et al., 2013). So far, there are no records of the population establishment of budgerigar (M. undulatus) in the state of Mato Grosso do Sul, which may mean an isolated case of domestic escape. It is recognized that invasive alien species have a competitive potential due to their great capacity of proliferation and invasion of ecosystems, as they are favoured by the absence of natural conspecifics or predators (Ziller et al., 2004). Considering that we have not found any record in the literature that proves the establishment of a population of budgerigar for the state of Mato Grosso do Sul, and consequently for the area where the predation event occurred, it is necessary that ecological studies be carried out in the study area to identify if our observation was an isolated case or if there really is a population of parakeets established in the reserve. In addition, future studies that aim to evaluate the wealth offered by domestic animals and invaders when being preyed upon by native species can help to understand if there is and what is the impact of this trophic interaction.

ACKNOWLEDGEMENTS

Silva, F.D. thanks current scholarship supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) and Matthijs Strietman for the translation.

REFERENCES

Albuquerque, N.M., Silvestre, S.M., Cardoso, T.S., Ruiz-Esparza, J.M., Rocha, P.A., Beltrão-Mendes, R., & Ferrari, S.F. (2014). Capture of a common marmoset (Callithrix jacchus) by a capuchin monkey (Sapajus sp.) in the Ibura National Forest, Sergipe (Brazil). Neotropical Primates, 21(2), 218-220. https://doi.org/10.1896/044.021.0216Links ]

Bezerra, D.M.M., Araujo, H.F.P., & Alves, R.R.N. (2012). Captura de aves silvestres no semiárido brasileiro: técnicas cinegéticas e implicações para conservação. Tropical Conservation Science, 5(1), 50-66. https://doi.org/10.1177/194008291200500106Links ]

Binks, G.S. (2006). The Challenge: Breeding Championship Budgerigars. Osprey International. [ Links ]

Bosa, C.R., & Aderlan, J. (2011). Abordagem histórica de uma mata destinada a conservação ambiental no município de Dourados - MS. Monografias Ambientais, 2(2), 228-240. https://doi.org/10.5902/223613082683Links ]

Canale, G.R., & Bernardo, C.S.S. (2016). Predator-prey interaction between two threatened species in a Brazilian hotspot. Biota Neotropica, 16(1), 1-4. https://doi.org/10.1590/1676-0611-bn-2015-0059Links ]

Canale, G.R., Freitas, M.A., & Andrade, L.L. (2013). Predation of lizards by a critically endangered primate (Sapajus xanthosternos) in a tropical biodiversity hotspot in Brazil. Herpetology Notes, 6, 323-326. [ Links ]

Carretero-Pinzón, X., Defler, T.R., & Ferrari, S.F. (2008). Observation of black-capped capuchins (Cebus apella) feeding on an owl monkey (Aotus brumbacki) in the Colombian Llanos. Neotropical Primates , 15(2), 62-63. https://doi.org/10.1896/044.015.0210Links ]

Castilla, J.C., Lagos, N.A., & Cerda, M. (2004). Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Marine Ecology Progress Series, 268, 119-130. http://www.jstor.org/stable/24867611Links ]

Costa, T.M. da, Silva, D.J.da, Carniello, M.A., Muniz, C.C., Gusmão, A.C., Silva, O.D.da, Alves, V.D.S., & Filho, M.dos S. (2020). Predação oportunística de Mico melanurus (Primates, Callitrichidae) por Sapajus cay (Primates, Cebidae) em ecótono entre Pantanal e Amazônia. Oecologia Australis, 24(01), 179-184. https://doi.org/10.4257/oeco.2020.2401.15Links ]

Crooks, J.A. (1998). Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Marine Ecology Progress Series , 162, 137-152. https://doi.org/10.3354/meps162137Links ]

Fadel, R.M., Thaler, R., Folly, H., Galvão, C., Hoffmann, M., Alves, L., Santana, D.J., & Mângia, S. (2019). Predation of anurans across multiple life stages in an Amazon - Cerrado transitional zone. Herpetology Notes , 12, 895-899. https://www.biotaxa.org/hn/article/view/46027/50726Links ]

Fontoura, P.M., Dyer, E., Blackburn, T.M., & Orsi, M.L. (2013). Non-native bird species in Brazil. Neotropical Biology and Conservation, 8(3), 165-175. https://doi.org/10.4013/nbc.2013.83.07Links ]

Fragaszy, D.M., Visalberghi, E., & Fedigan, L.M. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge University Press. [ Links ]

Huxel, G.R. (1999). Rapid displacement of native species by invasive species: Effects of hybridization. Biological Conservation, 89, 143-152. https://doi.org/10.1016/S0006-3207(98)00153-0Links ]

Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA). (1998). Portaria Ibama 93/1998 - Importação e Exportação de Fauna Silvestre Nativa ou Exótica; Lista de Fauna Doméstica para fins de Operacionalização do IBAMA. http://www.sema.df.gov.br/wp-conteudo/uploads/2017/09/Portaria-IBAMA-n%C2%BA-93-de-1998.pdfLinks ]

ICMBio, & Ministério do Meio Ambiente. (2018). Livro Vermelho de Fauna Brasileira Ameaçada de Extinção. (Vol. 2). Instituto Chico Mendes de Conservação da Biodiversidade. https://www.icmbio.gov.br/portal/images/stories/comunicacao/publicacoes/publicacoes-diversas/livro_vermelho_2018_vol2.pdfLinks ]

Izawa, K. (1978). Frog-eating behavior of wild black-capped capuchin (Cebus apella). Primates, 19(4), 633-642. https://doi.org/10.1007/BF02373631Links ]

Júnior, O.F., Porfirio, G.E.de O., Santos, F.M., Gimenes Nantes, W.A., Oliveira de Assis, W., Braziliano de Andrade, G., Herrera, H.M., & Rímoli, J. (2020). Behavioral activities and diet of Azaras’s capuchin monkey, Sapajus cay (Illiger, 1815), in a forest remnant of the Brazilian Cerrado. Studies on Neotropical Fauna and Environment, 55(2), 149-154. https://doi.org/10.1080/01650521.2019.1708228Links ]

Juniper, T., & Parr, M. (1998). Parrots - A Guide to Parrots of the World. Yale University Press. [ Links ]

Lodge, D.M. 1993. Biological Invasions: Lessons for Ecology. Tree Reviews, 8(4), 133-137. https://doi.org/10.1016/0031-9384(74)90281-9Links ]

Menchetti, M., & Mori, E. (2014). Worldwide impact of alien parrots (Aves Psittaciformes) on native biodiversity and environment: A review. Ethology Ecology and Evolution, 26(2-3), 172-194. https://doi.org/10.1080/03949370.2014.905981Links ]

Milano, M.Z., & Monteiro-Filho, E.L.A. (2009) Predation on small mammals by capuchin monkeys, Cebus cay. Neotropical Primates , 16(2), 78-80. https://doi.org/10.1896/044.016.0210Links ]

Palmeira, F.B.L., & Pianca, C.C. (2012). Predation attempt on a roadkilled brown-eared woolly opossum (Caluromys lanatus) by a black-horned capuchin (Sapajus nigritus). Neotropical Primates , 19(1), 36-38. https://doi.org/10.1896/044.019.0107Links ]

Paz, M.C.P., Medeiros, C.R., Silva, T.C.F., Freitas, G.L., & Paz, R.J. (2013). Contribuição a lista da fauna exótica invasora do estado da Paraíba, Brasil. Anais Do Congressoo Brasileiro de Gestão Ambiental e Sustentabilidade, 1, 231-236. http://eventos.ecogestaobrasil.net/congestas2013/trabalhos/pdf/congestas2013-et-05-001.pdfLinks ]

Pinto, M.C.M. (2006). Padrão comportamental de um grupo de macacos-prego (Cebus apella cay Illiger, 1815) no Parque Estadual Matas do Segredo, Campo Grande (MS). [Unpublished master dissertation]. Universidade Federal do Mato Grosso do Sul. [ Links ]

Resende, Briseida D, Greco, V.L.G., Ottoni, E.B., & Izar, P. (2003). Some observations on the predation of small mammals by tufted capuchin monkeys (Cebus apella). Neotropical Primates , 11(2), 103-104. http://static1.1.sqspcdn.com/static/f/1200343/18198314/1337026356940/NP11.2.cebus.predation.pdf?token=%2BaKRDCRsgs1wi8%2FCqp%2FopdYFIBg%3DLinks ]

Rose, L.M., Perry, S., Panger, M.A., Jack, K., Manson, J.H., Gros-Louis, J., Mackinnon, K. C., & Vogel, E. (2003). Interspecific interactions between Cebus capucinus and other species: Data from three Costa Rican sites. International Journal of Primatology, 24(4), 759-796. https://doi.org/10.1023/A:1024624721363Links ]

Sampaio, D.T., & Ferrari, S.F. (2005). Predation of an infant titi monkey (Callicebus moloch) by a tufted capuchin (Cebus apella). Folia Primatologica, 76(2), 113-115. https://doi.org/10.1159/000083617Links ]

Vitousek, P.M. (1990). Biological invasions and ecosystem processes: Towards an integration of population biology and ecosystem studies. Oikos, 57(1), 7-13. https://doi.org/10.2307/3565731Links ]

Wydham, E. (1980). Diurnal cycle, behaviour and social organization of the Budgerigar. Emu-Austral Ornithology, 80(1), 25-33. https://doi.org/10.1071/MU9800025Links ]

Ziller, S.R., Zenni, R.D., & Neto, J.G. (2004). Invasões biológicas: Introdução, Impactos e espécies exóticas invasoras no Brasil. In: J. H., Pedrosa-Macedo, Princípios e Rudimentos do Controle Biológico de Plantas: Coletanea. Curitiba: Laboratório Neotropical de Controle Biológico de plantas. [ Links ]

Received: December 01, 2020; Accepted: May 01, 2021

* Corresponding author: couto.murillo@gmail.com

CONFLICTS OF INTEREST

The authors express that there is no conflict of interest.

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