Therya_notes_114

THERYA NOTES 2023, Vol. 4 : 101-104 DOI: 10.12933/therya_notes-23-114 ISSN 2954-3614

Predation on neotropical lizards Tropidurus sp. by tamarin primate Leontocebus weddelli in Brazil

Depredación sobre la lagartija neotropical Tropidurus sp. por el primate tamarino Leontocebus weddelli en Brasil

Janayne Cristina Gomes Fernandes1, Matheus de Araújo Paz2,3, Raul Afonso Pommer-Barbosa3,4, and Marcela Alvares Oliveira3,5*

1Departamento de Ciências Biológicas, Campus José Ribeiro Filho, Universidade Federal de Rondônia. BR 364, s/n km 9.5, Porto Velho. Rondônia, Brasil. E-mail: janaynecristinagomes@gmail.com (JCGF).

2Laboratório de Biologia e Diversidade de Insetos (LaBDIn), Departamento de Ciências Biológicas, Campus José Ribeiro Filho, Universidade Federal de Rondônia. BR 364, s/n km 9.5, Porto Velho. Rondônia, Brasil. E-mail: matheuspza0001@gmail.com (MAP).

3Projeto Sagui-de-Rondônia, Associação de Defesa Etnoambiental Kanindé, Porto Velho. Rondônia, Brasil.

4Clube de Astronomia e Ciências de Rondônia, Campus José Ribeiro Filho, Universidade Federal de Rondônia, BR 364, s/n km 9.5, Porto Velho. Rondônia, Brasil. E-mail: raulpommer@hotmail.com (RAP-B).

5Programa de Pós-Graduação em Conservação e Uso de Recursos Naturais, Departamento de Ciências Biológicas, Campus José Ribeiro Filho, Universidade Federal de Rondônia. BR 364, s/n km 9.5, Porto Velho. Rondônia, Brasil. E-mail: marcela.mugrabe@gmail.com (MAO).

*Corresponding author

The diet of tamarin primates is predominantly frugivorous and insectivorous; it may include other elements in its diet such as nectar, seeds and arthropods, while vertebrate consumption is occasional. We present an unpublished record of the consumption of neotropical lizards (Tropidurus sp.) by the tamarin pichico (Leontocebus weddelli) in Porto Velho, Rondônia, Brazil. The record was conducted in 2022 at the José Ribeiro Filho campus of the Federal University of Rondônia, which is located in the peri-urban area, 9.5 km from the city of Porto Velho. The ad libitum method was used, continuously recording all important behavioral aspects of the primate. An adult individual of undetermined sex of Leontocebus weddelli was observed on the ground, completely consuming an adult individual of Tropidurus sp. for approximately 6 minutes. Representatives of the genus Leontocebus consume fruits and insects, and lizards are not the main items in their diet but represent an important energy source. This note reinforces the adaptive potential of this genus, in addition to the seasonal exploration of prey in highly disturbed environments.

Key words: Amazon; diet; forest edge; Rondônia; vertebrates.

La dieta de los primates tamarinos es predominantemente frugívora e insectívora, puede incluir otros elementos en su dieta como néctar, semillas y artrópodos, mientras que el consumo de vertebrados es ocasional. Se presenta un registro inédito de consumo de lagartijas neotropicales (Tropidurus sp.) por parte del tamarino pichico (Leontocebus weddelli) en Porto Velho, Rondônia, Brasil. El registro se realizó en el año 2022 en el campus José Ribeiro Filho de la Universidad Federal de Rondônia, la cual está situada en la zona periurbana, a 9.5 km de la ciudad de Porto Velho. Se utilizó el método ad libitum, registrando continuamente todos los aspectos conductuales importantes del primate. Se observó en el suelo a un individuo adulto de sexo indeterminado de Leontocebus weddelli, que durante aproximadamente 6 minutos consumió por completo a un individuo adulto de Tropidurus sp. Los representantes del género Leontocebus consumen frutas e insectos, y las lagartijas no son los principales ítems en su dieta, pero representan una importante fuente de energía. Esta nota refuerza el potencial adaptativo de este género, además de la exploración estacional de presas en entornos muy alterados.

Palabras claves: Amazonia; borde del bosque; dieta; Rondônia; vertebrados.

Tamarin primates, which include the genera Leontocebus and Saguinus, have a frugivorous and insectivorous diet, including other items such as nectar, seeds, arthropods, and occasionally vertebrates (Egler 1992; Lopes and Ferrari 1994; Oliveira and Ferrari 2008; García-Castillo and Defler 2018). Records of lizard consumption by tamarin primates include the consumption of Anolis fuscoauratus and Gonatodes humeralis by Leontocebus illigeri in Perú (Soini 1987). Heymann et al. (2000) recorded the consumption of 6 species of lizards Anolis spp., Kentropyx pelviceps, Mabuya nigropunctata, Norops fuscoauratus, N. nitens and 1 unidentified species by Saguinus mystax and Leontocebus fuscicollis in Perú. For Brazil, there is only 1 documented ancient record by Peres (1992) documented the consumption of Anolis sp. by Leontocebus fuscicollis and S. mystax in the state of Amazonas.

Among the different species from the genus Leontocebus, we highlight L. weddelli. This is a small primate, weighing on average 400 gr in Brazil, considered an insectivore, frugivore, and gumivore (Ferrari and Martins 1992; Paglia et al. 2012). Its distribution includes Bolivia, Perú and Brazil (including the states of Acre, Amazonas and Rondônia); it is categorized as Least Concern by the International Union for Conservation of Nature and Natural Resources (Ravetta et al. 2021). Until 2022, there are no records in the literature of the consumption of lizards by L. weddelli.

Given this scenario, this report aims to present the predation of lizard Tropidurus sp. by Weddell's saddle-back tamarin (Leontocebus weddelli) in a peri-urban area of the city of Porto Velho, Rondônia, Brazil.

The record was made at the José Ribeiro Filho campus of the Universidade Federal de Rondônia, Brazil (8° 50' 11.96" S, 63° 56' 24.89" W; WGS84), located 9.5 km (direction Rio Branco - Acre, in the southwestern portion) from the city of Porto Velho, in its peri-urban area (Figure 1). The campus has approximately 1 km2, of which 20 % have different buildings. The predominant vegetation type of the area is Lowland Open Ombrophylous Forest (Veloso et al. 1991), and there are large areas composed of secondary vegetation and illegal logging, as well as unfinished buildings and open areas.

A study carried out in 2008 showed that the primate fauna of the campus is of 6 species: Plecturocebus brunneus, Pithecia mittermeieri, Saimiri ustus, Sapajus apella, Mico rondoni and Leontocebus weddelli, the latter two being the 2 most abundant species (Alencar 2008). There have yet to be published scientific papers on the lizard fauna in the area. The identification of the genus of the lizard was based on its external characteristics, such as the size and shape of its body and head, and its cryptic color (Frost et al. 2001).

The ad libitum method proposed by Altmann (1974) was adopted to record the primate's behavior, recording all behaviors observed and deemed relevant by the observer, plus rare and significant records, such as the event documented here.

The observation was made on September 13, 2022 at 13:37 hr, during the dry season. The recording site was close to a bus stop. An adult individual of L. weddelli of undetermined sex was observed inspecting a tree trunk 50 cm high. An adult Tropidurus sp. of about 25 centimeters was observed in this trunk, which used cracks and holes in the trunk to hide from the primate. After 6 capture attempts, at 13:51 hr, L. weddelli managed to capture the lizard with his hands. The primate remained on the ground seated on the hind limbs and started to eat the head, followed by the rest of the body (Figure 2a, 2b). The process lasted approximately 6 min. After the total consumption of lizard, the individual from L. weddelli returned to the forest. The consumption starting from the head is already reported in L. weddelli and other species of callitrichids such as Saguinus mystax, to immobilize the prey, reducing the risk of the predator being attacked and reducing the possibility of prey escape (Steklis and King 1978; Clarke 1987; Heymann et al. 2000).

Among the items of animal origin, insects are the most exploited by representatives of the genus Leontocebus (Soini 1987; Garber 1993; Heymann et al. 2000) and lizards are not the main items in the diet of these primates, but they represent an important energy source (Peres 1992). The consumption of lizards and other vertebrates by species of the genus Leontocebus and Saguinus is occasional. For example, Porter (2001) found that vertebrate consumption accounts for < 1 % of the diet of L. weddelli, with vertebrate predation being on time. Garbino et al. (2022) also agree that the consumption of vertebrates by primates has a seasonal aspect, occurring mainly in the dry season, where some fruits are unavailable.

On the other hand, Heymann et al. (2000) highlighted the ability of these primates to exploit open micro-habitats, capturing exposed prey. The genera Tropidurus include diurnal species, of terrestrial habits and that can be observed in open areas, rocks, vertical walls and anthropized environments favorable for its development having an association of the species with artificial structures (Meira et al. 2007). The predation observation environment presents components that both favor the development of lizards and primates. Tropidurus spp. present higher densities in urbanized areas compared to rural ones, and the artificial structures associated with secondary and edge vegetation of the campus favor their development (Ribeiro-Júnior and Amaral 2016). At the same time, representatives of the genus Leontocebus are excellent explorers of forest edge and secondary vegetation environments (Sussman and Kinzey 1984) and show high densities in anthropized or regenerating environments (Ferronato et al. 2018; Silva et al. 2021). The scenario was favorable for the encounter between these 2 species, but it had not been previously documented due to the absence of studies on the primate diet. Studies are currently being carried out with primates of the genus Leontocebus in large forest blocks. The present record was only possible because both species explored an open environment, favoring total visualization of the predation event. These data reinforce the adaptive potentiality of genus Leontocebus, besides the seasonal exploration of prey in highly altered environments.

Acknowledgements

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) for PNPD research fellow to MAO (88887.717863/2022-00). To the 3 anonymous reviewers for improving the manuscript.

Literature cited

Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour 49:227-266.

Alencar, T. B. 2008. Inventário e estimativas populacionais da mastofauna diurna não-voadora em fragmento de floresta ombrófila aberta de terras baixas do campus da fundação Universidade Federal de Rondônia, Porto Velho - RO. Graduation’s monograph in Biological Sciences. Universidade Federal de Rondônia, UNIR. Porto Velho, Brazil.

Clarke, A. S. 1987. Animal food in the diet of prosimian and new world primates. Pp. 133–165 in Comparative primate biology: behavior, cognition, and motivation (Mitchell, G., and J. Erwin, eds.). Wiley Press. New York, U.S.A.

Egler, S. G. 1992. Feeding ecology of Saguinus bicolor bicolor (Callitrichidae: Primates) in a relict forest in Manaus, Brazilian Amazonia. Folia Primatologica 59:61-76.

Ferrari, S. F., and E. S. Martins. 1992. Gummivory and gut morphology in two sympatric callitrichids (Callithrix emiliae and Saguinus fuscicollis weddelli) from Western Brazilian Amazonia. American Journal of Physical Anthropology 88:97-103.

Ferronato, M. L., et al. 2018. Manejo florestal sustentável e a mastofauna amazônica: o caso da fazenda Manoa, Rondônia, Brasil. Revista Brasileira de Ciências da Amazônia 7:9-18.

Frost, D. R., et al. 2001. Phylogenetics of the lizard genus Tropidurus (Squamata: Tropiduridae: Tropidurinae): direct optimization, descriptive efficiency, and sensitivity analysis of congruence between molecular data and morphology. Molecular Phylogenetics and Evolution 21:352-371.

Garber, A. 1993. Seasonal patterns of diet and ranging in two species of tamarin monkeys: stability versus variability. International Journal of Primatology 14:145-166.

Garbino, G. S. T., et al. 2022. Seasonal variation in frog predation by black lion tamarins (Leontopithecus chrysopygus, Primates). Journal of Natural History 56:449-461.

García-Castillo, F., and T. R. Defler. 2018. The diet of Saguinus oedipus in a dry tropical forest and the importance of Spondias mombin Gum as a “fallback food”. Primate Conservation 32:67-79.

Heymann, E. W., C. Knogge, and E. R. Tirado Herreira. 2000. Vertebrate predation by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis. American Journal of Primatology 51:153-158.

Lopes, M. A., and S. F. Ferrari. 1994. Foraging behavior of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae). International Journal of Primatology 15:373-387.

Meira, K. T. R., et al. 2007. História natural de Tropidurus oreadicus em uma área de cerrado rupestre do Brasil Central. Biota Neotropica 7:155-163.

Oliveira, A. C. M., and S. F. Ferrari. 2008. Habitat exploitation by free-ranging Saguinus niger in eastern Amazonia. International Journal of Primatology 29:1499-1510.

Paglia, A. P., et al. 2012. Annotated checklist of Brazilian mammals. Occasional Pappers in Conservation Biology 6:1-76.

Peres, C. A. 1992. Prey-capture benefits in a mixed-species group of Amazonian tamarins, Saguinus fuscicollis and S. mystax. Behavioral Ecology and Sociobiology 31:339-347.

Porter, L. M. 2001. Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. International Journal of Primatology 22:961-992.

Ravetta, A. L., et al. 2021. Leontocebus weddelli. In: IUCN 2020. The IUCN Red List of Threatened Species. Version 2022.2. www.iucnredlist.org. Accessed on March 6, 2023.

Ribeiro-Júnior, M., and S. Amaral. 2016. Diversity, distribution, and conservation of lizards (Reptilia: Squamata) in the Brazilian Amazonia. Neotropical Biodiversity 2:195-421.

Silva, F. G., et al. 2021. Medium and large-sized mammals in a remnant forest in the state of Rondônia, Brazil. Mammalogy Notes 7:259.

Soini, P. 1987. Ecology of the Saddle-Back Tamarin Saguinus fuscicollis illigeri on the Río Pacaya, Northeastern Peru. Folia Primatologica 49:11-32.

Steklis, H. D., and G. E. King. 1978. The cranio-cervical killing bite: toward an ethology of primate predatory behavior. Journal of Human Evolution 7:567-581.

Sussman, R. W., and W. G. Kinzey. 1984. The ecological role of the Callitrichidae: a review. American Journal of Physical Anthropology 64:419-449.

Veloso, H. P., A. L. R. Rangel-Filho, and J. C. Lima. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal. IBGE. Rio de Janeiro, Brazil.

Associated editor: Itandehui Hernández Aguilar.

Submitted: December 7, 2022; Reviewed: April 17, 2023.

Accepted: July 14, 2023; Published on line: August 4, 2023.