Activity budget of a group of black-horned capuchin monkeys (Sapajus nigritus) in an urban environment

Authors

DOI:

https://doi.org/10.5433/1679-0367.2023v44n2p223

Keywords:

Anthropization, Behavioral flexibility, Primate, Urban capuchin monkeys

Abstract

Urban growth and human impacts on the environment have forced animals to adjust to habitat fragmentation and reduced home ranges. Capuchin monkeys are known for their great social and behavioral flexibility, occupying even highly urbanized environments in a way that the time budget of this primate in synanthropic situation may be affected by the area they inhabit. This study aims to analyze the activity budget of a group of Sapajus nigritus living in an anthropized area, 1) comparing the behavioral frequencies in urbanized areas and forest fragments; 2) comparing behavioral frequencies in different sex-age classes. During the study, the number of individuals ranged from 35 to 40 individuals identified based on sex-age classes. Behavioral data were collected using the instantaneous scan sampling method, for two minutes with eight-minute intervals. We obtained 319 scans over 28 days, distributed between November 2021 and June 2022, with eight hours per day. We compared the behaviors different areas and between sex-age classes using the Kruskal-Wallis’s test. Overall, the group performed a higher frequency of traveling (21.22%), followed by foraging (18.07%), feeding (16.57%) and vigilance (15.61%). The frequency of behaviors varied between areas, with vigilance, social, resting, interaction with humans and self-activity more frequent in urbanized areas compared to forest fragments. We also found variation between the sex-age classes, primarily with juveniles foraging more and adults performing more vigilance. The differences in the behaviors performed by the group express the behavioral flexibility of S. nigritus, adapting its activity pattern according to the area occupied.

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Author Biographies

Julia dos Santos Gutierres, Universidade Estadual de Londrina - UEL

PhD student in Biological Sciences at the Universidade Estadual de Londrina (UEL), Londrina, Paraná.

 

Laura Beatriz Cristóvão Radi, Universidade Estadual de Londrina - UEL

Biological Sciences undergraduate at the Universidade Estadual de Londrina (UEL), Londrina, Paraná

Thiago Deruza Garcia, Universidade Estadual de Londrina - UEL

PhD student in Biological Sciences at the Universidade Estadual de Londrina (UEL), Londrina, Paraná.

Felipe dos Santos Machado Pereira , Universidade Estadual de Londrina - UEL

PhD student in Biological Sciences at the State University of Londrina (UEL), Londrina, Paraná.

Guilherme Akira Awane, Universidade Estadual de Londrina - UEL

Biological Sciences undergraduates at the Universidade Estadual de Londrina (UEL), Londrina, Paraná...

Ana Paula Vidotto-Magnoni, Universidade Estadual de Londrina - UEL

PhD in Biological Sciences (Zoology) from the Universidade Estadual Paulista “Júlio de Mesquita Filho” (Unesp), Botucatu, São Paulo, Brazil. Adjunct Professor at the Universidade Estadual de Londrina (UEL), Londrina, Paraná.

References

Altmann J. Observational study of behavior: sampling methods. Behaviour. 1974;49(3):227-67. doi: 10.1163/156853974x00534. DOI: https://doi.org/10.1163/156853974X00534

Back JP, Suzin A, Aguiar LM. Activity budget and social behavior of urban capuchin monkeys (Sapajus sp.) (Primates, Cebidae). Zoologia. 2019;36:1-10. doi: 10.3897/zoologia.36.e30845. DOI: https://doi.org/10.3897/zoologia.36.e30845

Bateson P, Martin P. Measuring behavior: an introductory guide. New York: Cambridge University Press; 2021. DOI: https://doi.org/10.1017/9781108776462

Batista WP, Costa Neto EM, Spagnoletti N. Relação entre humanos primatas (Sapajus sp.) às margens do Rio São Francisco, Nordeste, Brasil. Ethnoscientia. 2017;2(1). doi: 10.18542/ethnoscientia.v2i1.10180. DOI: https://doi.org/10.22276/ethnoscientia.v2i1.49

Castro CSS. Pesquisa com primatas em ambiente natural: técnicas para coleta de dados ecológicos e comportamentais. In: Anais da 62ª Reunião da Sociedade Brasileira para Progresso da Ciência [Internet]; 2010 Jul 26-30; Natal [citado 2023 maio 23]. p. 1-27. Disponível em: http://www.sbpcnet.org.br/livro/62ra/minicursos/MC%20Carla%20Soraia%20Soares%20de%20Castro.pdf

Di Bitetti M, Kowalewski M, Lynch Alfaro J, Rylands AB. Sapajus nigritus ssp. cucullatus. The IUCN Red List of Threatened Species [Internet]. 2020 [cited 2023 May 5]. Available from: https://dx.doi.org/10.2305/IUCN.UK.2020-3.RLTS.T160945956A160945959.en DOI: https://doi.org/10.2305/IUCN.UK.2020-3.RLTS.T160945956A160945959.en

Fahrig L. Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst. 2003;34(1):487-515. doi: 10.1146/annurev.ecolsys.34.011802.132419. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132419

Ferreira RG, Lee PC, Izar P. Food competition in a semi-free-ranging Cebus apella group. Folia Primatol (Basel). 2008;79(6):463-75. doi: 10.1159/000158525. DOI: https://doi.org/10.1159/000158525

Fortes VB, Bicca-Marques JC. Ecologia e comportamento de primatas: métodos de estudo de campo. Cad La Salle XI [Internet]. 2005 [citado 2023 maio 12];2(1):207-18. Disponível em: https://www.researchgate.net/publication/265208340_Ecologia_e_comportamento_de_primatas_Metodos_de_estudo_de_campo

Fragaszy DM, Visalberghi E, Fedigan LM. The complete capuchin, the biology of the Genus Cebus. Cambridge: Cambridge University Press; 2004.

Freese CH, Oppenheimer JR. The capuchin monkeys, genus Cebus. In: Coimbra-Filho AF, Mittermeier RA, editors. Ecology and behavior of neotropical primates. Rio de Janeiro: Academia Brasileira de Ciências; 1981. p. 331-89.

Galetti M, Dirzo R. Ecological and evolutionary consequences of living in a defaunated world. Biological Conservation. 2013;163:1-6. doi: 10.1016/j.biocon.2013.04.020. DOI: https://doi.org/10.1016/j.biocon.2013.04.020

Galleti M, Pedroni F. Seasonal diet of capuchin monkeys (Cebus apella) in a semideciduous forest in south-east Brazil. J Trop Ecol. 1994;10(1):27-39. doi: 10.1017/S0266467400007689. DOI: https://doi.org/10.1017/S0266467400007689

Hendges CD, Melo GL, Gonçalves AS, Cerezer FO, Cáceres NC. Landscape attributes as drivers of the geographical variation in density of Sapajus Nigritus Kerr, 1792, a primate endemic to the Atlantic Forest. Acta Oecol. 2017;84:57-63. doi: 10.1016/j.actao.2017.08.007. DOI: https://doi.org/10.1016/j.actao.2017.08.007

Instituto Agronômico do Paraná (IAPAR). Cartas do Paraná [Internet] 2019 [citado 2022 set 8]. Disponível em: http://www.Iapar.Br/Modules/Conteudo/Conteudo.Php?Conteudo=863

Izar P, Verderane MP, Peternelli-Dos-Santos L, Mendonça-Furtado O, Presotto A, Tokuda M, et al. Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. Am J Primatol. 2012;74(4):315-31. doi: 10.1002/ajp.20968. DOI: https://doi.org/10.1002/ajp.20968

Jaman MF, Huffman MA. The effect of urban and rural habitats and resource type on activity budgets of commensal rhesus macaques (Macaca mulatta) in Bangladesh. Primates. 2013;54(1):49-59. doi: 10.1007/s10329-012-0330-6. DOI: https://doi.org/10.1007/s10329-012-0330-6

Joly CA, Metzger JP, Tabarelli M. Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytol. 2014;204(3):459-73. doi: 10.1111/nph.12989. DOI: https://doi.org/10.1111/nph.12989

Lima RA, Oliveira AA, Pitta GR, Gasper AL, Vibrans AC, Chave J, et al. The erosion of biodiversity and biomass in the Atlantic Forest biodiversity hotspot. Nat Commun. 2020;11(1),6347. doi: 10.1038/s41467-020-20217-w. DOI: https://doi.org/10.1038/s41467-020-20217-w

Lorenzo MP. Comportamento e ecologia de uma população de macacos-prego (Sapajus nigritus goldfuss, 1809) em um fragmento florestal inserido em área urbana no Município de Londrina, Paraná, Brasil [dissertatação]. Londrina (PR): Universidade Estadual de Londrina; 2018.

Lousa TC, Grande TO, Mendes FDC. Time budget and foraging strategies of two provisioned groups of tufted capuchin monkeys, Sapajus libidinosus, in a small, seasonal urban forest fragment. Primates. 2022;63(4):387-95. doi: 10.1007/s10329-022-00993-3. DOI: https://doi.org/10.1007/s10329-022-00993-3

Lousa TC. Influências dos alimentos antrópicos no comportamento e ecologia de macacos-prego. [dissertação]. Brasília (DF): Universidade de Brasília; 2013.

Lynch Alfaro JW, Izar P, Ferreira RG. Capuchin monkey research priorities and urgent issues. Am J Primatol. 2014;76(8):705-20. doi: 10.1002/ajp.22269. DOI: https://doi.org/10.1002/ajp.22269

Mendonça-Furtado O, Edaes M, Palme R, Rodrigues A, Siqueira J, Izar P. Does hierarchy stability influence testosterone and cortisol levels of bearded capuchin monkeys (Sapajus libidinosus) adult males? A comparison between two wild groups. Behav Process. 2014;109:79-88. doi: 10.1016/j.beproc.2014.09.010. DOI: https://doi.org/10.1016/j.beproc.2014.09.010

Mikich SB, Liebsch D. Damage to forest plantations by tufted capuchins (Sapajus nigritus): Too many monkeys or not enough fruits? For Ecol Manag. 2014;314:9-16. doi: 10.1016/j.foreco.2013.11.026. DOI: https://doi.org/10.1016/j.foreco.2013.11.026

Mittermeier RA, Gil PR, Hoffmann M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, Mittermeier CG, et al. Hotspots revisited: earth's biologically richest and most endangered terrestrial ecoregions. México: Cemex; 2004.

Pereira AD, Antoniazzi MH, Magnoni APV, Orsi ML. Mamíferos silvestres predados por cães domésticos em fragmentos de Mata Atlântica no sul do Brasil. Biotemas. 2019;32(2):107-13. doi: 10.5007/2175-7925.2019v32n2p107. DOI: https://doi.org/10.5007/2175-7925.2019v32n2p107

R Core Team. R: a language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2022 [cited 2023 Oct 24]. Available from: https://www.R-project.org/

Rasec-Silva A, Bertassoni A, De Marco Júnior P. Capuchin monkey (Sapajus spp.) diet: current knowledge, gaps, and future directions. Primates. 2023;64(3):305-17. doi: 10.1007/s10329-023-01057-w. DOI: https://doi.org/10.1007/s10329-023-01057-w

Resende BD, Ottoni EB, Fragaszy DM. Ontogeny of manipulative behavior and nut-cracking in young tufted capuchin monkeys (Cebus apella): a Perception-action perspective. Dev Sci. 2008;11(6):828-40. doi: 10.1111/j.1467-7687.2008.00731.x. DOI: https://doi.org/10.1111/j.1467-7687.2008.00731.x

Rezende CL, Scarano FR, Assad ED, Joly CA, Metzger, JP, Strassburg BBN, et al. From hotspot to hopespot: An opportunity for the Brazilian Atlantic Forest. Perspec Ecol Conserv. 2018;16:208-14. doi:10.1016/j.pecon.2018.10.002. DOI: https://doi.org/10.1016/j.pecon.2018.10.002

Rímoli J, Strier KB, Ferrari SF. Seasonal and longitudinal variation in the behavior of free-ranging black tufted capuchins Cebus nigritus (Goldfuss, 1809) in a fragment of Atlantic Forest in Southeastern Brazil. In: Ferrari SF, Rímoli J, editors. A primatologia no Brasil. Aracaju: Sociedade Brasileira de Primatologia; 2008. p. 130-46.

Rocha VJ. Macaco-prego, como controlar esta nova praga florestal? Floresta. 2000;30(1-2):95-9. doi:10.5380/rf.v30i12.2329. DOI: https://doi.org/10.5380/rf.v30i12.2329

Sabbatini G, Stammati M, Tavares MC, Visalberghi E. Behavioral flexibility of a group of bearded capuchin monkeys (Cebus libidinosus) in the National Park of Brasília (Brazil): consequences of cohabitation with visitors. Braz J Biol. 2008;68(4):685-93. doi: 10.1590/s1519-69842008000400002. DOI: https://doi.org/10.1590/S1519-69842008000400002

Spagnoletti N, Cardoso TCM, Fragaszy, D, Izar P. Coexistence between humans and capuchins (Sapajus libidinosus): comparing observational data with farmers’ perceptions of crop losses. Int J Primatol. 2016;38(2):243-62. doi:10.1007/s10764-016-9926-9. DOI: https://doi.org/10.1007/s10764-016-9926-9

Suzin A, Back JP, Garey MV, Aguiar LM. The relationship between humans and capuchins (Sapajus sp.) in an urban green area in Brazil. Int J Primatol. 2017;38:1058-71. doi: 10.1007/s10764-017-9996-3. DOI: https://doi.org/10.1007/s10764-017-9996-3

Tárano Z, López MC. Behavioural repertoires and time budgets of semi-free-ranging and captive groups of wedge-capped capuchin monkeys, Cebus olivaceus, in zoo exhibits in Venezuela. Folia Primatol (Basel). 2015;86(3):203-22. doi: 10.1159/000381397. DOI: https://doi.org/10.1159/000381397

Vilanova R, Silva Junior JS, Grelle CEV, Marroig G, Cerqueira R. Limites climáticos e vegetacionais das distribuições de Cebus nigritus e Cebus robustus (Cebinae, Platyrrhini). Neotrop Primates. 2005;13(1):14-9. doi:10.1896/1413-4705.13.1.14. DOI: https://doi.org/10.1896/1413-4705.13.1.14

Wehncke1 EV, Domínguez. Seed dispersal ecology of non-restricted frugivores, capuchin monkeys in three neotropical forests. J Trop Ecol. 2007;23:519-28. doi:10.1017/S0266467407004257. DOI: https://doi.org/10.1017/S0266467407004257

Wickham H, Navarro D, Pedersen T. ggplot2: elegant graphics for data analysis (3e) [Internet]. 2nd ed. New York: Springer-Verlag; 2016 [cited 2021 Jul 25]. Available from: https://ggplot2-book.org/

Williamson EA, Feistner AT. Habituating primates: processes, techniques, variables and ethics. In: Setchell JM, Curtis DJ, editors. Field and laboratory methods in primatology: a practical guide. Cambridge: Cambridge University Press; 2003. p. 25-39. DOI: https://doi.org/10.1017/CBO9781139165105.004

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Published

2023-12-13

How to Cite

1.
Gutierres J dos S, Radi LBC, Deruza Garcia T, Pereira F dos SM, Akira Awane G, Vidotto-Magnoni AP. Activity budget of a group of black-horned capuchin monkeys (Sapajus nigritus) in an urban environment. Semin. Cienc. Biol. Saude [Internet]. 2023 Dec. 13 [cited 2024 Nov. 21];44(2):223-36. Available from: https://ojs.uel.br/revistas/uel/index.php/seminabio/article/view/48252

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