Levantamento populacional e identificação individual de macacos-prego (Sapajus nigritus cucullatus) do Parque Municipal Arthur Thomas, Londrina, Paraná, Brasil
DOI:
https://doi.org/10.62015/np.2025.v31.803Keywords:
Cebidae, habituation, home range, sex-age classes, urbanizationAbstract
Arthur Thomas Municipal Park (ATMP), located in Londrina, Paraná state, Brazil, is home to a population of black-horned capuchin monkeys (Sapajus nigritus cucullatus), for which the first ecological and behavioral studies were conducted about 25 years ago. However, basic information such as population size, number of groups, degree of habituation, and individual identification of the monkeys within the ATMP has remained unknown. The present study aimed to conduct a population survey of black-horned capuchin monkeys, including the identification of single or multiple groups, assessment of sex-age classes, and development of an individual identification catalog. The census was carried out using the direct observation method during each field encounter. Photographic equipment and image analysis were used for individual identification and catalog preparation. Geographic coordinates were collected for spatial analysis. A total of 58 individuals were identified, divided into two groups, designated as Group 1 (13 individuals) and Group 2 (45 individuals). This study provides fundamental information on the population structure, degree of habituation, and spatial dynamics of the capuchin monkeys inhabiting ATMP, using non-invasive methods for population assessment.
References
Adobe. 2020. Adobe Lightroom Classic. Versão [9.2.1]. Adobe. https://www.adobe.com/br/products/photoshop-lightroom-classic.html
Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour 49(3): 227–266. https://doi.org/10.1163/156853974x00534
Back, J., Suzin A. e Aguiar, L. M. 2019. Activity budget and social behavior of urban capuchin monkeys, Sapajus sp. (Primates: Cebidae). Zoologia 36: e30845. https://doi.org/10.3897/zoologia.36.e30845
Allan, A. T. L., Bailey, A. L. e Hill, R. A. 2020. Habituation is not neutral or equal: individual differences in tolerance suggest an overlooked personality trait. Sci. Adv. 6(28): eaaz0870. https://doi.org/10.1126/sciadv.aaz0870
Alonso, R. S., McClintock, B. T., Lyren, L. M., Boydston, E. E. e Crooks, K. R. 2015. Mark-Recapture and Mark-Resight methods for estimating abundance with remote cameras: a carnivore case study. PLOS ONE 10(3): e0123032. https://doi.org/10.1371/journal.pone.0123032
Arroyo-Rodríguez, V. e Fahrig, L. 2014. Why is a landscape perspective important in studies of primates? Am. J. Primatol. 76(10): 901–909. https://doi.org/10.1002/ajp.22282
Bateson, M. e Martin, P. 2021. Individuals and Groups. Em: Measuring Behaviour, M. Bateson, P. Martin (eds.) pp.223–227. Cambridge University Press, Cambridge.
Bolger, D. T., Morrison, T. A., Vance, B., Lee, D. e Farid, H. 2012. A computer-assisted system for photographic mark-recapture analysis. Methods in Ecol. Evol. 3(5): 813–822. https://doi.org/10.1111/j.2041-210X.2012.00212.x
Canale, G. R., Guidorizzi, C. E., Kierulff, M. C. M. e Gatto, C. A. F. 2009. First record of tool use by wild populations of the yellow-breasted capuchin monkey (Cebus xanthosternos) and new records for the bearded capuchin (Cebus libidinosus). Am. J. Primatol. 71(5): 366–372. https://doi.org/10.1002/ajp.20648
Castro, C. S. S. 2010. Pesquisa com primatas em ambiente natural: Técnicas para coleta de dados ecológicos e comportamentais. Em: 62ª Reunião Anual da Sociedade Brasileira de Pesquisa Científica, SBPC, Natal, Rio Grande do Norte.
Chapman, C. A. e Chapman, L. J. 2000. Determinants of group size in social primates: the importance of travel costs. In: Group Movement in Social Primates and Other Animals: Patterns, Processes, and Cognitive Implications, S. Boinski e P. Garber (eds.), pp.24–42. University of Chicago Press, Chicago.
Cipolleta, C. 2003. Ranging patterns of a western gorilla group during habituation to humans in the Dzanga-Ndoki National Park, Central African Republic. Int. J. Primatol. 24(6): 1207–1226. https://doi.org/10.1023/B:IJOP.0000005988.52177.45
Cotarelli, V. M., Vieira, A. O. S., Dias, M. C. e Dolibaina, P. C. 2008. Florística do Parque Arthur Thomas, Londrina, Paraná, Brasil. Acta Biol. Parana 37 (1, 2): 123–146. https://doi.org/10.5380/abpr.v37i0.13200
Crouse, D., Jacobs, R. L., Richardson, Z., Klum, S., Jain, A. e Baden, A. L. 2017. LemurFaceID: a face recognition system to facilitate individual identification of lemurs. BMC Zoology 2(2). https://doi.org/10.1186/s40850-016-0011-9
Cruickshank, S. C. e Schmidt, B. R. 2017. Error rates and variation between observers are reduced with the use of photographic matching software for capture-recapture studies. Amphib. Reptil. 38(3): 315–325. https://doi.org/10.1163/15685381-00003112
Deb, D., Wiper, S., Gong, S., Shi, Y., Tymoszek, C., Fletcher, A. e Jain, A. J. 2018. Face recognition: primates in the wild. IEEE Xplore. Em: 2018 IEEE 9th International Conference on Biometrics Theory, Applications and Systems. https://doi.org/10.1109/BTAS.2018.8698538
Diniz, M. F., Coelho, M. T. P., Sousa, F. G., Hasui, E. e Loyola, R. 2021. The underestimated role of small fragments for carnivore dispersal in the Atlantic Forest. Perspect. Ecol. Conserv. 19(1): 81–89. https://doi.org/10.1016/j.pecon.2020.12.001
Dheer, A., Samarasinghe, D., Dloniak, S. M. D. e Braczkowski, A. 2022. Using camera traps to study hyenas: challenges, opportunities, and outlook. Mamm. Biol. 102(3): 847–854. https://doi.org/10.1007/s42991-021-00188-1
Di Bitetti, M.S. 2001. Home-range use by the tufted capuchin monkey (Cebus apella nigritus) in a subtropical rainforest of Argentina. J. Zool. 253: 33–45. https://doi.org/10.1017/S0952836901000048
Di Bitetti, M., Kowalewski, M., Lynch Alfaro, J.W. e Rylands, A.B. 2020. Sapajus nigritus ssp. cucullatus. The IUCN Red List of Threatened Species 2020: e.T160945956A160945959. https://dx.doi.org/10.2305/IUCN.UK.2020-3.RLTS.T160945956A160945959.en
Estrada, A., Garber, P. A. e Chaudhary, A. 2020. Current and future trends in socio-economic, demographic and governance factors affecting global primate conservation. PeerJ. 8: e9816. https://doi.org/10.7717/peerj.9816
Falótico, T. 2022. Robust capuchin tool use cognition in the wild. Curr. Opin. Behav. Sci. 46: 101170. https://doi.org/10.1016/j.cobeha.2022.101170
Falótico, T. e Ottoni e E. B. 2016. The manifold use of pounding stone tools by wild capuchin monkeys of Serra da Capivara National Park, Brazil. Behaviour 153(4): 421–442. https://doi.org/10.1163/1568539X-00003357
Ferreira, R. G., Emidio, R. A. e Jerusalinsky, L. 2009. Three stones for three seeds: natural occurrence of selective tool use by capuchins (Cebus libidinosus) based on an analysis of the weight of stones found at nutting sites. Am. J. Primatol. 72(3): 270–275. https://doi.org/10.1163/1568539X-00003357
Fragaszy, D. M., Aiempichitkijkarn, N., Eshchar, Y., Mangalam, M., Izar, P., Resende, B. e Visalberghi, E. 2023. The development of expertise at cracking palm nuts by wild bearded capuchin monkeys, Sapajus libidinosus. Anim. Behav. 197: 1–14. https://doi.org/10.1016/j.anbehav.2022.12.008
Fragaszy, D. M., Visalberghi, E. e Fedigan, L. M. 2004. The Complete Capuchin. Cambridge: Cambridge University Press, Cambridge.
Garber, P.A., Gomes, D.F. e Bicca-Marques, J. C. (2012). Experimental field study of problem-solving using tools in free-ranging capuchins (Sapajus nigritus, formerly Cebus nigritus). Am. J. Primatol. 74: 344–358. https://doi.org/10.1002/ajp.20957
Global Forest Watch. 2025. Mapa Interativo. Instituto de Recursos Mundiais (WRI), Washington, DC. Disponível em: https://www.globalforestwatch.org/map/. Acessada em 17 de janeiro de 2025.
Gutierres, J. S., Radi, L. B. C., Garcia, T. D., Machado Pereira, F. S., Awane, G. A. e Vidotto-Magnoni, A. P. 2023. Activity budget of a group of black-horned capuchin monkeys (Sapajus nigritus) in an urban environment. Semin., Ciênc. Biol. Saúde (Online) 44(2): 223–236. https://doi.org/10.5433/1679-0367.2023v44n2p223
Gutierres, J. S., Machado Pereira, F. S., Lynch, J.W. e Vidotto Magnoni, A. P. 2025. Stone tool use by Black-Horned Capuchin Monkeys (Sapajus nigritus cucullatus) in an urban park in Londrina, Brazil. Am. J. Primatol. 87: 87–1 e23704. https://doi.org/10.1002/ajp.23704
Hendges, C. D., Melo, G. L., Gonçalves, A. S., Cerezer, F. O. e Cáceres, N. C. 2017. Landscape attributes as drivers of the geographical variation in density of Sapajus nigritus Kerr, 1792, a primate endemic to the Atlantic Forest. Acta Oecol. 84: 57–63. https://doi.org/10.1016/j.actao.2017.08.007
Ilham, K. 2024. Roadside provisioning threatens both humans and monkeys. Anim. Conserv. 27: 146–147. https://doi.org/10.1111/acv.12909
Izar, P. 1999. Aspectos de ecologia e comportamento de um grupo de macacos-prego (Cebus apella) em área de Mata Atlântica, São Paulo. Tese de Doutorado, Universidade de São Paulo, São Paulo, Brasil.
Izawa, K. 1980. Social behavior of the wild black-capped capuchin (Cebus apella). Primates 21(4): 443–467. https://doi.org/10.1007/BF02373834
Janson, C. H., Baldovino, M. C., e Bitetti, M. Di. 2012. The group life cycle and demography of Brown Capuchin Monkeys (Cebus [apella] nigritus) in Iguazú National Park. Em: Long-Term Field Studies of Primates, P. M. Kappeler e D. P. Watts (eds.), pp.185–214. Springer-Verlag. https://doi.org/10.1007/978-3-642-22514-7_9
Kappeler, P. M. e Watts, D. P. 2012. Long-term field studies of primates. Springer Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22514-7
Karczmarski, L., Stephen, C. Y. C., Scott, Y. S. C. e Cameron, E. Z. 2022. Individual identification and photographic techniques in mammalian ecological and behavioural research—Part 2: Field studies and applications. Mamm. Biol. 102(4):1047–54. https://doi.org/10.1007/s42991-023-00344-9
Knight, J. 2009. Making wildlife viewable: habituation and attraction. Society & Animals 17(2): 167–184. https://doi.org/10.1163/156853009X418091
Lima, G. C. B., Lacerda, J. C., Taynor, R., Araújo, M., Bezerra, B. M. e Souza-Alves, J. P. 2024. A new addition to the toolbox: stone tool use in blonde capuchin monkeys (Sapajus flavius). Primates 65: 383–389. https://doi.org/10.1007/s10329-024-01143-7
Lira, P. K., Tambosi, L. R., Ewers, R. M. e Metzger, J. P. 2012. Land-use and land-cover change in Atlantic Forest landscapes. For. Ecol. Manag. 278: 80–89. https://doi.org/10.1016/j.foreco.2012.05.008
Lovato D. L. F. L. 2024. Diversidade de mamíferos de médio e grande porte em fragmentos florestais urbanos e periurbano de Mata Atlântica. Dissertação de Mestrado, Universidade Estadual de Londrina, Londrina, Paraná, Brasil.
Lynch Alfaro, J. W., Izar, P. e Ferreira, R. G. 2014. Capuchin monkey research priorities and urgent issues. Am. J. Primatol. 8: 705–20. https://doi.org/10.1002/ajp.22269
Mainette, R. D., Lynch, J. W., Izar, P., Canale, G. e Martins W. 2025. Characterization of stone tool use in wild groups of critically endangered yellow-breasted capuchin monkeys (Sapajus xanthosternos). Am. J. Biol. Anthro. 186: e70002. https://doi.org/10.1002/ajpa.70002
McDougall, P. 2012. Is passive observation of habituated animals truly passive? J. Ethol. 30(2): 219–223. https://doi.org/10.1007/s10164-011-0313-x
Medeiros PS, Heming NM, Lynch JW, Martins WP. 2025. Range extension for the Critically Endangered yellow-breasted capuchin monkey (Sapajus xanthosternos), with observations of stone tool use at the lower limit of habitat suitability. Int. J. Primatol. 46: 573–597. https://doi.org/10.1007/s10764-024-00480-0
Mendes, F. D. C., Cardoso, R. M., Ottoni, E. B., Izar, P., Villar, D. N. A. e Marquezan, R. F. 2015. Diversity of nutcracking tool sites used by Sapajus libidinosus in Brazilian Cerrado. Am. J. Primatol. 77(5): 535–46. https://doi.org/10.1002/ajp.22373
Milleo, G. B. 2023. Aspectos Ecológicos E Comportamentais De Quatis Nasua nasua (Linnaeus, 1766) Do Parque Municipal Arthur Thomas, Londrina-PR. Dissertação de Mestrado, Universidade Estadual de Londrina, Paraná, Brasil.
Moraes, B. L. C., Silva Souto, A. D. e Schiel, N. 2014. Adaptability in stone tool use by wild capuchin monkeys (Sapajus libidinosus). Am. J. Primatol. 76(10): 967–977. https://doi.org/10.1002/ajp.22286
Ness, I. F. G., Jung, T. S. e Schmiegelow, F. K. A. 2022. Evaluating likelihood-based photogrammetry for individual recognition of four species of northern ungulates. Mamm. Biol. 102(3): 701–718. https://doi.org/10.1007/s42991-021-00223-1
O’Connell-Rodwell, C. E., Freeman, P. T., Kinzley, C., Sandri, M. N., Berezin, J. L., Wiśniewska, M., Jessup, K. e Rodwell, T. C. 2022. A novel technique for aging male African elephants (Loxodonta africana) using craniofacial photogrammetry and geometric morphometrics. Mamm. Biol. 102(3): 591–613. https://doi.org/10.1007/s42991-022-00238-2
Patterson, L., Kalle, R. e Downs, C. 2018. Factors affecing presence of vervet monkey troops in a suburban matrix in KwaZulu-Natal, South Africa. Landsc. Urban Plan. 169: 220–228. https://doi.org/10.1016/j.landurbplan.2017.09.016
Penedo, D. M., de Armada, J. L. A., da Silva, J. F. S., Neves, D. M., Pissinatti, A., e Nogueira, D. M. 2014. C-banding patterns and phenotypic characteristics in individuals of Sapajus (Primates: Platyrrhini) and its application to management in captivity. Caryologia, 67(4): 314–320. https://doi.org/10.1080/00087114.2014.980097
Powell, R. A. e Proulx, G. 2003. Trapping and marking terrestrial mammals for research: integrating ethics, performance criteria, techniques, and common sense. ILAR Journal 44(4): 259–276. https://doi.org/10.1093/ilar.44.4.259
QGIS.org, 2024. QGIS Geographic Information System. QGIS Association. https://qgis.org/
Resende, B. D., Ottoni, E. B. e Fragaszy, D. M. 2008. Ontogeny of manipulative behavior and nut-cracking in young tufted capuchin monkeys (Cebus apella): a perception-action perspective. Devel. Sci. 11(6): 828–840. https://doi.org/10.1111/j.1467-7687.2008.00731.x
Rezende, C. L., Scarano, F. R., Assad, E. D., Joly, C. A., Metzger, J. P., Strassburg, B. B. N., Tabarelli, M., Fonseca, G. A. e Mittermeier, R. A. 2018. From hotspot to hopespot: An opportunity for the Brazilian Atlantic. For. Perspec. Ecol. Conserv. 16(4): 208–14. https://doi.org/10.1016/j.pecon.2018.10.002
Richardson, J. L., Levy, E. J., Ranjithkumar, R., Yang, H., Monson, E., Cronin, A. J., Galbany, J., Robbins, M. M., Alberts, S. C., Reeves, M. E. e McFarlin, S. C. 2022. Automated, high-throughput image calibration for parallel-laser photogrammetry. Mamm. Biol. 102(3): 615–627. https://doi.org/10.1007/s42991-021-00174-7
Rocha, V. J., Reis, N. R. e Sekiama, M. L. 1998. Uso de ferramentas por Cebus apella (Linnaeus) (Primates, Cebidae) para obtenção de larvas de coleoptera que parasitam sementes de Syagrus romanzoffianum (Cham.) Glassm. (Arecaceae). Rev. Bras. Zool. 15(4): 945–50. https://doi.org/10.1590/S0101-81751998000400012
Ross, C. A. e Reeve, N. 2003. Survey and census methods: population distribution and density. Em: Field and Laboratory Methods in Primatology A Practical Guide, J. M., Setchell e D. J., Curtis (eds.), pp.90–109. Cambridge University Press, Cambridge.
Samuni, L., Mundry, R., Terkel, J., Zuberbühler, K. e Hobaiter, C. 2014. Socially learned habituation to human observers in wild chimpanzees. Anim. Cogn. 17(4): 997-1005. https://doi.org/10.1007/s10071-014-0731-6
Sugiyama, Y. 2015. Influence of provisioning on primate behavior and primate studies. Mammalia 79( 3): 255–265. https://doi.org/10.1515/mammalia-2014-0028
Sengupta, A. e Radhakrishna, S. 2018. The hand that feeds the monkey: mutual influence of humans and Rhesus Macaques (Macaca mulatta) in the context of provisioning. Int. J. Primatol. 39( 5): 817–830. https://doi.org/10.1007/s10764-018-0014-1
Spagnuolo, O. S. B., Lemerle, M. A., Holekamp, K. E. e Wiesel, I. 2022. The value of individual identification in studies of free-living hyenas and aardwolves. Mamm. Biol. 102: 1089–1112. https://doi.org/10.1007/s42991-022-00309-4
Steinberg, D. L., Lynch, J. W. e Cartmill, E. A. 2022. A robust tool kit: first report of tool use in captive crested capuchin monkeys (Sapajus robustus). Am. J. Primatol. 84: e23428. https://doi.org/10.1002/ajp.23428
Strier, K. B. 2016. Primate Behavioral Ecology. Routledge, London. https://doi.org/10.4324/9781315657127
STCP Engenharia de Projetos Ltda. 2004. Plano de Manejo Parque Municipal Arthur Thomas. Londrina, Paraná.
Tee, S. L., Samantha, L. D., Kamarudin, N., Akbar, Z., Lechner, A. M., Ashton-Butt, A. e Azhar, B. 2018. Urban forest fragmentation impoverishes native mammalian biodiversity in the tropics. Ecol Evol. 8(24): 12506–12521. https://doi.org/10.1002/ece3.4632
Thomas, K. S., Biffi, D., Chipps, A. S. Hale. A. H. e Williams, D. A. 2025. Gene flow of small mammals is inhibited by highways and the urbanized habitat matrix in a large urban forest fragment. Ecosphere 16(8): e70343. https://doi.org/10.1002/ecs2.70343
Tutin, C. E. G. e Fernandez, M. 1991. Responses of wild chimpanzees and gorillas to the arrival of primatologists: behaviour observed during habituation. Em: Primate Responses to Environmental Change, H.O. Box (ed.). Springer, Dordrecht.
Zago, L., Miranda, J. M. D., Ludwig, G. e Fernando, C. P. 2014. Primatologia de campo: métodos para estudos ecológicos e comportamentais. Em: A Primatologia no Brasil 13, F. C., Passos, J. M. D., Miranda (eds.), pp.2–34. Sociedade Brasileira De Primatologia, Curitiba, Paraná.
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