Hematological parameters of captive capuchin monkeys (Sapajus libidinosus and S. apella) illegally kept in homes in northeast Brazil
DOI:
https://doi.org/10.62015/np.2024.v30.836Keywords:
Hematology, capuchin monkey, captivity, one health, zoonosesAbstract
This study presents the hematological parameters of captive capuchin monkeys (Sapajus libidinosus and S. apella) kept in homes in the state of Ceará, in Northeast Brazil. Morphometry measurements and blood samples were taken from 35 individuals illegally kept as pets in 34 houses across 12 municipalities. The sample consists of 20 females and 15 males, classified in juvenile (n = 15), adult (n = 17) and senior (n = 3) age groups. The majority of animals were chained (74.2%) and dehydrated (62.8%), and almost half of them had injuries (48.57%). Except for three obese individuals, the animals weighed less than that described in other studies (2.08 kg ± 0.65, n=24), with greater differences in adult males (1.97 kg ± 0.55, n=3). Evidence for anemia included lower median red blood cell count (4.95 x 10⁶/µl ± 0.8) and higher mean corpuscular volume (76.6 fl ± 7.12) in the sample relative to other studies. Very low values of neutrophils (3.82 x 10³/µl ± 1.8) suggest a bone marrow condition or a severe active infection. In general, animals illegally kept as pets were in worse condition (with low body weight, dehydration, anemia and worse immunological conditions) when compared to reported data from wild animal populations, indicating a need to rescue these animals and rehabilitate them in rescue centers before releasing them back to their natural habitat.
References
Allison, R. W. 2015. Laboratory assessment of liver function. In: Veterinary Clinical Hematology and Biochemistry, 2nd ed. (eds.) M. A. Thrall, G. Weiser, R. W. Allison and T. W. Campbell, pp.853–903. Roca, São Paulo.
Barbosa, C., Sanches, L. and Freire, M. 2014. Zoonoses transmitted by wild animals originating from trafficking. Faculty of Veterinary Medicine and Animal Science of the University of São Paulo. Website: https://bichosonline.vet.br/wp-content/uploads/2016/07/Zoonoses-transmitidas-por-animais-silvestres-provenientes-de-tr%C3%A1fico.pdf. Accessed 21 August 2023.
Cardoso, D. de L., Costa, S. de M., Muniz, J. A. P. C., de Castro, P. H. G., da Costa, J. B. and Dias, H. L. T. 2021. Avaliação do perfil hematológico e bioquímico de macacos-de-cheiro (Saimiri collinsi) cativos no Centro Nacional de Primatas no Estado do Pará. Braz. J. Anim. Environ. Res. 4(2): 2764–2776. https://doi.org/10.34188/bjaerv4n2-097
Castañeda-Herrera, F. E., Cortés-Vera, M. and Vélez-García, J. F. 2020. Estudio hematológico en monos cariblancos (Cebus albifrons) en condiciones de cautiverio en Colombia. Rev. Investig. Vet. Perú 31(2): e17849. https://doi.org/10.15381/rivep.v31i2.17849.
Damasceno, T. M. M. 2022. Non-human primates received at screening centers in the Northeast between 2019 and 2022. Course Completion Work. Federal University of Rio Grande do Norte, Brazil. Website: https://repositorio.ufrn.br/handle/123456789/51347. Accessed 21 August 2023.
Destro, G. F. G., Pimentel, T. L., Sabaini, R. M., Borges, R. C. and Barreto, R. 2012. Efforts to combat wild animals trafficking in Brazil. In: Biodiversity Enrichment in a Diverse World, G. A. Lameed. IntechOpen, Rijeka (ed.). pp.421–436. https://doi.org/10.5772/48351
Diehl, K. H., Hull, R., Morton, D., Pfister, R., Rabemampianina, Y., Smith, D. and Vorstenbosch, C. V. D. 2001. A good practice guide to the administration of substances and removal of blood, including routes and volumes. J. Appl. Toxicol. 21(1): 15–23. https://doi.org/10.1002/jat.727
Duarte, N. F. H. 2022. Rabies in the state of Ceará: epidemiological characterization, surveillance actions and the population’s knowledge about the disease (1970–2020). Doctoral thesis, Federal University of Ceará, Fortaleza, Brazil.
Duarte, N. F. H., Alencar, C. H., Pires Neto, R. J., Moreno, J. O., Melo, I. M. L. A., Duarte, B. H. and Heukelbach, J. 2021. Integration of human rabies surveillance and preventive measures in the State of Ceará, Northeast Brazil. One Health Implement. Res. 1: 17–30. https://doi.org/10.20517/ohir.2021.02.
Duarte, N. F. H., Pires, R. D. J., Viana, V. F., Feijão, L. X., Alencar, C. H. and Heukelbach, J. 2021. Clinical aspects of human rabies in the state of Ceará, Brazil: an overview of 63 cases. Rev. Soc. Bras. Med. Trop. 54: e0104-2021. https://doi.org/10.1590/0037-8682-0104-2021.
Duarte, N. F. H., Barbosa, P. P. L., Araujo, D. B., Favoretto, S. R., Romijn, P. C., Neres, R. W. P. and Heukelbach, J. 2021. Knowledge, attitudes and practices regarding sylvatic rabies among high-risk households in Ceará State, Brazil. Trop. Med. Infect. Dis. 6(4): 209–224. https://doi.org/10.3390/tropicalmed6040209.
Estrada, A. et al. 2018. Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation. PeerJ 6: e4869. https://doi.org/10.7717/peerj.4869.
Favareto, A. D., Costa, M. M., Grumann, M. R., Silva Filho, J. R., da Silva, Z., Duda, N. C. B. and de Faria Valle, S. 2016. Hematological and biochemical profile of capuchin monkeys (Cebus spp.) kept in captivity. Braz. J. Vet. Med. 38(4): 406–412. Website: https://scispace.com/pdf/hematological-and-biochemical-profile-of-capuchin-monkeys-3x2368vmz8.pdf. Accessed 21 August 2023.
Ferreira, A. F., Queiroga, F. L., Mota, R. A., Rêgo, E. W., Mota, S. M., Teixeira, M. G. and Colaço, A. 2018. Hematological profile of captive bearded capuchin monkeys (Sapajus libidinosus) from Northeastern Brazil. Ciênc. Rural 48(10): 21–48. https://doi.org/10.1590/0103-8478cr20180065
Ferreira, V. H. B., Silva, C. P. C., Paiva, E., Chagas, A. C. C. S., Mesquita, L. G., Pelegrino, H., Galvão-Coelho, N., de Sousa Cordeiro, M. B. and Ferreira, R. G. 2018. Hormonal correlates of behavioral profiles and coping strategies in captive capuchin monkeys (Sapajus libidinosus). Appl. Anim. Behav. Sci. 207: 108–115. https://doi.org/10.1016/j.applanim.2018.07.002
Flaiban, K. K. M. D. C., Spohr, K. A. H., Malanski, L. D. S., Svoboda, W. K., Shiozawa, M. M., Hilst, C. L. S. and Lisbôa, J. A. N. 2008. Hematologic values of free-ranging Cebus cay and Cebus nigritus in southern Brazil. Int. J. Primatol. 29(5): 1375–1382. https://doi.org/10.1007/s10764-008-9290-5
Fragaszy, D. M., Visalberghi, E. and Fedigan, L. M. 2004. The Complete Capuchin: The Biology of the Genus Cebus. Cambridge University Press, Cambridge.
Garber, P. A., McKenney, A., Bartling-John, E., Bicca-Marques, J. C., de La Fuente, M. F., Abreu, F., Schiel, N., Souto, A. and Phillips, K. A. 2020. Life in a harsh environment: the effects of age, sex, reproductive condition, and season on hair cortisol concentration in a wild non-human primate. PeerJ 8: e9365. https://doi.org/10.7717/peerj.9365
García-Feria, L. M., Chapman, C. A., Pastor-Nieto, R. and Serio-Silva, J. C. 2017. Biochemical and hematological evaluations of black howler monkeys (Alouatta pigra) in highly degraded landscapes in Mexico. J. Med. Primatol. 46(6): 304–310. https://doi.org/10.1111/jmp.12286
Hernández-Cruz, G., Ferreira, R. G., Rooney, N. J., Guidi, R. D. S., Rego, R. D. P. D., Costa, T. S. F. and Mendl, M. 2022. Haematology, physiological parameters, morphometry and parasitological status of rescued bearded capuchin monkeys (Sapajus libidinosus). J. Med. Primatol. 51(4): 213–222. https://doi.org/10.1111/jmp.12584
IBGE – Brazilian Institute of Geography and Statistics, 2021. Territorial area of the country. Website: https://ibge.gov.br/geociencias/organizacao-do-territorio/estrutura-territorial/15761-areas-dos-municipios.html. Accessed 15 June 2023.
IBGE – Brazilian Institute of Geography and Statistics, 2022. Preview of the population calculated based on the results of the 2022 Demographic Census until December 25, 2022. Website: https://www.ibge.gov.br/CE_POP2022. Accessed 28 January 2023.
ICMBio, 2023. Diversity of the world’s non-human primates. Website: https://www.icmbio.gov.br/cpb/index.php/primatas-brasileiros. Accessed 15 June 2023.
IUCN, 2024. The IUCN Red List of Threatened Species. Version 2024-1. Website: https://www.iucnredlist.org. Accessed 12 September 2024.
Larsson, M. H. M. A., Birgel, E. H., Benesi, F. J., Birgel Jr., E. H., Lazaretti, P., Fedullo, J. D. L. and Prada, C. S. 1999. Hematological values of Cebus apella anesthetized with ketamine. Braz. J. Vet. Res. Anim. Sci. 36: 131–135. https://doi.org/10.1590/S1413-95961999000300005.
Larsson, M. H. M. A., Lucas, S. R. R., Mirandola, R. M. S., Lazaretti, P., Fedullo, J. D. L. and Guimarães, M. A. B. V. 1997. Reference values for liver and kidney function tests and some electrolytes in Cebus apella anesthetized with ketamine. Ciênc. Rural 27: 257–262. https://doi.org/10.1590/S0103-84781997000200014.
Levacov, D., Jerusalinsky, L. and Fialho, M. de S. 2011. Survey of primates received in Triage Centers and their relationship with wildlife trafficking in Brazil. Primatol. Braz. 11: 281–305.
Lima, D. B. C., Santos, K. D., Almeida, H. D., Nascimento, C. B., Conde Júnior, A. M. and Rizzo, M. D. S. 2014. Evaluation of hematological profile, biochemical and peripheral blood smear with a view to the health profile in primates of the Cebus genus maintained in captivity. Semina 35: 1847–1854.
de Miranda, C. B., Cabala, R. W., Atan, J. B. C. D., Müller, L. C. C. M., Silva, P. C., de Magalhães Vivas, L. A. and Ferreira, M. L. 2011. Contenção farmacológica em primatas não-humanos com emprego de ketamina e xilazina: uma revisão bibliográfica. Pubvet 5: Art-1043. https://doi.org/10.22256/pubvet.v5n8.1045
Naves, E. de A., Ferreira, F. A., Mundim, A. V. and Guimarães, E. C. 2006. Hematological values of capuchin monkeys (Cebus apella Linnaeus, 1758) in captivity. Biosci. J. https://pesquisa.bvsalud.org/portal/resource/pt/lil-561908. Accessed 21 August 2023.
Nellemann, C., Henriksen, R., Pravettoni, R., Stewart, D., Kotsovou, M., Schlingemann, M., Shaw, M. and Reitano, T. (eds.). 2018. World atlas of illicit flows. A RHIP-TO-INTERPOL-GI assessment. RHIPTO Norwegian Center for Global Analyses, INTERPOL and the Global Initiative Against Transnational Organized Crime, Oslo. pp.12–17.
Núñez, H., Araya, M., Cisternas, F., Arredondo, M., Méndez, M., Pizarro, F., Ortiz, A., Ortiz, R. and Olivares, M. 2008. Blood biochemical indicators in young and adult Cebus apella of both sexes. J. Med. Primatol. 37(1): 47-50. https://doi.org/10.1111/j.1600-0684.2007.00215.x
Nunes, V. F., Lopes, P. M. and Ferreira, R. G. 2021. Monkeying around the Anthropocene: patterns of human–nonhuman primate interactions in Brazil. Ethnobiol. Conserv. 10: 1–32. https://doi.org/10.15451/ec2021-04-10.23-1-32.
Nunes, V. F., Lopes, P. M. and Ferreira, R. G. 2023. #Capuchinmonkeys on social media: a threat for species conservation. Anthrozoös 36: 1–19. https://doi.org/10.1080/08927936.2023.2210440.
Ramalho, C. A., Guimarães, R. A. de A., Cavalcante, T.A., Stipp, D. T. and Guerra, R. R. 2015. Identification of enterobacteria in Galician capuchin monkeys (Sapajus flavius) kept in captivity in the state of Paraíba. Rev. Biotemas 28: 177–180. Website: https://doi.org/10.5007/2175-7925.2015v28n3p177.
Renctas – National Network to Combat Wild Animal Trafficking. 2001. 1st National Report on Wildlife Trafficking. Website: https://renctas.org.br/trafico-de-animais/. Accessed 12 February 2024.
Ribeiro, C. L. B., Melo-Reis, P. R., Lemes, S. R., de Araújo, L. A. and da Silva-Júnior, N. J. 2015. Hematological analysis of capuchin monkeys (Sapajus libidinosus Spix, 1923) and howler monkeys (Alouatta caraya Humboldt, 1812) free-living in the south of the state of Tocantins. Brazil. Braz. J. Biosci. 12: 110–114.
Riviello, M. C. and Wirz, A. 2001. Hematology and blood chemistry of Cebus apella in relation to sex and age. J. Med. Primatol. 30: 308–321. https://doi.org/10.1034/j.1600-0684.2001.300604.x.
Sacramento, T. S., Mendes, F. D. C., Peres, M. K. and Tavares, M. C. H. 2017. Feeding behavior and activity pattern of capuchin monkeys (Sapajus libidinosus) kept in Brasília National Park, D. F. In: Primatology in Brazil 114, M. A. B. Oliveira, R. G. Ferreira and V. Luna da Silva (eds.), pp.158–172. Editora Sociedade Brasileira de Primatologia, Recife.
Santos, M. C., Gomes, D. M., Lima, M. R., Santos, M. V., Santos, U. G., Cerqueira, R. B. and Pedroso, P. M. 2021. Estudo quantitativo de animais silvestres recebidos nos Centros de Triagem de Animais Silvestres (CETAS) da Bahia e identificação de rotas de tráfico. Pesq. Vet. Bras. 41: e06942. https://doi.org/10.1590/1678-5150-PVB-6942.
Santos, M. V. S. 2006. Survey of intestinal helminths in red-headed howler monkeys (Alouatta guariba, Primates, Atelidae) in the Ribeirão Cachoeira forest, district of Souzas. Master’s thesis, State University of São Paulo, Campinas, SP, Brazil.
Silva Júnior, J. S. 2001. Especiação nos macacos-prego e caiararas, gênero Cebus Erxleben, 1777 (Primates, Cebidae). Doctoral thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
Silva, G. P. d., Pereira, T. H. S., de Melo, J. T., Imbeloni, A. A., de Andrade, R. S., Monteiro, M. V. B., Monteiro, F. O. B. and Takeshita, R. S. C. 2023. Hematological and serum biochemistry evaluation in howler monkeys (Alouatta caraya) and capuchin monkeys (Sapajus apella): a comparative study. J. Med. Primatol. 52(3). https://doi.org/10.1111/jmp.12644.
Sousa, G. A., Paludo, G. R., Teixeira, D. S. and Morais Ribeiro, B. 2020. Haematological and biochemical parameters of wild capuchin monkeys in Brasília, Federal District, Brazil. J. Med. Primatol. 49(4): 211–217. https://doi.org/10.1111/jmp.12468.
Stockham, S. L. and Scott, M. A. 2011. Fundamentos da Patologia Clínica Veterinária, 2ª ed. Guanabara Koogan, Rio de Janeiro. Thrall, M. A. 2015. Erythrocyte morphology. In: Veterinary Clinical Hematology and Biochemistry (2nd ed.), M. A. Thrall, G. Weiser, R. W. Allison and T. W. Campbell (eds.), pp.222–225. Roca, São Paulo.
Weiser, G. 2015. Interpretation of the leukocyte response in disease. In: Veterinary Clinical Hematology and Biochemistry 2nd ed., M. A. Thrall, G. Weiser, R. W. Allison and T. W. Campbell (eds.), pp.276–305. Roca, São Paulo.
Wirz, A., Truppa, V. and Riviello, M. C. 2008. Hematological and plasma biochemical values for captive tufted capuchin monkeys (Cebus apella). Am. J. Primatol. 70: 463–472. https://doi.org/10.1002/ajp.20520.
Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourn, A., Spielman, A. and Lal, A. A. 1998. Wild primate populations in emerging infectious disease research: the missing link? Emerg. Infect. Dis. 4(2): 149–156. https://doi.org/10.3201/eid0402.980202.
Zago, G. 2018. Factors that affect enteroparasitosis in capuchin monkeys (Sapajus libidinosus) from the Cerrado/Caatinga ecotone. Doctoral thesis, University of São Paulo, Institute of Psychology, São Paulo, Brazil. Website: https://teses.usp.br/teses/disponiveis/47/47132/tde-01042019-101708/pt-br.php. Accessed 8 July 2025
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Copyright (c) 2024 Naylê Francelino Holanda Duarte, Gabriele Vitor de Andrade, Katariny Michelle de Araújo Pinheiro Tavares, Victoria Forte Viana, Patrícia Pereira Lima Barbosa, Bruna Holanda Duarte, Walber Feijó de Oliveira, Jorg Heukelbach, Renata Gonçalves Ferreira
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