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Threats to health and conservation of free-living sloths (Bradypus and Choloepus) under anthropic influence in the city of Manaus, Amazonas state, Brazil

Ameaças à saúde e conservação de preguiças (Bradypus e Choloepus) de vida livre sob influência antrópica em Manaus, Estado do Amazonas, Brasil

Abstract

Anthropogenic disturbances affecting forest areas can increase disease prevalence and susceptibility in several species of arboreal mammals, such as sloths. Thus, this study aimed to evaluate the most common conditions in body systems of free-ranging sloths admitted at the Wildlife Triage and Rehabilitation Center of Amazonas of the Institute of Environment and Renewable Natural Resources. A total of 227 individuals (139 retrospective cases from 2015 to 2019, and 88 prospective cases from July 2020 to July 2021) were evaluated over a six-year period. Cases from the genus Bradypus showed involvement of the following body systems: 44% respiratory, 29% integumentary, 15% musculoskeletal, 5% digestive, 3% visual, 2% auditory, 1% circulatory and 1% genitourinary, while that distribution in the genus Choloepus was: 39% musculoskeletal, 27% integumentary, 19% respiratory, 9% digestive, 3% circulatory, 1% visual, 1% auditory and 1% genitourinary. The results reveal significant differences between the condition detected and the genus (Bradypus and Choloepus), age and case outcome. These results can provide data for future investigations of sloth diseases, confirming lesions, as well as motivating and suggesting adequate management methods.

Keywords
Wild animals; Xenarthra; Pilosa; clinic; diseases

Resumo

Distúrbios antrópicos que afetam áreas florestais podem aumentar a prevalência de afecções e a suscetibilidade às doenças em diversas espécies de mamíferos arborícolas, como as preguiças. Desta forma, este estudo teve como objetivo avaliar as condições mais comuns nos sistemas orgânicos de preguiças de vida livre admitidas no Centro de Triagem e Reabilitação de Animais Silvestres do Amazonas. Um total de 227 indivíduos (139 casos retrospectivos de 2015 a 2019 e 88 casos prospectivos de julho de 2020 a julho de 2021) foram avaliados durante um período de seis anos. Para o gênero Bradypus foram diagnosticadas 44% de afecções do sistema respiratório, 29% tegumentar, 15% musculoesquelético, 5% digestório, 3% visual, 2% auditivo, 1% circulatório e 1% genitourinário. Por sua vez, para o gênero Choloepus foram detectadas 39% de afecções do sistema musculoesquelético, 27% tegumentar, 19% do sistema respiratório, 19% do sistema respiratório, 9% digestório, 3% circulatório, 1% visual, 1% auditivo e 1% genitourinário. Os resultados mostraram diferenças significativas na prevalência da afecção e gênero das preguiças (Bradypus e Choloepus), a faixa etária e desfecho do caso. Esses resultados podem fornecer subsídios para investigar as doenças de preguiças, confirmando afecções, motivo e sugerir métodos adequados de manejo.

Palavras-chave
Animais selvagens; Xenarthra; Pilosa; clínica; doenças

Introduction

Urban expansion, habitat loss, fragmentation, and climate change represent complex scenarios that can alter health in the human-animal-plant-environment interface, increasing the risk of zoonotic diseases in the One Health perspective (Jones et al. 2008JONES, K.E., PATEL, N.G., LEVY, M.A., STOREYGARD, A., BALK, D., GITTLEMAN, J.L. & DASZAK, P. (2008). Global trends in emerging infectious diseases. Nature. 451(7181):990–993., Thompson et al. 2016THOMPSON, P.L., RAYFIELD, B. & GONZALEZ, A. 2016. Loss of habitat and connectivity erodes species diversity, ecosystem functioning, and stability in metacommunity networks. Ecography. 40:98–108. , OHHLEP et al. 2022One Health High-Level Expert Panel (OHHLEP), ADISASMITO, W.B., ALMUHAIRI, S., BEHRAVESH, C.B., BILIVOGUI, P., BUKACHI, S.A., CASAS, N., CEDIEL BECERRA, N., CHARRON, D.F., CHAUDHARY, A., CIACCI ZANELLA, J.R., CUNNINGHAM, A. A., DAR, O., DEBNATH, N., DUNGU, B., FARAG, E., GAO, G.F., HAYMAN, D.T.S., KHAITSA, M., KOOPMANS, M.P.G., MACHALABA, C., MACKENZIE, J.S., MARKOTTER, W., METTENLEITER, T.C., MORAND, S., SMOLENSKIY, V. & ZHOU, L. 2022. One Health: A new definition for a sustainable and healthy future. PLoS Pathog. 18(6):e1010537.). The monitoring of diseases in wildlife plays a fundamental role in the zoonotic disease dynamics in nature and may contribute to the evaluation of the prevalence, surveillance, and dissemination of important diseases for animal and environmental health (Jones et al. 2008JONES, K.E., PATEL, N.G., LEVY, M.A., STOREYGARD, A., BALK, D., GITTLEMAN, J.L. & DASZAK, P. (2008). Global trends in emerging infectious diseases. Nature. 451(7181):990–993., Rahman et al. 2020RAHMAN, M.T., SOBUR, M.A., ISLAM, M.S., IEVY, S., HOSSAIN, M.J., EL ZOWALATY, M.E., RAHMAN, A.T. & ASHOUR, H.M. 2020. Zoonotic diseases: etiology, impact, and control. Microorganisms. 8(9):1405.).

The Amazon, the largest biome in South America, is located in a humid tropical area with constant temperatures and climatic oscillations that vary between dry and wet rainy seasons (Veblen et al. 2007VEBLEN, T.T., YOUNG, K.R. & ORME, A.R. 2007. The Physical Geography of South America, Oxford University Press, Oxford, United Kingdom.). However, more and more Amazon areas are threatened by anthropic factors, such as constant fires and deforestation, which pose threats of extinction to endemic species (Silva et al. 2020SILVA, S.M., SANTOS P.M., MOLINA, K.T., LOPES, A.M.C., BRAGA, F.G., OHANA, A., MIRANDA, F.R. & BERTASSONI, A. 2020. Wildfire against the survival of Xenarthra: anteaters, armadillos, and sloths. Bol. Mus. Para. Emílio. Goeldi. Cienc. Nat. 15(3):523–532.). These anthropic factors increase the risks to diversity, even in species with high adaptation to environmental changes, since they become not only vulnerable to habitat fragmentation and degradation but also susceptible to diseases, which can occur in ecotones among wildlife, domestic animals and humans (Santos et al. 2017SANTOS, L.S., PEREIRA, H. & GORDO, M. 2017. Interações entre população humana e saium-de-coleira (Saguinus bicolor) em fragmentos florestais urbanos de Manaus, Amazonas - Brasil. In Olhares cruzados sobre as relações entre seres humanos e animais silvestres na Amazônia (Brasil, Guiana Francesa) (G. Marchand & F.V. Velden, eds). EDUA, Manaus, p.85–102.).

The superorder Xenarthra is divided into two orders, Cingulata (armadillos) and Pilosa (anteaters and sloths), comprising about 31 living species distributed throughout the Neotropical region (Rose & Gaudin 2010ROSE, K.D. & GAUDIN, T.J. 2010. Xenarthra and Pholidota (Armadillos, Anteaters, Sloths and Pangolins). In Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, United Kingdom., Martins et al. 2015MARTINS, A.B., SILVA, K.F.M., FIALHO, M.S. & MIRANDA, F.R. 2015. Avaliação do estado de conservação de Pilosa e Cingulata no Brasil. In Avaliação do Risco de Extinção dos Xenarthros Brasileiros (Instituto Chico Mendes de Conservação da Biodiversidade, ed.). ICMBio, Brasília, p.7–11.). The order Pilosa, suborder Folivora, includes two distinct families of sloths, Bradypodidae (three-toed sloths), and Megalonychidae (two-toed sloths) (Gardner 2007GARDNER, A.L. 2007. Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. The University of Chicago Press, Chicago, USA., Gibb et al. 2016GIBB, G.C., CONDAMINE, F.L., KUCH, M., ENK, J., MORAES-BARROS, N., SUPERINA, M. & DELSUC, F. 2016. Shotgun mitogenomics provides a reference phylogenetic framework and timescale for living Xenarthrans. Mol. Biol. Evol. 33(3):621–642.). The family Bradypodidae contains the species Bradypus pygmaeus, B. tridactylus, B. variegatus, B. torquatus (Gardner 2007GARDNER, A.L. 2007. Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. The University of Chicago Press, Chicago, USA.), and more recently B. crinitus according to a new taxonomic rearrangement (Miranda et al. 2023LOPES, G.S., CASSANO, C.R., MUREB, L.S., MIRANDA, F.R., CRUZ-NETO, A.P., & GINÉ, G.A.F. 2023. Combined effect of ambient temperature and solar radiation on maned sloths’ behaviour and detectability. Austral Ecol. 1–17. ). Members of the genus Bradypus are generally solitary and arboreal, exhibit strictly folivorous habits, are excellent swimmers and use treetops exposed to the sun for thermoregulation (Medri et al. 2006MEDRI, I.M., MOURÃO, G.M. & RODRIGUES, F.H.G. 2006. Ordem Xenarthra. In Mamíferos do Brasil (N.R. Reis, A.L Peracchi, W.A. Pedro & I.P. Lima, eds). UEL, Londrina, Paraná, p.71–99., Miranda 2014MIRANDA, F. 2014. Cingulata (tatus) e Pilosa (preguiças e tamanduás). In Tratado de animais selvagens (Z.S. Cubas, J.C.R. Silva & J.L. CATÃO-DIAS, eds). São Paulo, Roca, p.707–722.). The family Megalonychidae with two species of the genus Choloepus (Choloepus didactylus and Choloepus hoffmanni) is characterized by omnivorous sloths that consume a greater variety of food items, including fruits, flower buds and small vertebrates (Esbérard 2001ESBÉRARD, C. 2001. Biology and Captive Management of Sloths, Order Xenarthra (Edentata) (Sloths, Armadillos, Anteaters). In Biology, Medicine, and Surgery of South American Wild Animals (M.E. Fowler & Z.S. Cubas, eds). Iowa State Press, Iowa, USA, p.245–246., Miranda 2014MIRANDA, F. 2014. Cingulata (tatus) e Pilosa (preguiças e tamanduás). In Tratado de animais selvagens (Z.S. Cubas, J.C.R. Silva & J.L. CATÃO-DIAS, eds). São Paulo, Roca, p.707–722.). In addition, this family is primarily nocturnal, using trees with lianas, vines, and tree-creepers for rest and protection against possible predators (Wetzel 1982WETZEL, R.M. 1982. Systematics, distribution, ecology and conservation of South American edentates. In Mammalian biology in South America (M.A. Mares & H.H. Genoways, eds). University Pittsburgh, Pennsylvania, USA, p.345–375., Medri et al. 2006MEDRI, I.M., MOURÃO, G.M. & RODRIGUES, F.H.G. 2006. Ordem Xenarthra. In Mamíferos do Brasil (N.R. Reis, A.L Peracchi, W.A. Pedro & I.P. Lima, eds). UEL, Londrina, Paraná, p.71–99.). Sloths depend on trees to perform various daily activities, so deforestation and urban expansion imply habitat loss (Medri et al. 2006MEDRI, I.M., MOURÃO, G.M. & RODRIGUES, F.H.G. 2006. Ordem Xenarthra. In Mamíferos do Brasil (N.R. Reis, A.L Peracchi, W.A. Pedro & I.P. Lima, eds). UEL, Londrina, Paraná, p.71–99., Dünner & Pastor 2017DÜNNER C, PASTOR G. 2017. Manual de Manejo, Medicina y Rehabilitación de Perezosos. Fundación Huálamo, Chile.). Besides mortality from anthropic factors, human-wildlife interaction can trigger the increase in diseases that these sloths can acquire, in addition to other conditions.

The Brazilian Amazon harbors four sloth species: two of the genus Choloepus (Choloepus didactylus, Choloepus hoffmanni) and two of the genus Bradypus (Bradypus tridactylus and Bradypus variegatus) (Wetzel 1985WETZEL R.M. 1985. The identification and distribution of recent Xenarthra (Edentata). In The Evolution and Ecology of Armadillos, Sloths and Vermilinguas (G. Montgomery, ed). Smithsonian Institution Press, Washington, DC., Medri et al. 2006MEDRI, I.M., MOURÃO, G.M. & RODRIGUES, F.H.G. 2006. Ordem Xenarthra. In Mamíferos do Brasil (N.R. Reis, A.L Peracchi, W.A. Pedro & I.P. Lima, eds). UEL, Londrina, Paraná, p.71–99., Chiarello et al. 2022CHIARELLO, A., PLESE, T., DE THOISY, B., POOL, M., ALIAGA-ROSSEL, E., SANTOS, P. & MORAES-BARROS, N. 2022. Choloepus didactylus. The IUCN Red List of Threatened Species 2022:e.T4777A210443323. Accessed on 11 June 2023., Moraes-Barros et al. 2022MORAES-BARROS, N., CHIARELLO, A., PLESE, T., SANTOS, P., ALIAGA-ROSSEL, E., AGUILAR BORBÓN, A. & TURCIOS CASCO, M. 2022. Bradypus variegatus. The IUCN Red List of Threatened Species 2022: e.T3038A210442893. Accessed on 11 June 2023., Plese et al. 2022CHIARELLO, A., PLESE, T., DE THOISY, B., POOL, M., ALIAGA-ROSSEL, E., SANTOS, P. & MORAES-BARROS, N. 2022. Choloepus didactylus. The IUCN Red List of Threatened Species 2022:e.T4777A210443323. Accessed on 11 June 2023., Pool et al. 2022CHIARELLO, A., PLESE, T., DE THOISY, B., POOL, M., ALIAGA-ROSSEL, E., SANTOS, P. & MORAES-BARROS, N. 2022. Choloepus didactylus. The IUCN Red List of Threatened Species 2022:e.T4777A210443323. Accessed on 11 June 2023.). Three of these species are found in forest areas and neighborhoods in the city of Manaus, Amazonas. Studies in a forest fragment in the Manaus region found that Bradypus tridactylus and Choloepus didactylus were equally abundant in primary and secondary forests (Carmo 2003CARMO, N.A.S. 2003. Densidade e distribuição espacial de Bradypus tridactylus (Mammalia: Edentata: Xenarthra) em um fragmento florestal urbano de Manaus, AM, Brasil. In VI Congresso de Ecologia do Brasil, Fortaleza. p.42–43., Mata 2009MATA, V. C. A, 2009. Distribuição temporal e geográfica dos resgates de 6 espécies de mamíferos em Manaus entre 2002 e 2008. Universidade Federal do Amazonas – UFAM. Manaus. AM. Relatório (Estágio de Monografia II) p.17.). Despite the threats to which they are exposed, the IUCN (International Union for Conservation of Nature) classifies them as threat status in the Least Concern (LC) category (Chiarello et al. 2022CHIARELLO, A., PLESE, T., DE THOISY, B., POOL, M., ALIAGA-ROSSEL, E., SANTOS, P. & MORAES-BARROS, N. 2022. Choloepus didactylus. The IUCN Red List of Threatened Species 2022:e.T4777A210443323. Accessed on 11 June 2023., Moraes-Barros et al. 2022MORAES-BARROS, N., CHIARELLO, A., PLESE, T., SANTOS, P., ALIAGA-ROSSEL, E., AGUILAR BORBÓN, A. & TURCIOS CASCO, M. 2022. Bradypus variegatus. The IUCN Red List of Threatened Species 2022: e.T3038A210442893. Accessed on 11 June 2023., Plese et al. 2022PLESE, T., CHIARELLO, A., TURCIOS CASCO, M., AGUILAR BORBÓN, A., SANTOS, P., ALIAGA-ROSSEL, E. & MORAES-BARROS, N. 2022. Choloepus hoffmanni. The IUCN Red List of Threatened Species 2022: e.T4778A210443596. Accessed on 11 June 2023., Pool et al. 2022POOL, M., DE THOISY, B., MORAES-BARROS, N. & CHIARELLO, A. 2022. Bradypus tridactylus. The IUCN Red List of Threatened Species 2022: e.T3037A210442660. Accessed on 11 June 2023.). However, urban expansion compromises conservation areas for the species (Andrade et al. 2020ANDRADE, A.C., MEDEIROS, S. & CHIARELLO, A.G. 2020. City sloths and marmosets in Atlantic forest fragments with contrasting levels of anthropogenic disturbance. Mammal Res. 65(3):481–491.), making it one of the leading causes of admissions to the Wildlife Sorting Center that receives animals rescued, trafficked, or delivered by the population.

In order to contribute to the comprehension and conservation of wildlife species, this study aimed to evaluate the most common conditions in body systems of free-ranging sloths admitted at the Wildlife Triage and Rehabilitation Center of Amazonas of the Institute of Environment and Renewable Natural Resources (CETAS/IBAMA-AM) and to discuss the possible implications of the urban expansion for the sloths’ health. To the best of the authors’ knowledge, data have not yet been documented for sloths in the Manaus region, Amazonas state, Brazil.

Material and Methods

This study was approved by Ethics Committee for Animal Care and Use from the School of Veterinary Medicine and Animal Science, UNESP Campus Botucatu, SP-Brazil (no. 0031/2020–CEUA). Data from sloths (Choloepus didactylus, Bradypus tridactylus, Bradypus variegatus) admitted at the CETAS/IBAMA-AM were collected, analyzed and categorized over a period of six years (2015 to 2021). Data were collected from two different information sources: (a) retrospective consultation of the files and database from the Supervisory nucleus (NUFIS) of the CETAS/IBAMA-AM from 2015 to 2019; (b) prospective analysis, with follow-up for one year (July 2020 to July 2021) of all sloths received at CETAS/IBAMA-AM with an individualized clinical record. In both data collections, the variables checked included locality, admission history, sex, age group (adult, juvenile, young), body weight, clinical diagnosis and case outcome (survival or death).

To categorize the data, a nominal qualitative variable analysis was performed, identifying the main conditions according to the following systems: musculoskeletal, integumentary, visual, auditory, digestive, respiratory, circulatory and genitourinary. Since the cases of the musculoskeletal system presented a high percentage, the occurrence registration was based on the degree of case concentration in the neighborhoods. A map of Manaus city, Amazonas state, enabled estimation of the locations where the highest numbers of animals were found. By calculating Cramér’s V coefficient (Cramér 1999CRAMÉR, H. 1999. Mathematical Methods of Statistics. Princeton University Press, Princeton, New Jersey.), implemented in the R package “rcompanion” (R Core Team, 2021R CORE TEAM. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
https://www.R-project.org/...
; Mangiafico 2022MANGIAFICO, S. 2022. rcompanion: Functions to Support Extension Education Program Evaluation. R package version 2.4.13. https://CRAN.R-project.org/package=rcompanion
https://CRAN.R-project.org/package=rcomp...
), we evaluated the existence of a prevalence between age and condition type, as well as animal mortality and/or outcome predictors (death or survival). The correlation was defined as strong, moderate, or weak (range, 0.63–0.81) (Cohen 1988COHEN, J. 1988. Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates, Hillsdale, New Jersey.). The calculation was repeated for 10,000 bootstraps to obtain a 95% confidence interval.

Results

Data were analyzed from 227 sloths, including 139 retrospective (2015 to 2019) and 88 prospective cases (July 2020 to July 2021). A total of 60% of the animals were males, 30% were females, and 10% had no information as to sex. Sloths were 48% adult animals, 31% young and 21% juveniles. Body weight was not provided in the retrospective data. Body weight information was only obtained in prospective cases (n = 88), ranging from 203 g to 6.3 kg for the genus Bradypus and from 307 g to 8.8 kg for the genus Choloepus. The reasons for admission included: rescue (73%) carried out by a competent authority associated with electrocution, dog attacks, or having been hit by a car; and admission volunteer agreement to deliver the animal (27%) was usually related to being orphaned/abandoned or dispersed in backyards. There was no information in 8% of the cases. The conditions according to the systems are shown in Table 1.

Table 1
Conditions on body systems in 227 free-ranging sloths of the genera Bradypus and Choloepus admitted at the Wildlife Triage and Rehabilitation Center of Amazonas of the Institute of Environment and Renewable Natural Resources (CETAS/IBAMA-AM).

The highest percentage of cases occurred in Bradypus related to respiratory (44%) and integumentary (29%) systems. In the respiratory system were observed mainly bronchopneumonia and pneumonia, but there were cases with no specific cause. A correlation coefficient of 0.72 was detected between these respiratory diseases and age, which was most frequent in young Bradypus sloths (20%). In relation to the integumentary system, the most significant lesions were skin lacerations caused by dog bites and burns due to electrocution, besides mites (Sarcoptes scabiei) and ticks (Amblyomma spp.), which had a high prevalence of infestation.

In the genus Choloepus, the prevalence of lesions were associated with the integumentary (39%) and musculoskeletal (27%) systems. Cases related to the integumentary system involved skin lacerations of the head caused by an attack by a domestic animal (dog); palmar and facial lacerations due to conflict with conspecifics; and burns of different degrees due to electrocution. The lesions in the musculoskeletal system consisted of fractures and luxations. In general, the fractures involved the femur, radius/ulna, or multiple ones involving more than one bone, caused by being hit by a car or by electrocution. There was also one case of osteosclerosis of the interphalangeal joints attributable to deformity of the claws/nails.

Figure 1 shows primary conditions according to the following systems: musculoskeletal, integumentary, visual, auditory, digestive, respiratory, circulatory, and genitourinary. The west zone of Manaus presented the greatest concentration of musculoskeletal and integumentary system conditions (example fractures, skin laceration and burns), and reported the second-highest rate of population growth of the decade in the region and ecological consequences of forest fragmentation in the Amazon rainforests (Figure 2).

Figure 1
Prevalence between affected system and sloth genus (Bradypus and Choloepus).
Figure 2.
Records of the occurrence of musculoskeletal and integumentary lesions in sloths verified in the city of Manaus-AM.

Regarding the other systems, the percentage was very similar for both genera, as shown in Table 1. Eye injuries and traumatic corneal ulcers were detected in the visual system. In the auditory system, only one sloth of the genus Bradypus presented fungal otitis (Malassezia spp.) with no defined history. In the digestive system, the following were observed: bloat associated with multiple traumas and gastric impaction, parasite infections (coccidiosis/giardiasis), malabsorption syndrome and fecaloma because of inadequate diet, and rectal prolapse due to constipation. Age was associated with the affected system, and a correlation coefficient of 0.81 was detected between these digestive diseases and age, which was most frequent in young Choloepus (22%). As to the circulatory system, animals were identified with endocarditis and cardiomyopathy, whereas the genitourinary system presented cases of urinary obstruction.

The outcome of the cases (death or survival) did not differ statistically in relation to age (p > 0.05), but there was a significant difference when comparing outcome and affected system (p < 0.001). The musculoskeletal, respiratory and integumentary systems were the main outcome predictors of death, comprising 70% of the cases, while the survival outcome corresponded to 30%.

Discussion

The present study showed data on the principal conditions in body systems of sloths that live in the region of Manaus, Amazonas state, Brazil. Studies on sloths are generally focused on taxonomy and ecology (Xenarthra, Pilosa) (Carmo 2003CARMO, N.A.S. 2003. Densidade e distribuição espacial de Bradypus tridactylus (Mammalia: Edentata: Xenarthra) em um fragmento florestal urbano de Manaus, AM, Brasil. In VI Congresso de Ecologia do Brasil, Fortaleza. p.42–43., Aguiar 2004AGUIAR J.M. 2004. Species summaries and species discussions. Edentata. 6:3–26., Réus & Sousa 2007RÉUS C.L. & SOUZA C.M. 2007. Population structure of Bradypus tridactylus (Xenarthra, Bradypodidae) in Manaus forest urban fragment, Amazonas State, Brazil. Estud. Biol. 29:249–256., Moraes-Barros 2011MORAES-BARROS, N., SILVA, J.A.B. & MORGANTE, J.S. 2011. Morphology, molecular phylogeny, and taxonomic inconsistencies in the study of Bradypus sloths (Pilosa: Bradypodidae). J. Mammal. 92:86–100., Vidal 2018VIDAL, L.V. 2018. Área de uso, uso do espaço e padrão de atividades de Bradypus tridactylus (Pilosa: bradypodidae) em um fragmento florestal na Amazônia Central. Dissertação, Universidade Federal do Amazonas, Manaus.). Although such studies contribute to conservation, they have not address the health problems resulting from anthropization, which may threaten the conservation of these mammals (Lopes & Ferrari 2000LOPES M.A. & FERRARI S.F. 2000. Effects of human colonization on the abundance and diversity of mammals in eastern Brazilian Amazonia. Conserv. Biol. 14 (6):1658–1665. ).

In the genus Choloepus, the highest percentage of lesions corresponded to the integumentary and musculoskeletal systems confirming that free-living sloths are subject to traumas such as being hit by a car, falling trees, electrocution, and fights with domestic animals. A sloth rehabilitation center in Colombia also verified that C. hoffmanni has been subjected to several injuries, including being hit by cars, stoned by children, or electrical shocks, even with the greater adaptability of these sloths to habitat alteration (Moreno & Plese 2006MORENO, S. & PLESE, T. 2006. The illegal traffic in sloths and threats to their survival in Colombia. Edentata 6:10–18. ).

The integumentary system presents a similar morphology for both genus (Dünner & Pastor 2017DÜNNER C, PASTOR G. 2017. Manual de Manejo, Medicina y Rehabilitación de Perezosos. Fundación Huálamo, Chile.), which probably influenced this system to have a high proportion of cases in both genera in the current study. Two ectoparasites were detected in the sloths, Sarcoptes scabiei and Amblyomma spp. The infestation by Sarcoptes scabiei has also be described in C. hoffmanni and B. variegatus in captivity from Costa Rica (Sibaja-Morales et al. 2009SIBAJA-MORALES, K. D., DE OLIVEIRA, J. B., JIMÉNEZ ROCHA, A. E., HERNÁNDEZ GAMBOA, J., PRENDAS GAMBOA, J., ARROYO MURILLO, F., SANDÍ, J., NUÑEZ, Y. & Baldi, M. 2009. Gastrointestinal parasites and ectoparasites of Bradypus variegatus and Choloepus hoffmanni sloths in captivity from Costa Rica. J. Zoo Wildl. Med. 40(1):86–90. ). The zoonotic potential of this mite must be considered due to the risk of transmission to the persons who rescued or are responsible for the care of the infested animal. Sarcoptic mange has a global distribution and is considered an emerging disease in some wildlife species (Escobar et al. 2022ESCOBAR, L. E., CARVER, S., CROSS, P. C., ROSSI, L., ALMBERG, E. S., YABSLEY, M. J., NIEDRINGHAUS, K. D., VAN WICK, P., DOMINGUEZ-VILLEGAS, E., GAKUYA, F., XIE, Y., ANGELONE, S., GORTÁZAR, C. & ASTORGA, F. 2022. Sarcoptic mange: An emerging panzootic in wildlife. Transbound. Emerg. Dis. 2022;69(3):927–942. ), as observed in the current study. Among the ticks, the Amblyomma varium presents high host specificity and is frequently verified in the Choloepus and Bradypus genera (Marques et al. 2002MARQUES. S., BARROS-BATTESTI, D.M., FACCINI, J.L. & ONOFRIO, V.C. 2002. Brazilian distribution of Amblyomma varium Koch, 1844 (Acari: Ixodidae), a common parasite of sloths (Mammalia: Xenarthra). Mem. Inst. Oswaldo Cruz 97(8):1141–1146.). Ticks, lice, and algae are observed in sloths under natural conditions but must be treated in captivity animals if a host-parasite imbalance occurs.

The musculoskeletal system of sloths presents disparities in functional adaptations, and variation may occur eventually in individuals within the same species (Mendel 1985MENDEL, F.C. 1985. Use of hands and feet of three-toed sloths (Bradypus variegatus) during climbing and terrestrial locomotion. J. Mammal. 66(2):359–366., Miranda 2014MIRANDA, F. 2014. Cingulata (tatus) e Pilosa (preguiças e tamanduás). In Tratado de animais selvagens (Z.S. Cubas, J.C.R. Silva & J.L. CATÃO-DIAS, eds). São Paulo, Roca, p.707–722., Dünner & Pastor 2017DÜNNER C, PASTOR G. 2017. Manual de Manejo, Medicina y Rehabilitación de Perezosos. Fundación Huálamo, Chile.). The activity pattern and movement rates also differ between sloths, since Cholloepus ones are nocturnal with a cyclic activity pattern, and Bradypus decrease activity before and after sunrise (Sunquist & Montgomery 1973SUNQUIST, M.E. & MONTGOMERY, G.G. 1973. Activity patterns and rates of movement of two-toed and three-toed sloths (Choloepus hoffmanni and Bradypus infuscatus). J. Mammal. 54(4):946–954.). Therefore, injuries may have different impacts between species and individuals, as verified in the current study, since the musculoskeletal system had the second-highest percentage of lesions in the sloths of the genus Choloepus and the third in the genus Bradypus.

Sloth genera differ in ecological behavior, which may have influenced the differences in lesion percentages, especially in the integumentary, musculoskeletal, and respiratory systems. While sloths of the Bradypus genus move less often, staying for a prolonged period in a tree and with both daytime and nighttime activity in less frequency, sloths of the Choloepus genus present strictly nocturnal activities spending little time at a single location (Sunquist & Montgomery 1973SUNQUIST, M.E. & MONTGOMERY, G.G. 1973. Activity patterns and rates of movement of two-toed and three-toed sloths (Choloepus hoffmanni and Bradypus infuscatus). J. Mammal. 54(4):946–954., Chiarello 2008CHIARELLO, A.G. 2008. Sloth ecology: an overview of field studies. In Biology of the Xenarthra (S.F. VIZCAÍNO & W.J. LOUGHRY, eds) The. University Press of Florida, Gainesville, USA, p.269–280.). In addition, a study showed that activity patterns in Bradypus variegatus are influenced by environmental temperature, besides nutritional requirements and protection against predators (Chiarello 1998CHIARELLO, A.G. (1998). Activity budgets and ranging patterns of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J. Zool. 246(1):1–10. , Castro-Sá et al. 2021CASTRO-SÁ, M.J., DIAS-SILVA, R.H.P. & BARNETT, A.A. 2021. Cathemeral activity by brown-throated three-toed sloths (Bradypus variegatus) in central Amazonian flooded igapó forests. Can. J. Zool. 99:832–838. , Lopes et al. 2023LOPES, G.S., CASSANO, C.R., MUREB, L.S., MIRANDA, F.R., CRUZ-NETO, A.P., & GINÉ, G.A.F. 2023. Combined effect of ambient temperature and solar radiation on maned sloths’ behaviour and detectability. Austral Ecol. 1–17. ). These differences influenced the high percentage of electrocution and being hit by a car for Choloepus, resulting in fractures, injuries, lacerations, and burns. Therefore, the activity pattern of these species, associated with the high rates of destruction and fragmentation of the habitat, may be considered the main consequence of the large number of traumatic conditions distributed throughout the neighborhoods, as verified in the spatial analysis. There were significantly more abundant rescue points in forested areas, where anthropization levels are considered high (De Andrade et al. 2020ANDRADE, A.C., MEDEIROS, S. & CHIARELLO, A.G. 2020. City sloths and marmosets in Atlantic forest fragments with contrasting levels of anthropogenic disturbance. Mammal Res. 65(3):481–491.).

Electrocution, for example, is a common problem for several arboreal mammals due to urban expansion, causing injuries of different degrees and complexity (Dünner & Pastor 2017DÜNNER C, PASTOR G. 2017. Manual de Manejo, Medicina y Rehabilitación de Perezosos. Fundación Huálamo, Chile., Carmo et al. 2019CARMO, C.C., MIRANDA, J.M.S., CAVALCANTE, M.J.S., BATISTA JÚNIOR, F.A., SIVA, A.L., RIBEIRO, A.S.S. 2019. Electrocution in common sloth (Bradypus variegatus). Cienc. Animal 29:27–33., Almeida et al. 2022ALMEIDA, D.V.C., LOPES, C.T. A., MATOS, P.C.M., PEREIRA JÚNIOR, J.J., IMBELONI, A.A. & DOMINGUES, S.F.S. (2022). Electrocution in a sloth (Choloepus didactylus) - clinical and surgical approach. Acta Sci. Vet., 50(Suppl 1):830.). In this context, the modified ecological matrix (roads, constructions, invasions in neighborhoods, industries, electrical wiring) can account for the high number of traumatic conditions related to the behavior of species in search of new areas to establish territory and use for foraging. The evaluation area of the present study has been subjected to different types of anthropic pressure due to exacerbated urban growth of the city and population growth with a percentage increase of 25.5% in a decade. Manaus, the state capital of Amazonas, has experienced significant population growth in recent years (IBGE, 2023IBGE. População estimada. Instituto Brasileiro de Geografia e Estatística. Instituto Brasileiro de Geografia e Estatística. https://cidades.ibge.gov.br/brasil/am/manaus/panorama. Accessed 12 Sept 2023
https://cidades.ibge.gov.br/brasil/am/ma...
), a fact that has resulted in areas of destroyed or fragmented forests. Faced with such challenges, public bodies must seek solutions through public policies that guarantee the sustainable development of the city, including by actions that conserve the environment and species of the Amazon region. The houses present lands adjacent to forest fragments that generate direct and indirect human - domestic animal - wildlife interactions (Gontijo 2008GONTIJO, J.C.F. 2008. Uso e características dos fragmentos florestais urbanos da cidade de Manaus/AM. Dissertação, Universidade Federal do Amazonas, Manaus., Santos et al. 2017SANTOS, L.S., PEREIRA, H. & GORDO, M. 2017. Interações entre população humana e saium-de-coleira (Saguinus bicolor) em fragmentos florestais urbanos de Manaus, Amazonas - Brasil. In Olhares cruzados sobre as relações entre seres humanos e animais silvestres na Amazônia (Brasil, Guiana Francesa) (G. Marchand & F.V. Velden, eds). EDUA, Manaus, p.85–102.). Consequently, the populations of free-living sloths (Choloepus didactylus, Bradypus tridactylus, B. variegatus) that inhabit green areas, anthropic forest fragments, and permanently protected areas in Manaus presented lacerations or injuries from attacks/bites by dogs when descending to the soil or when trying to connect to another forest fragment through the resident backyards. A study around a cacao farm in Costa Rica detected that most mortality of the adult sloths of the genera Bradypus and Choloepus was associated with predation by coyotes and domestic dogs and suggested that B. variegatus require immigration to maintain a stable population (Peery & Pauli 2014PEERY, M.Z., PAULI, J.N. 2014. Shade-grown cacao supports a self-sustaining population of two-toed but not three-toed sloths. J. Appl. Ecol. 51:162–170.).

Since the present study did not consider specific variables for spatial epidemiological analysis, further studies must be conducted to correlate clinical lesions with negative interactions that threaten sloth survival and to promote conservation strategies. The urban matrix directly influences threats to arboreal mammals, such as sloths and primates (Gordo et al. 2013GORDO, M., CALLEIA, F.O., VASCONCELOS, S.A., LEITE, J.F., FERRARI, S. 2013. The challenges of survival in a concrete jungle: conservation of the pied tamarin (Saguinus bicolor) in the urban landscape of Manaus, Brazil. In: L.K. MARSH, C.A. CHAPMAN, eds) Primates in Fragments: Complexity and Reslience. New York, Springer, p.357–370., Katsis et al. 2018KATSIS, L., CUNNEYWORTH, P.M.K., TURNER, K.M.E., & PRESOTTO, A. 2018. Spatial patterns of primate electrocutions in Diani, Kenya. Int. J. Primatol. 39(4):493–510., Brandão et al. 2019BRANDÃO, M.L., FURTADO, M.C., ALBUQUERQUE, D.D., CORDEIRO, J.L.P., LOURENÇO, M.C.S., FIGUEIREDO, F.B. 2019. Management of wild sloths in an anthropized area at Atlantic forest. Oecol. Australis 23(3):644–651. , Carmo et al. 2019CARMO, C.C., MIRANDA, J.M.S., CAVALCANTE, M.J.S., BATISTA JÚNIOR, F.A., SIVA, A.L., RIBEIRO, A.S.S. 2019. Electrocution in common sloth (Bradypus variegatus). Cienc. Animal 29:27–33.), vulnerable to urbanization because of the high dependence on trees for displacement.

The lesions verified in the respiratory and digestive systems probably were influenced by the time in captivity. Stressed animals can develop enteric and respiratory disturbances (Messias-Costa & Esbérard 2001MESSIAS-COSTA, A. & ESBÉRARD, C. 2001. Husbandry. In Biology, Medicine, and Surgery of South American Wild Animals (M.E. Fowler & Z.S. Cubas, eds). Iowa State Press, Iowa, USA, p.246–247.). Bronchopneumonia and pneumonia were the most frequent respiratory diseases in the present study. Severe climate changes were associated with developing pneumonia among sloths living in captivity at one São Paulo zoo (Diniz & Oliveira 1999DINIZ, L.S., OLIVEIRA, P.M. 1999. Clinical problems of sloths (Bradypus sp. and Choloepus sp.) in captivity. J. Zoo Wildl. Med. 30:76–80.). Bronchopneumonia and acute edema of the lungs was also the major causes of death in sloths received at a zoo in Belém, Amazonia (Messias-Costa 2001MESSIAS-COSTA, A. 2001. Medicine and neonatal care of sloths. In Biology, Medicine, and Surgery of South American Wild Animals (M.E. Fowler & Z.S. Cubas, eds). Iowa State Press, Iowa, USA, p.247–249.). The sloths have poor thermoregulatory ability and are sensitive to temperature changes (Gilmore et al. 2000), which must be considered in captivity animals.

Parasitism, bloat, and malabsorption syndrome were some of the digestive alterations detected in the present study. Coccidia and Giardia were the intestinal protozoan parasites identified. Free-living sloths may have coccidian infection without disease manifestation (Messias-Costa 2001MESSIAS-COSTA, A. 2001. Medicine and neonatal care of sloths. In Biology, Medicine, and Surgery of South American Wild Animals (M.E. Fowler & Z.S. Cubas, eds). Iowa State Press, Iowa, USA, p.247–249.). Giardia duodenalis has already been diagnosed in baby sloths rescued in Manaus and must be considered part of the zoonotic scenario in the region (Reis et al. 2023REIS, L.L., SOUZA, L.S.S., BRAGA, F.C.O., LIMA, D.C.S, PADINHA, J.S., NAVA, A.F.D., VICENTE, A.C.P. 2023. Zoonotic Giardia duodenalis Assemblage A in Northern Sloth from Brazilian Amazon. Research Square. https://doi.org/10.21203/rs.3.rs-2883298/v1
https://doi.org/10.21203/rs.3.rs-2883298...
). Traumas and gastric impaction occurred in cases of bloat in the present study, evidencing that veterinary complications and the maintenance of a standardized and adequate nutritional protocol for the pup in captivity are crucial for its maintenance. (Gage 2002GAGE, L. 2002. Hand-rearing wild and domestic animals. Iowa State University Press, Iowa. p.279., Larrazábal 2004LARRAZÁBAL, L.B. 2004. Crianza en cautiverio de perezoso de dos dedos (Choloepus didactylus). Edentata 6:30–36. , Dünner & Pastor 2017DÜNNER C, PASTOR G. 2017. Manual de Manejo, Medicina y Rehabilitación de Perezosos. Fundación Huálamo, Chile.). Tympanism and constipation are common in sloths and related to stress factors (Messias-Costa 2001MESSIAS-COSTA, A. 2001. Medicine and neonatal care of sloths. In Biology, Medicine, and Surgery of South American Wild Animals (M.E. Fowler & Z.S. Cubas, eds). Iowa State Press, Iowa, USA, p.247–249.). A study of young Choloepus didactylus in captivity reported tympanism as the most frequent alteration, which was attributed to the food and position feeding position (Larrazábal 2004LARRAZÁBAL, L.B. 2004. Crianza en cautiverio de perezoso de dos dedos (Choloepus didactylus). Edentata 6:30–36. ). In addition, tympanism has been observed in politraumatized free-ranging sloths (Dünner & Pastor 2017DÜNNER C, PASTOR G. 2017. Manual de Manejo, Medicina y Rehabilitación de Perezosos. Fundación Huálamo, Chile.), as verified in animals with bloat in the present study.

It should be mentioned that the respiratory and digestive conditions in the current study were mainly associated with young sloths of the genus Bradypus removed from their natural environment, often resulting in death. Common problems reported in young and newly arrived captive animals include milk maladaptation (diarrhea), bloat, and fecaloma, as well as malabsorption syndrome that causes poor body condition and peeling of the skin and nails (Messias-Costa 2001MESSIAS-COSTA, A. 2001. Medicine and neonatal care of sloths. In Biology, Medicine, and Surgery of South American Wild Animals (M.E. Fowler & Z.S. Cubas, eds). Iowa State Press, Iowa, USA, p.247–249., Dünner & Pastor 2017DÜNNER C, PASTOR G. 2017. Manual de Manejo, Medicina y Rehabilitación de Perezosos. Fundación Huálamo, Chile.). Furthermore, the lesions related to the visual, auditory, circulatory and genitourinary systems were considered isolated and punctual cases.

In conclusion, the most common conditions in body systems of free-ranging sloths from Manaus included the musculoskeletal, integumentary, and respiratory systems; however, there were differences between genera. These results can provide data for future investigations about clinical diseases in sloths and their respective causes, to support adequate management measures that contribute to the health and conservation of these mammals.

Acknowledgments

We are grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); Universidade Estadual Paulista “Júlio de Mesquita Filho (UNESP), Programa de pós-graduação em Animais Selvagens; Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA)-Centro de Triagem de Animais Selvagens (CETAS/AMAZONAS).

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on a reasonable request.

All data supporting the results in papers published in the journal must be archived in an appropriate public archive offering open access and guaranteed preservation (http://hdl.handle.net/11449/236499).

The datasets generated during and/or analyzed during the current study are available at: https://doi.org/10.48331/scielodata.7YO9P7.

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Edited by

Associate Editor

Diego Astúa

Publication Dates

  • Publication in this collection
    15 Dec 2023
  • Date of issue
    2023

History

  • Received
    15 Mar 2023
  • Accepted
    18 Oct 2023
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