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Gastrointestinal parasites in marsupials from Atlantic Forest of Northeastern Brazil

[Parasitos gastrointestinais em marsupiais da Mata Atlântica do nordeste do Brasil]

RESUMO

Os marsupiais estão envolvidos no ciclo de vida de vários patógenos de interesse médico e veterinário. O objetivo deste estudo foi relatar a ocorrência de parasitos gastrointestinais em marsupiais capturados em fragmentos da Mata Atlântica, estado de Sergipe, nordeste do Brasil. De junho de 2017 a janeiro de 2018, marsupiais foram capturados usando-se armadilhas, e foram obtidas amostras fecais frescas após defecação espontânea. Os animais foram identificados morfometricamente e as fezes analisadas pela técnica FLOTAC. Foram capturados 88 animais, sendo 37 Marmosops incanus, 30 Marmosa demerarae, 20 Didelphis albiventris e 01 Marmosa murina. A espécie mais parasitada foi D. albiventris (45,95%) seguida de M. incanus (43,24%) e M. demerarae (23,3%). No geral, ovos de helmintos foram detectados em 47,72% (42/88) das amostras, enquanto oocistos de protozoários em 32,95% (29/88). Ovos de Ancylostoma sp. predominaram sobre outros parasitos. Este estudo aponta para a ocorrência de parasitos gastrointestinais e contribui para um melhor entendimento do parasitismo em marsupiais que vivem em fragmentos florestais da Mata Atlântica.

Palavras-chave:
diagnóstico parasitológico; mamíferos; FLOTAC; endoparasitos

Keywords:
parasitological diagnosis; mammals; FLOTAC; endoparasites

Palavras-chave:
diagnóstico parasitológico; mamíferos; FLOTAC; endoparasitos

Marsupials have been recognized as animals of great ecological and sanitary relevance due to their role as disseminators of seeds and the involvement in the life cycle of several pathogens of zoonotic concern (Bezerra-Santos et al., 2021). Over the last decades, the contact between these animals and humans has been intensified because of the loss of natural habitat, which may imply in a negative impact for both animal and human species (Cooper et al., 2018COOPER, C.; KEATLEY, S.; NORTHOVER, A. et al. Next generation sequencing reveals widespread trypanosome diversity and polyparasitism in marsupials from Western Australia. Int. J. Parasitol. Parasites Wildl., v.7, p.58-67, 2018.). Currently, Brazil encompasses a high diversity of marsupials with at least 62 recognized species (Faria et al., 2019FARIA, M.B.; LANES, R.O.; BONVICINO, C.R. Marsupiais do Brasil: guia de identificação com base em caracteres morfológicos externos e cranianos. São Caetano do Sul: Amélie, 2019. 81p.), being many of them directly affected by anthropic actions.

The synanthropic behavior presented by some marsupial species (e.g., Didelphis spp.) may facilitate the sharing of pathogens with domestic species (Roque et al., 2013ROQUE, A.L.; XAVIER, S.C.; GERHARDT, M. et al. Trypanosoma cruzi among wild and domestic mammals in different areas of the Abaetetuba municipality (Pará State, Brazil), an endemic Chagas disease transmission area. Vet. Parasitol., v.193, p.71-77, 2013.). For instance, the black-eared opossum (D. aurita) captured in an urban area of Southeastern Brazil presented a high prevalence of Ancylostoma caninum (Bezerra-Santos et al., 2020), a common species to domestic dogs. Additionally, to helminths, gastrointestinal (Eimeria spp.) and blood (Trypanosoma cruzi and Leishmania sp.) protozoa are also reported, demonstrating that they can harbor a wide plethora of parasites of medical and veterinary concern (Teodoro et al., 2019TEODORO, A.K.M.; CUTOLO, A.A.; MOTOIE, G. et al. Gastrointestinal, skin and blood parasites in Didelphis spp. from urban and sylvatic areas in São Paulo state, Brazil. Vet. Parasitol. Reg. Stud. Rep., v.16, n.100286, 2019.).

Marsupials can thrive in different environments, benefiting from the resources (food and shelter) available in human-modified areas (Roque et al., 2013ROQUE, A.L.; XAVIER, S.C.; GERHARDT, M. et al. Trypanosoma cruzi among wild and domestic mammals in different areas of the Abaetetuba municipality (Pará State, Brazil), an endemic Chagas disease transmission area. Vet. Parasitol., v.193, p.71-77, 2013.). The access of these animals to food available in the peri-urban areas is pivotal to their infection with zoonotic pathogens (Aragón-Pech et al., 2018). This synanthropic behavior is typical for species of generalist habitat; who have presented a good adaptation to situations of loss of natural habitat and fragmentation. Undoubtedly, this behavior acquired by some species is a consequence of anthropic actions, such as demographic pressures, agricultural exploitation, and disorderly occupation of the territory (Pinto et al., 2006PINTO, L.P.; BEDÊ, L.; PAESE, A. et al. Mata Atlântica brasileira: os desafios para conservação da biodiversidade de um hotspot mundial. In: ROCHA, C.F.D.; BERGALHO, H.G.; ALVES, M.A.A. (Eds.). Biologia da conservação: essências. São Carlos: RiMa, 2006. p.91-118.).

Currently, the Atlantic Forest, an important natural habitat of several marsupial species, is restricted to only about 12.4% of its original area, and the area remains predominantly distributed in small forest fragments (SOS Mata Atlântica, 2021). Most of the remnants of the Atlantic Forest are very small and inserted in an anthropic matrix (Ribeiro et al., 2009RIBEIRO, M.C.; METZGER, J.P.; MARTENSEN, A.C. et al. The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv., v.142, p.1141-1153, 2009.). This scenario changes the natural structure of arboreal mammal populations, favoring the emergence of small and isolated populations that are more susceptible to parasitic infections (Fahrig, 2003FAHRIG, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst., v.34, p.487-515, 2003.). Therefore, the aim of this study was to report the occurrence of gastrointestinal parasites of marsupials captured in fragments of the Atlantic Forest in Northeastern Brazil.

The study was conducted in two remnants of the Atlantic Forest located in the state of Sergipe, Northeastern Brazil, the forest fragment of the Federal University of Sergipe - UFS - Campus, and the legal forest reserve of Santana farm - SF. The forest fragment of the UFS is in the São Cristóvão Campus (10º55’S, 37º04’W), peri-urban parkland surrounded by a 30ha forest remnant (Rocha et al., 2011ROCHA, M.F.; PASSAMANI, M.; LOUZADA, J. A small mammal community in a forest fragment, vegetation corridor and coffee matrix system in the Brazilian Atlantic forest. PLoS One, v.6, p.e23312, 2011.). The legal forest reserve of SF (600ha; 10°32'07"S, 36°45'54"W) is a sugarcane plant located between the municipalities of Japoatã and Pacatuba (Pedroso et al., 2020PEDROSO, M.A.; PEREIRA, A.S.; OLIVEIRA, H.S. et al. Rapid survey of bats (Chiroptera) in the Atlantic Forest in eastern Sergipe, Brazil: unexpected diversity in a fragmented landscape. Neotrop. Biol. Conserv., v.15, p.317-331, 2020.). A predominant seasonal semi-deciduous vegetation features these areas, with annual temperature mean ranging from 24 to 30°C, and tropical climate (As) according to the Köppen’s climate classification (Alvares et al., 2013ALVARES, C.A.; STAPE, J.L.; SENTELHAS, P.C. Köppen’s climate classification map for Brazil. Meteorol. Z., v.22, p. 711-728, 2013.).

From June 2017 to January 2018 marsupials were captured using live traps (Tomahawk 40cm x 12cm x 12cm; Zootech®), which were armed on the ground along six transects of 15 points and checked daily, totaling a sampling effort of 90 trap-nights. The traps were baited with a mixture of corn meal, sardine, peanut butter, banana, oatmeal, bacon, and vanilla essence to attract species with different types of diet (Astúa et al., 2006ASTÚA, D.; MOURA, R.T.; GRELLE, C.E.V.; FONSECA, M.T. Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Bol. Mus. Biol. Mello Leitão, v.19, p.31-44, 2006.). The animals were marked with numbered aluminum earrings (“Ear Tags”) and released at the same point of capture. Fresh fecal samples were obtained after spontaneous defecation. All material was kept in isothermal boxes at 4°C until laboratory processing.

The captured animals were identified by external morphometry according to Faria et al. (2019FARIA, M.B.; LANES, R.O.; BONVICINO, C.R. Marsupiais do Brasil: guia de identificação com base em caracteres morfológicos externos e cranianos. São Caetano do Sul: Amélie, 2019. 81p.). All animals were handled according to the American Society of Mammalogists (Sikes and Gannon, 2011SIKES, R.S.; GANNON, W.L. The Animal care and use Committee of the American Society of Mammalogists. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal., v.92, p.235-253, 2011.). The research was authorized by the ICMBio permit (SISBio 11283-2).

Fecal samples were processed individually and analyzed through FLOTAC technique (Cringoli et al., 2010CRINGOLI, G.; RINALDI, L.; MAURELLI, M.P.; UTZINGER, J. FLOTAC: new multivalente techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat. Protoc., v.5, p.503-515, 2010.). The FLOTAC was performed with two flotation solutions (sodium chloride, specific gravity, s.g. = 1.200 and zinc sulfate, s.g. = 1.350). All parasitic stages observed were morphologically identified based on previous taxonomic keys (Taylor et al., 2017TAYLOR, M.A.; COOP, R.L.; WALL, R.L. Parasitologia veterinária. Rio de Janeiro: Guanabara Koogan, 2017. 1052p.).

Initially, relative and absolute frequencies were calculated through descriptive statistics. Subsequently, the Lilliefors test was used to verify the normality of the data. The Chi-square (χ2) test was used to compare the overall positivity for different marsupial species. Additionally, the Kruskal-Wallis test was used to compare different helminths/protozoa (genus/family) according to each marsupial species. For all tests, a significance level of 5% was considered, and the BioEstat software version 5.3 was used (Ayres et al., 2007AYRES, M.; AYRES JÚNIOR, M.; AYRES, D.L.; SANTOS, A.D.A. Aplicações estatísticas nas áreas das ciências bio-médicas. Belém: Instituto Mamirauá, 2007. 381p.).

A total of 88 animals (37 Marmosops incanus, 30 Marmosa demerarae, 20 Didelphis albiventris, and 01 Marmosa murina) were captured. The most parasitized species was D. albiventris (45.95%) followed by M. incanus (43.24%) and M. demerarae (23.3%), without significant difference (χ2 = 3.579; p = 0.1671). M. murina was not parasitized.

Overall, eggs of helminths were detected in 47.72% (42/88) of samples, whereas oocysts of protozoa in 32.95% (29/88). In particular 12 different types of parasites were diagnosed, but those of the Family Ancylostomatidae predominated over the others (Table 1).

Interestingly, M. incanus and M. demerarae hosted six different gastrointestinal parasites (H = 14.4282; p = 0.0007). Although frequent, Ancylostoma sp. eggs did not differ statistically from other helminths (H= 5.9910; p = 0.1120). It is important to highlight that D. albiventris was the most parasitized species, hosting 83.33% (10/12) of the gastrointestinal parasites herein diagnosed, with predominance of Ascaris sp. eggs (H = 6.6093; p = 0.3585). Coccidea predominated over Giardia sp. and Entamoeba sp. (H = 14.7016; p = 0.0006). The detailed information about co-infections is summarized in Table 2.

This study reports the parasitism by different gastrointestinal parasites in marsupials captured from the Atlantic Forest of Northeastern Brazil. Although only half of the animals were parasitized, those positive samples represent three species of wild mammals captured. This finding demonstrates the susceptibility of several species of marsupials to gastrointestinal parasites, which may be related also to the generalist feeding behavior presented by these animals (Jiménez et al., 2011JIMÉNEZ, F.A.; CATZEFLIS, F.; GARDNER, S.L. Structure of parasite component communities of didelphid marsupials: insights from a comparative study. J. Parasitol., v.97, p.779-787, 2011.). It is known that the diet changes according to the environment where they are inserted, so it is possible to have availability of food from wild, rural, and urban environments (Bezerra-Santos et al., 2021). It is important to note that D. albiventris was the species more parasitized. This animal has been considered a generalist mammal with high prolificity and adaptability to the anthropic environments. Therefore, its interaction with other synanthropic animals, domestic animals and humans may contribute for the sharing of pathogens among all species involved (Janes et al., 2017JANES, C.R.; CORBETT, K.K.; JONES, J.H.; TROSTLE, J. Emerging infectious diseases: the role of social sciences. Lancet, v.380, p.1884-1886, 2017.).

Table 1
Absolute and relative frequencies for each gastrointestinal parasite found in marsupials

Table 2
Frequency of gastrointestinal co-infections

Eggs belonging to Ancylostoma sp. were those more frequently detected in this study. This retrieval has been a common finding in these animals, especially in D. albiventris where a positivity of up to 100% has been observed (Teodoro et al., 2019TEODORO, A.K.M.; CUTOLO, A.A.; MOTOIE, G. et al. Gastrointestinal, skin and blood parasites in Didelphis spp. from urban and sylvatic areas in São Paulo state, Brazil. Vet. Parasitol. Reg. Stud. Rep., v.16, n.100286, 2019.). Unfortunately, in this study the identification at level species of parasites was not achieved. However, recently the retrieval of A. caninum in D. albiventris sounded as an alert, indicating the strict sharing of this nematode species between wild and domestic animals (Bezerra-Santos et al., 2020).

Co-infections with other gastrointestinal parasites were a common finding. This is a consequence of the lifestyle of these animals, as well as the availability of food in some areas that exposes them to different species (Jimenez et al., 2011JIMÉNEZ, F.A.; CATZEFLIS, F.; GARDNER, S.L. Structure of parasite component communities of didelphid marsupials: insights from a comparative study. J. Parasitol., v.97, p.779-787, 2011.). Some of the parasites detected here may be related to zoonotic infections (e.g., Giardia and Entamoeba), raising concern about the spill-over of pathogens from humans and domestic animals into wildlife (Vermeulen et al., 2015VERMEULEN, E.T.; ASHWORTH, D.L.; ELDRIDGE, M.D.; POWER, M.L. Investigation into potential transmission sources of Giardia duodenalis in a threatened marsupial (Petrogale penicillata). Infect. Genet. Evol., v.33, p.277-280, 2015.). Among all marsupial species assessed, the role of D. albiventris as synanthropic species is notable, for this reason these animals have been extensively studied over the last years (Bezerra-Santos et al., 2021).

Overall, this study brings important data about the gastrointestinal fauna of marsupials demonstrating the wide variety of parasites in which these animals are exposed. It is important to adopt measures of conservation of natural habitat of these animals to avoid its interaction with domestic animals and human species. Although, at the moment of the sampling no animal presented clinical signs suggestive of the infection by gastrointestinal parasites, the impact of this kind of parasitism needs to be better assessed to clarify its role in the conservation of these marsupials’ species.

ACKNOWLEDGEMENTS

The authors would like to thank Tatiene Rossana Mota Silva (Federal University of the Agreste of Pernambuco) for her aid on data analyses.

REFERENCES

  • ALVARES, C.A.; STAPE, J.L.; SENTELHAS, P.C. Köppen’s climate classification map for Brazil. Meteorol. Z., v.22, p. 711-728, 2013.
  • ARAGÓN-PECH, R.A.; RUIZ-PIÑA, H.A.; RODRÍGUEZ-VIVAS, R.I. et al. Prevalence, abundance and intensity of eggs and oocysts of gastrointestinal parasites in the opossum Didelphis virginiana Kerr, 1792 in Yucatan, Mexico. Helminthologia, v.55, p.119-126, 2018.
  • ASTÚA, D.; MOURA, R.T.; GRELLE, C.E.V.; FONSECA, M.T. Influence of baits, trap type and position for small mammal capture in a Brazilian lowland Atlantic Forest. Bol. Mus. Biol. Mello Leitão, v.19, p.31-44, 2006.
  • AYRES, M.; AYRES JÚNIOR, M.; AYRES, D.L.; SANTOS, A.D.A. Aplicações estatísticas nas áreas das ciências bio-médicas. Belém: Instituto Mamirauá, 2007. 381p.
  • BEZERRA-SANTOS, M.A.; FONTES, C.S.; NOGUEIRA, B.C.F. et al. Gastrointestinal parasites in the opossum Didelphis aurita: are they a potential threat to human health? J. Parasit. Dis., v.44, p.355-363, 2020.
  • BEZERRA-SANTOS, M.A.; RAMOS, R.A.N.; CAMPOS, A.K. et al. Didelphis spp. opossums and their parasites in the Americas: a one health perspective. Parasitol. Res., v.120, p.4091-4111, 2021.
  • COOPER, C.; KEATLEY, S.; NORTHOVER, A. et al. Next generation sequencing reveals widespread trypanosome diversity and polyparasitism in marsupials from Western Australia. Int. J. Parasitol. Parasites Wildl., v.7, p.58-67, 2018.
  • CRINGOLI, G.; RINALDI, L.; MAURELLI, M.P.; UTZINGER, J. FLOTAC: new multivalente techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat. Protoc., v.5, p.503-515, 2010.
  • FAHRIG, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst., v.34, p.487-515, 2003.
  • FARIA, M.B.; LANES, R.O.; BONVICINO, C.R. Marsupiais do Brasil: guia de identificação com base em caracteres morfológicos externos e cranianos. São Caetano do Sul: Amélie, 2019. 81p.
  • JANES, C.R.; CORBETT, K.K.; JONES, J.H.; TROSTLE, J. Emerging infectious diseases: the role of social sciences. Lancet, v.380, p.1884-1886, 2017.
  • JIMÉNEZ, F.A.; CATZEFLIS, F.; GARDNER, S.L. Structure of parasite component communities of didelphid marsupials: insights from a comparative study. J. Parasitol., v.97, p.779-787, 2011.
  • PEDROSO, M.A.; PEREIRA, A.S.; OLIVEIRA, H.S. et al. Rapid survey of bats (Chiroptera) in the Atlantic Forest in eastern Sergipe, Brazil: unexpected diversity in a fragmented landscape. Neotrop. Biol. Conserv., v.15, p.317-331, 2020.
  • PINTO, L.P.; BEDÊ, L.; PAESE, A. et al. Mata Atlântica brasileira: os desafios para conservação da biodiversidade de um hotspot mundial. In: ROCHA, C.F.D.; BERGALHO, H.G.; ALVES, M.A.A. (Eds.). Biologia da conservação: essências. São Carlos: RiMa, 2006. p.91-118.
  • RIBEIRO, M.C.; METZGER, J.P.; MARTENSEN, A.C. et al. The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv., v.142, p.1141-1153, 2009.
  • ROCHA, M.F.; PASSAMANI, M.; LOUZADA, J. A small mammal community in a forest fragment, vegetation corridor and coffee matrix system in the Brazilian Atlantic forest. PLoS One, v.6, p.e23312, 2011.
  • ROQUE, A.L.; XAVIER, S.C.; GERHARDT, M. et al. Trypanosoma cruzi among wild and domestic mammals in different areas of the Abaetetuba municipality (Pará State, Brazil), an endemic Chagas disease transmission area. Vet. Parasitol., v.193, p.71-77, 2013.
  • SIKES, R.S.; GANNON, W.L. The Animal care and use Committee of the American Society of Mammalogists. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal., v.92, p.235-253, 2011.
  • SOS Mata Atlântica. Atlas dos remanescentes florestais da Mata Atlântica. Período 2019 - 2010 / Relatório Técnico. São Paulo: Fundação SOS Mata Atlântica / Instituto Nacional de Pesquisas Espaciais, 2021. 38p.
  • TAYLOR, M.A.; COOP, R.L.; WALL, R.L. Parasitologia veterinária. Rio de Janeiro: Guanabara Koogan, 2017. 1052p.
  • TEODORO, A.K.M.; CUTOLO, A.A.; MOTOIE, G. et al. Gastrointestinal, skin and blood parasites in Didelphis spp. from urban and sylvatic areas in São Paulo state, Brazil. Vet. Parasitol. Reg. Stud. Rep., v.16, n.100286, 2019.
  • VERMEULEN, E.T.; ASHWORTH, D.L.; ELDRIDGE, M.D.; POWER, M.L. Investigation into potential transmission sources of Giardia duodenalis in a threatened marsupial (Petrogale penicillata). Infect. Genet. Evol., v.33, p.277-280, 2015.

Publication Dates

  • Publication in this collection
    19 Aug 2022
  • Date of issue
    Jul-Aug 2022

History

  • Received
    18 Oct 2021
  • Accepted
    13 May 2022
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