Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-06-07T14:05:30.394Z Has data issue: false hasContentIssue false
  • English
  • Français

Gleasonian structure in the helminth metacommunity of the opossum Didelphis albiventris in two extremes of the Atlantic Forest

Published online by Cambridge University Press:  28 January 2022

B.S. Cirino Open the ORCID record for B.S. Cirino [Opens in a new window] ,
S.F. Costa-Neto Open the ORCID record for S.F. Costa-Neto [Opens in a new window] ,
T.S. Cardoso Open the ORCID record for T.S. Cardoso [Opens in a new window] ,
P.C. Estrela Open the ORCID record for P.C. Estrela [Opens in a new window] ,
A. Maldonado Jr Open the ORCID record for A. Maldonado Jr [Opens in a new window]  and
R. Gentile Open the ORCID record for R. Gentile [Opens in a new window]
B.S. Cirino*
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, 21040-360, Rio de Janeiro, RJ, Brazil Programa de Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil, 4365, 21040-360, Rio de Janeiro, RJ, Brazil
S.F. Costa-Neto
Affiliation:
Programa de Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil, 4365, 21040-360, Rio de Janeiro, RJ, Brazil Campus Fiocruz Mata Atlântica, Fundação Oswaldo Cruz, Rio de Janeiro, RJ, Brazil
T.S. Cardoso
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, 21040-360, Rio de Janeiro, RJ, Brazil Programa Fiocruz de Fomento à Inovação – INOVA FIOCRUZ, Fundação Oswaldo Cruz, Av. Brasil 4365, 21045-900, Rio de Janeiro, RJ, Brazil
P.C. Estrela
Affiliation:
Laboratório de Mamíferos, Coleção de Mamíferos da UFPB, Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, Jardim Universitário s/n, Castelo Branco, 58051-900, João Pessoa, PB, Brazil
A. Maldonado Jr
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, 21040-360, Rio de Janeiro, RJ, Brazil
R. Gentile
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, 21040-360, Rio de Janeiro, RJ, Brazil
*
Author for correspondence: B.S. Cirino, E-mail: brunascirino@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Didelphis albiventris is the opossum with the largest geographic distribution in Brazil and has a wide spectrum of helminth parasites. This study aimed to describe the species composition and analyse the structure of helminth communities of D. albiventris in two extremes of the Atlantic Forest in Brazil. The influence of host sex, body mass, age, helminth species richness and locality on the abundance and prevalence of the most prevalent helminth species was investigated. Ninety-five per cent of the animals were infected with at least one species. Nine helminth species were found: the nematodes Aspidodera raillieti, Cruzia tentaculata, Trichuris didelphis and Trichuris minuta in the large intestine; Turgida turgida in the stomach; Travassostrongylus orloffi and Viannaia hamata; and the trematodes Brachylaima advena and Rhopalias coronatus in the small intestine. Three helminth morphospecies were also recovered: the nematodes Hoineffia sp. and Viannaia sp. and a cestode in the small intestine. Cruzia tentaculata and V. hamata were the species with the highest mean abundances and intensities, while the most prevalent species were A. raillieti, C. tentaculata, T. turgida and V. hamata, forming the central nucleus of the helminth component community. The analysis of the helminth metacommunity structure indicated a Gleasonian pattern for the total set of infracommunities, corroborating the beta diversity indices, which indicated more species replacement than loss between localities and infracommunities, although at a low level. The results indicated a stronger influence of host attributes than geographical distance on the community structure.

Keywords

EcologymarsupialsNematodaparasitesPlatyhelminthes
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e7
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amato, JFR, Walter, AB and Amato, SB (1991) Protocolo para laboratório: coleta e processamento de parasitas do pescado. 1st edn. p. 81. Rio de Janeiro, Imprensa Universitária UFRRJ.Google Scholar
Anderson, RC, Chaubaud, AG and Willmott, S (2009) Keys to the nematode parasites of vertebrates: archival volume. p. 336. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Ayoade, J (1986) Introdução a climatologia dos trópicos. p. 332. São Paulo, Difel.Google Scholar
Baselga, A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19, 134–143.CrossRefGoogle Scholar
Baselga, A (2017) Partitioning abundance-based multiple-site dissimilarity into components: balanced variation in abundance and abundance gradients. Methods in Ecology and Evolution 8, 799–808.CrossRefGoogle Scholar
Baselga, A, Orme, O, Villeger, S, Bortoli, J and Leprieur, F (2018) betapart: partitioning beta diversity into turnover and nestedness components. R package version 1.5.1. Available at https://CRAN.R-project.org/package=betapartGoogle Scholar
Bezerra-Santos, MA, Ramos, RAN, Campos, AK, Dantas-Torres, F and Otranto, D (2021) Didelphis spp. opossums and their parasites in the Americas: a one health perspective. Parasitology Research 120, 4091–4111.CrossRefGoogle ScholarPubMed
Boullosa, RG, Cardoso, TS, Costa-Neto, SF, Teixeira, BR, Freitas, TPT, Maldonado-Júnior, A and Gentile, R (2020) Helminth community structure of three sigmodontine rodents in the Atlantic Forest, southern Brazil. Oecologia Australis 24, 577–589.CrossRefGoogle Scholar
Braga, C, Oliveira, JA and Cerqueira, R (2017) Metacomunidades: uma introdução aos termos e conceitos. Oecologia Australis 21, 108–118.CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Cáceres, NC, de Moraes Weber, M, Melo, GL, et al. (2016) Which factors determine spatial segregation in the South American opossums (Didelphis aurita and D. albiventris)? An ecological niche modelling and geometric morphometrics approach. PLoS One 11, e0157723.CrossRefGoogle Scholar
Cantor, M, Ferreira, LA, Silva, WR and Setz, EZF (2010) Potential seed dispersal by Didelphis albiventris (Marsupialia, Didelphidae) in highly disturbed environment. Biota Neotropica 10, 45–51.CrossRefGoogle Scholar
Cardoso, TS, Macabu, CE, Simões, RO, Maldonado Júnior, A, Luque, JL and Gentile, R (2019) Helminth community structure of two sigmodontine rodents in Serra dos Órgãos National Park, state of Rio de Janeiro, Brazil. Oecologia Australis 23, 301–314.CrossRefGoogle Scholar
Castro, RGBM, Costa-Neto, SF, Maldonado Júnior, A and Gentile, R (2017) Ecological aspects of nematode parasites of Didelphis aurita (Didelphimorphia, Didelphidae) in urban-sylvatic habitats in Rio de Janeiro, Brazil. Oecologia Australis 21, 54–61.CrossRefGoogle Scholar
Cirino, BS, Costa-Neto, SF, Maldonado Júnior, A and Gentile, R (2020) First study on the helminth community structure of the neotropical marsupial Metachirus myosuros (Didelphimorphia, Didelphidae). Revista Brasileira de Parasitologia Veterinária 29, e005420.CrossRefGoogle Scholar
Combes, C (2001) Parasitism: the ecology and evolution of intimate interactions. 1st edn. p. 728. Chicago, University of Chicago Press.Google Scholar
Conservation International (2021) Biodiversity hotspots [online]. Arlington, Conservation International. Available at https://www.conservation.org/priorities/biodiversity-hotspots (accessed 13 February 2021).Google Scholar
Corrêa, SHR and Passos, EC (2008) Wild animals and public health. pp. 493–499 in Fowler, ME and Cubas, ZS (Eds) Biology, medicine, and surgery of South American wild animals. Ames, Iowa University Press.CrossRefGoogle Scholar
Costa-Neto, SF, Cardoso, TS, Boullosa, RG, Maldonado, A Jr. and Gentile, R (2019) Metacommunity structure of the helminths of the black-eared opossum Didelphis aurita in peri-urban. Sylvatic and rural environments in south-eastern Brazil. Journal of Helminthology 93, 720–731.CrossRefGoogle ScholarPubMed
Daszak, P, Cunningham, A and Hyatt, A (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287, 443–449.CrossRefGoogle ScholarPubMed
Figueiredo, M, Barros, C, Delciellos, AC, et al. (2017) Abundance of small mammals in the Atlantic Forest (ASMAF): a data set for analyzing tropical community patterns. Ecology 98, 2981–2981.CrossRefGoogle ScholarPubMed
Fornazari, F, Teixeira, CR, da Silva, RC, Leiva, M, de Almeida, SC and Langoni, H (2011) Prevalence of antibodies against toxoplasma gondii among Brazilian white-eared opossums (Didelphis albiventris). Veterinary Parasitology 179, 238–241.CrossRefGoogle Scholar
Fornazari, F, Langoni, H, Marson, PM, Nóbrega, DB and Teixeira, CR (2018) Leptospira reservoirs among wildlife in Brazil: Beyond rodents. Acta Tropica 178, 205–212.CrossRefGoogle ScholarPubMed
Francisco, PRM, Medeiros, RD, Santos, D and Matos, RD (2015) Classificação climática de Köppen e Thornthwaite para o estado da Paraíba. Revista Brasileira de Geografia Física 8, 1006–1016.CrossRefGoogle Scholar
Gentile, R, Cardoso, TS, Costa-Neto, SF, Teixeira, BR and D'Andrea, PS (2018) Community structure and population dynamics of small mammals in an urban-sylvatic interface area in Rio de Janeiro, Brazil. Zoologia 35, 1–12.CrossRefGoogle Scholar
Gibson, DI, Jones, A and Bray, RA (2002) Keys to the trematoda, vol. 1. p. 512. London, CABI Publishing and the Natural History Museum.CrossRefGoogle Scholar
Gleason, HA (1926) The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club 53, 7–26.CrossRefGoogle Scholar
Guégan, J-F, Lambert, A, Lévêque, C, Combes, C and Euzet, L (1992) Can host body size explain the parasite species richness in tropical freshwater fishes? Oecologia 90, 197–204.CrossRefGoogle ScholarPubMed
Higgins, CL (2008) Elements of metacommunity structure [online]. Texas, Tarleton State University. Available at http://faculty.tarleton.edu/higgins/documents/EMS.zip (accessed 20 Mar 2020).Google Scholar
ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (2003) Unidades de conservação – mata atlântica: Rebio guaribas [online]. Brasília, ICMBio. Available at https://www.icmbio.gov.br/portal/unidadesdeconservacao/biomas-brasileiros/mata-atlantica/unidades-de-conservacao-mata-atlantica/2151-rebio-de-guaribas (accessed 13 Feb 2021).Google Scholar
INPE (Instituto Nacional de Pesquisas Espaciais) (2019) SOS mata atlântica e INPE lançam novos dados do atlas do bioma [online]. São José dos Campos, INPE; Available at http://www.inpe.br/noticias/noticia.php?Cod_Noticia=5115 (accessed 6 Apr 2021).Google Scholar
Jansen, AM, Xavier, SCC and Roque, ALR (2015) The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Tropica 151, 1–15.CrossRefGoogle ScholarPubMed
Kajin, M, Cerqueira, R, Vieira, MV and Gentile, R (2008) Nine-year demography of the black-eared opossum Didelphis aurita (Didelphimorphia: Didelphidae) using life tables. Revista Brasileira de Zoologia 25, 206–213.CrossRefGoogle Scholar
Kersul, MG, Costa, NA, Boullosa, RG, et al. (2020) Helminth communities of sigmonontine rodents in cocoa agroforestry systems in Brazil. International Journal for Parasitology: Parasites and Wildlife 11, 62–71.Google ScholarPubMed
Khalil, LF, Jones, A and Bray, RA (1994) Keys to the Cestoda parasites of vertebrates. p. 751. London, CAB International.Google Scholar
Leibold, MA and Mikkelson, GM (2002) Coherence, species turnover and boundary clumping: elements of meta-community structure. Oikos 97, 237–250.CrossRefGoogle Scholar
Leibold, MA, Holyoak, M, Mouquet, N, et al. (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters 7, 601–613.CrossRefGoogle Scholar
Lemos, ER and D'Andrea, PS (2014) Trabalho de campo com animais: procedimentos, riscos e biossegurança. 1st edn. p. 180. Rio de Janeiro, Editora FIOCRUZ.CrossRefGoogle Scholar
Macedo, J, Loretto, D, Vieira, MV and Cerqueira, R (2006) Classes de desenvolvimento em marsupiais: um método para animais vivos. Mastozoologia Neotropical 13, 133–136.Google Scholar
MathWorks (2021) Bioinformatics toolbox: user's guide (R2021a). Natick, The MathWorks, Inc. Available at https://www.mathworks.com/?s_tid=gn_logo (accessed 28 Mar 2021).Google Scholar
Mihaljevic, JR (2012) Linking metacommunity theory and symbiont evolutionary ecology. Trends in Ecology and Evolution 27, 323–329.CrossRefGoogle ScholarPubMed
Morales-Castilla, I, Pappalardo, P, Farrell, MJ, Aguirre, AA, Huang, S, Gehman, ALM and Davies, TJ (2021) Forecasting parasite sharing under climate change. Philosophical Transactions of the Royal Society B 376(1837), 20200360.CrossRefGoogle ScholarPubMed
Müller, GA (2005) Diversidade e potencial zoonótico de parasitos de Didelphis albivrentris Lund, 1841 (Marsupialia: Didelphidae). Thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre. p. 122.Google Scholar
Oksanen, J, Blanchet, FG, Friendly, M, et al. (2020) vegan: community ecology package. R package version 2.5-7., https://cran.r-project.org, https://github.com/vegandevs/vegan.Google Scholar
Pinto, HA, Mati, VLT and Melo, ALD (2014) Toxocara cati (Nematoda: Ascarididae) in Didelphis albiventris (Marsupialia: Didelphidae) from Brazil: a case of pseudoparasitism. Brazilian Journal of Veterinary Parasitology 23, 522–525.Google ScholarPubMed
Poulin, R (1995) Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283–302.CrossRefGoogle Scholar
Poulin, R (2007) Evolutionary ecology of parasites. 2nd edn. p. 360. Princeton, Princeton University Press.CrossRefGoogle Scholar
Poulin, R (2013) Explaining variability in parasite aggregation levels among host samples. Parasitology 140, 541–546.CrossRefGoogle ScholarPubMed
Poulin, R (2014) Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology 44, 581–589.CrossRefGoogle ScholarPubMed
Poulin, R, Mouillot, D and George-Nascimento, M (2003) The relationship between species richness and productivity in metazoan parasite communities. Oecologia 137, 277–285.CrossRefGoogle ScholarPubMed
Presley, SJ, Higgins, CL and Willig, MR (2010) A comprehensive framework for the evaluation of metacommunity structure. Oikos 119, 908–917.CrossRefGoogle Scholar
Quintão e Silva, MG and Costa, HM (1999) Helminths of white-bellied opossum from Brazil. Journal of Wildlife Diseases 35, 371–374.CrossRefGoogle Scholar
Ramos, DGS, Santos, ARGLO, Freitas, LC, et al. (2016) Endoparasites of wild animals from three biomes in the state of Mato Grosso, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 68, 571–578.CrossRefGoogle Scholar
R Core Team (2021) R: a language and environment for statistical computing. Vienna, The R Project for Statistical Computing.Google Scholar
Runghen, R, Poulin, R, Monlleó-Borrull, C and Llopis-Belenguer, C (2021) Network analysis: ten years shining light on host–parasite interactions. Trends in Parasitology 37, 445–455.CrossRefGoogle ScholarPubMed
Simões, RO, Júnior, A, Olifiers, N, Garcia, JS, Bertolino, AVF and Luque, JL (2014) A longitudinal study of Angiostrongylus cantonensis in an urban population of Rattus norvegicus in Brazil: the influences of seasonality and host features on the pattern of infection. Parasites & Vectors 7, 100.CrossRefGoogle Scholar
Wells, K, Gibson, DI, Clark, NJ, Ribas, A, Morand, S and McCallum, HI (2018) Global spread of helminth parasites at the human–domestic animal–wildlife interface. Global Change Biology 24, 3254–3265.CrossRefGoogle ScholarPubMed
Whittaker, RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs 30, 279–338.CrossRefGoogle Scholar
Xavier, SCC, Roque, ALR, Bilac, D, Araújo, VAL, Costa-Neto, SF, Lorosa, ES and Jansen, AM (2014) Distantiae transmission of Trypanosoma cruzi: a new epidemiological feature of acute chagas disease in Brazil. PLOS Neglected Tropical Diseases 8, 1–9.CrossRefGoogle ScholarPubMed
Zabott, MV, Pinto, SB, Viott, AM, Gruchouskei, L and Bittencourt, LHF (2017) Helmintofauna de Didelphis albiventris (Lund. 1841) no Município de Palotina, Paraná, Brasil. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR 20, 19–22.CrossRefGoogle Scholar
Zuk, M and McKean, KA (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle ScholarPubMed
Supplementary material: File

Cirino et al. supplementary material

Cirino et al. supplementary material

Download Cirino et al. supplementary material(File)
File 38.3 KB