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Endoparasites of Adelophryne maranguapensis Hoogmoed, Borges & Cascon, 1994 (Anura, Eleutherodactylidae), an endemic and threatened species from an altitude swamp in northeastern Brazil

  • Immunology and Host-Parasite Interactions - Short Communication
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Abstract

Adelophryne maranguapensis is an endangered anuran species endemic to the Maranguape residual mountain, Ceará State, northeaster Brazil, which is under strong anthropogenic pressure. There are still few studies on the natural history of this species that allow a better understanding of its biology and can provide the basis for conservation actions. Studies on endoparasitism are an important source for the comprehension of ecological relationships, as well as for providing information on host biology and its relevance to ecosystems. Thus, we present information about the endoparasites helminths, the relationship of parasite abundance with the size of individuals and the parasite difference between the sexes in A. maranguapensis, to elucidate some characteristics in the host-parasite relationship and the use of the area of this anuran. We analysed 107 specimens deposited in the Herpetological Collection of the Federal University of Ceará, sampled from 2010 to 2012. Total prevalence of 24.30% was recorded, and four parasitic taxa were identified, Aplectana sp., Physaloptera sp., Parapharyngodon sp. and an unidentified Ascarid. No relationship between the abundance of parasites and snout-vent length was found and the parasite difference between the sexes. Even though identification of the parasites at species level was not possible, A. maranguapensis follows a common pattern in parasitism of Neotropical species.

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References

  • Abrahão CR, Escarlate-Tavares F (2019) Ameaças à Herpetofauna da Mata Atlântica nordestina. In: Abrahão CR, Moura GJB, Freitas MA, Escarlate-Tavares F (Org.) Plano de ação nacional para a conservação da herpetofauna ameaçada da Mata Atlântica nordestina. Instituto Chico Mendes de Conservação da Biodiversidade, ICMBio, Brasília, pp. 162–174

  • Aho JM (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In: Esch GW, Bush AO, Aho JM (Eds.) Parasite Communities: Patterns and Processes. New York, Chapman & Hall.

  • Amato JFR, Boeger WA, Amato SB (1991) Protocolos para Laboratório-Coleta e Processamento de Parasitos de Pescado. Universidade Federal do Rio de Janeiro, Seropédica

    Google Scholar 

  • Anderson RC (2000) Nematode parasites of vertebrates, their development and transmission, 2nd edn. Oxon, CABI Publishing, Wallingford

    Google Scholar 

  • Araújo-Filho JA, Brito SV, Almeida WO, Morais DH, Ávila RW (2015) A new species of Parapharyngodon (Nematoda: Pharyngodonidae) infecting Dermatonotus muelleri (Anura: Microhylidae) from Caatinga, Northeastern Brazil. Zootaxa 4012:386–390.https://doi.org/10.11646/zootaxa.4012.2.10

  • Ávila RW, Anjos LA, Ribeiro SC, Morais DH, Silva RJ, Almeida WO (2012) Nematodes of lizards (Reptilia: Squamata) from Caatinga Biome, northeastern Brazil. Comp Parasitol 79:56–63. https://doi.org/10.1654/4518.1

    Article  Google Scholar 

  • Boquimpani-Freitas ID, Vrcibradic D, Vicente JJ, Bursey CR, Rocha CFD, Sluys MV (2001) Helminths of the horned leaf frog, Proceratophrys appendiculata, from southeastern Brazil. J Helminthol 75:233–236. https://doi.org/10.1079/JOH200155

    Article  CAS  PubMed  Google Scholar 

  • Bursey CR, Goldberg SR (2015) Description of a new species of Parapharyngodon (Nematoda: Pharyngodonidae) from Mexico with a list of current species and key to species from the Panamanian region. J Parasitol 101:374–381. https://doi.org/10.1645/13-460.1

    Article  PubMed  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227

    Article  CAS  PubMed  Google Scholar 

  • Camardelli M, Napoli M (2012) Amphibian conservation in the Caatinga Biome and semiarid region of Brazil. Herpetologica 68:31–47. https://doi.org/10.1655/HERPETOLOGICA-D-10-00033.1

    Article  Google Scholar 

  • Campião KM, Ribas ACA, Morais DH, Dias OT, Silva RJ, Tavares LER (2015) How many parasites species a frog might have? Determinants of parasite diversity in South American anurans. PLoS One 10:e0140577. https://doi.org/10.1371/journal.pone.0140577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campião KM, Silva IC, Dalazen GT, Paiva F, Tavares LE (2016) Helminth parasites of 11 anuran species from the Pantanal Wetland, Brazil. Comp Parasitol 83:92–100. https://doi.org/10.1654/1525-2647-83.1.92

    Article  Google Scholar 

  • Cassiano-Lima D, Borges-Nojosa DM, Cechin SZ (2014) The advertisement call of Adelophryne maranguapensis (Anura, Eleutherodactylidae). Zootaxa 3835:299–300 https://doi.org/10.11646/zootaxa.3835.2.11

  • Cassiano-Lima D, Lima AV, Fortunato ME, Sousa TA, Castro DP, Borges-Nojosa DM, Cechin SZ (2020) Reproductive biology of direct developing and threatened frog Adelophryne maranguapensis (Anura, Eleutherodactylidae) reveals a cryptic reproductive mode for anurans and the first record of parental care for the genus. J Nat Hist 54:1721–1733. https://doi.org/10.1080/00222933.2020.1830192

    Article  Google Scholar 

  • Ferreira ACS, Vieira FM, Da Silva DCN, Ribeiro LB, Ferreira JA, Muniz-Pereira LC (2021) Parapharyngodon hispidus n. sp. (Nematoda: Pharyngodonidae) in Tropidurus hispidus (Spix) (Squamata: Tropiduridae) from Caatinga Biome of the Vale do São Francisco, state of Pernambuco, Brazil with a key for the Neotropical species of the genus Parapharyngodon Chatterji. Zootaxa 4980:195–200 https://doi.org/10.11646/zootaxa.4980.1.12

  • Freitas JFT (1957) Sôbre os gêneros Thelandros Wedl, 1862 e Parapharyngodon Chatterji, 1933, com descrição de Parapharyngodon alvarengai sp. n. (Nematoda, Oxyuroidea). Mem Inst Oswaldo Cruz 55:21–45

    Article  Google Scholar 

  • Freitas JFT, Dobbin JE Jr (1959) Nova espécie do gênero Parapharyngodon Chatterji, 1933 (Nematoda, Oxyuroidea). An Soc Biol Pernambuco 16:23–33

    Google Scholar 

  • Frost DR (2021) Amphibian species of the world: an online reference. Version 6.1. Electronic Database. Accessible at: https://amphibiansoftheworld.amnh.org/index.php. (access: 22 September 2021)

  • Gibbons L (2010) Keys to the nematode parasites of vertebrates. Supplementary Volume. CABI International, Wallingford

  • González CE, Hamann MI (2013) First record of Brevimulticaecum larvae (Nematoda, Heterocheilidae) in amphibians from northern Argentina. Braz J Biol 73:451–452. https://doi.org/10.1590/S1519-69842013000200031

    Article  PubMed  Google Scholar 

  • Guillén-Hernández S, Salgado-Maldonado G, Lamothe-Argumedo R (2000) Digeneans (Plathelminthes: Trematoda) of seven sympatric species of anurans from Los Tuxtlas, Veracruz, Mexico. Stud Neotrop Fauna Environ 35:10–13. https://doi.org/10.1076/0165-0521(200004)35:1;1-M;FT010

    Article  Google Scholar 

  • Hartwich G (2009) Ascaridida. In: Anderson RC, Chabaud AG, Wilmott S (eds) Keys to the nematode parasites of vertebrates. CAB International, Wallingford, pp 309–323

    Chapter  Google Scholar 

  • IUCN (2020) The IUCN red list of threatened species. Version 2020-1. Accessible at: https://www.iucnredlist.org (last access on: 14/04/2021)

  • Klaion T, Gomes MA, Tavares LER, Rocha CFD, Sluys MV (2011) Diet and nematode infection in Proceratoprhys boiei (Anura: Cycloramphidae) from two Atlantic Rainforest remnants in southeastern Brazil. An Acad Bras Ciênc 83:1303–1312 https://doi.org/10.1590/S0001-37652011000400017

  • Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, Johnson PTJ (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9:342–360. https://doi.org/10.1007/s10393-012-0785-3

    Article  PubMed  Google Scholar 

  • Lins AGS, Aguiar A, Morais DH, Silva LAF, Ávila RW, Silva RJ (2017) Helmintofauna de Leptodactylus syphax (Anura: Leptodactylidae) do bioma da Caatinga, Nordeste do Brasil. Rev Bras Parasitol Vet 26:74–80. https://doi.org/10.1590/S1984-29612017013

    Article  PubMed  Google Scholar 

  • Luque JL, Martins NA, Tavares LER (2005) Community structure of metazoan parasites of the yellow Cururu toad, Bufo ictericus (Anura, Bufonidae) from Rio de Janeiro, Brazil. Acta Parasitol 50:215–220

    Google Scholar 

  • Mascarenhas W, Oliveira CR, Benício RA, Ávila RW, Ribeiro SC (2021) Nematodes of Proceratophrysararype (Anura: Odontophrynidae), an endemic frog from the Araripe Plateau, Northeastern Brazil. Biota Neotrop 21:e20201164. https://doi.org/10.1590/1676-0611-BN-2020-1164

    Article  Google Scholar 

  • Marcogliese DJ (2004) Parasites: small players with crucial roles in the ecological theatre. Ecohealth 1:151–164. https://doi.org/10.1007/s10393-004-0028-3

    Article  Google Scholar 

  • Miranda C (1924) Alguns nematodeos do gênero Aplectana Railliet Henry, 1916. Mem Inst Oswaldo Cruz 17:45–54

    Article  Google Scholar 

  • Moravec F, Kaiser H (1994) Brevimulticaecum sp. larvae (Nematoda: Anisakidae) from the frog Hyla minuta Peters in Trinidad. J Parasitol 80:154–156. https://doi.org/10.2307/3283361

    Article  CAS  PubMed  Google Scholar 

  • Oliveira CR, Ávila RW, Morais DH (2019) Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, brazil. Acta Parasitol 64:205–212. https://doi.org/10.2478/s11686-018-00022-8

    Article  PubMed  Google Scholar 

  • Pereira FB, Alves PV, Rocha BM, Souza-Lima S, Luque JL (2012) A new Physaloptera (Nematoda: Physalopteridae) parasite of Tupinambis merianae (Squamata: Teiidae) from south eastern Brazil. J Parasitol 98:1227–1235. https://doi.org/10.1645/GE-3159.1

    Article  PubMed  Google Scholar 

  • Ramírez-Bautista A, Balderas-Valdivia C, Vitt LJ (2000) Reproductive ecology of the whiptail lizard Cnemidophorus lineatissimus (Squamata: Teiidae) in a tropical dry forest. Copeia 2000:712–722. https://doi.org/10.1643/0045-8511(2000)000[0712:REOTWL]2.0.CO;2

    Article  Google Scholar 

  • Reyda FB (2008) Intestinal helminths of freshwater stingrays in Southeaster Peru, and a new genus and two new species of cestode. J Parasitol 94:684–699. https://doi.org/10.1645/GE-1230.1

    Article  PubMed  Google Scholar 

  • Silva-Neta AD, Alcântara EP, Oliveira CR, Carvalho EFF, Morais DH, Silva RJ, Ávila RW (2020) Helminths associated with 15 species of anurans from the Ibiapaba Plateau, northeastern Brazil. Neotrop Helminthol 14:207–216

    Article  Google Scholar 

  • Silvano DL, Segalla MV (2005) Conservation of Brazilian amphibians. Conserv Biol 19:653–658. https://doi.org/10.1111/j.1523-1739.2005.00681.x

    Article  Google Scholar 

  • Tabarelli M, Pinto LP, Silva JMC, Hirota MM, Bedê LC (2005) Desafios e oportunidades para a conservação da biodiversidade na Mata Atlântica brasileira. Megadiversidade 1:132–138

    Google Scholar 

  • Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM (1991) Nematóides do Brasil, 2° parte: Nematóides de anfíbios. Rev Bras Zool 7:549–626

    Article  Google Scholar 

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Acknowledgements

We would like to acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) for the scholarship granted to CRO (C.R.O., # 88882.454307/2019-01). RWA and DMBN thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting research grants (R.W.A., PQ # 303622/2015-6; and 305988/2018-2; D.M.B.N., PQ # 309617/2012-0; and 311961/2016-9). D.C.L. thanks the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP, Proc. 04006575/2021 and BDS-0017-00003.01.18/10). Lastly, we also thank to CNPq for their financial support (Project PVE # 401800/2013-0) and Castiele Holanda Bezerra for help in processing the analysed material.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Ecologia e Recursos Naturais - Bloco 902, Centro de Ciências, Universidade Federal do Ceará – UFC, Campus do PICI, Av. Humberto Monte, s/n, Fortaleza, Ceará, CEP, 60455-760, Brazil

    Cicero Ricardo de Oliveira, Robson Waldemar Ávila & Diva Maria Borges-Nojosa

  2. Núcleo Regional de Ofiologia - Bloco 905, Universidade Federal do Ceará, Campus do PICI, Avenida Humberto Monte, s/n, Fortaleza, Ceará, CEP, 60455-760, Brazil

    Cicero Ricardo de Oliveira, Robson Waldemar Ávila & Diva Maria Borges-Nojosa

  3. Museu de História Natural do Ceará Professor Dias da Rocha, Universidade Estadual do Ceará, Rua Divino Salvador, 225, Pacoti, Ceará, CEP, 62770-000, Brazil

    Daniel Cassiano Lima

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  1. Cicero Ricardo de Oliveira
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  2. Daniel Cassiano Lima
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  3. Robson Waldemar Ávila
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  4. Diva Maria Borges-Nojosa
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Correspondence to Cicero Ricardo de Oliveira.

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de Oliveira, C.R., Lima, D.C., Ávila, R.W. et al. Endoparasites of Adelophryne maranguapensis Hoogmoed, Borges & Cascon, 1994 (Anura, Eleutherodactylidae), an endemic and threatened species from an altitude swamp in northeastern Brazil. Parasitol Res 121, 1053–1057 (2022). https://doi.org/10.1007/s00436-022-07458-y

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