Publicado

2023-10-15

Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid

Nemátodos infectando a la rana escudo Adelophryne baturitensis en enclaves de la selva tropical del semiárido brasileño

DOI:

https://doi.org/10.15446/caldasia.v46n1.100705

Palabras clave:

parasitism, anuran, highland marshes, threatened species, protected areas (en)
parasitismo, anuros, pantanos de la sierra, especies en peligro, áreas de protección (es)

Autores/as

Parasitological studies provide important information about host biology. However, most anuran species in mountain environments have their helminth fauna understudied. In the present study, we aimed to inventory the endoparasites associated with the shield frog Adelophryne baturitensis from an altitudinal rainforest enclave in the Brazilian semiarid region. We found 57 specimens from five nematode taxa. Perhaps, the high nematode infection on this mountain frog might be related to the host’s direct life cycle where they do not need water ponds to lay eggs and reach tadpole development. Trematodes and other endoparasite taxa are commonly reported in water-dependent frogs. Although shield frogs seem to be myrmecophagous, more studies are still needed to investigate how their feeding habits might influence parasitological infection. Our study is an important contribution to understanding the parasite-host ecological relationship in minute frogs.

Los estudios parasitológicos proporcionan información importante sobre la biología del huésped. Sin embargo, la mayoría de las especies de anuros de los entornos montañosos tienen una fauna de helmintos poco estudiada. En el presente estudio, inventariamos los endoparásitos asociados al sapo escudo Adelophryne baturitensis de un enclave de selva tropical altitudinal en la región semiárida brasileña. Encontramos 57 especímenes de cinco taxones de nematodos. La elevada infección por nematodos en esta rana de montaña puede estar relacionada con el ciclo de vida directo del hospedador el cual ocurre sin necesidad de charcos de agua para la puesta de huevos y el desarrollo de renacuajos. Los trematodos y otros taxones endoparásitos son habituales en las ranas dependientes del agua. Aunque los sapos escuderos parecen ser mirmecófagos, todavía se necesitan más estudios para investigar cómo sus hábitos alimentarios pueden influir en la infección parasitológica. Nuestro estudio constituye una importante contribución a la comprensión de la relación ecológica parásito-huésped en las ranas pequeñas.

Referencias

Ab'Saber AN. 1974. O domínio morfoclimático semi-árido das caatingas brasileiras. Geomorfologia 43:1-39.

Aguiar A, Morais DH, Pyles PC, Silva RJ. 2014. Evaluation of helminths associated with 14 amphibian species from a Neotropical Island near the southeast coast of Brazil. Herpetol. Rev. 45:227-236.

Aho JM. 1990. Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In: Esch GW, Bush AO, Aho JM, Editors. Parasite Communities: Patterns and Processes. New York, Chapman & Hall. p. 157-195.

Alcantara EP, Ferreira-Silva C, Silva LAF, Lins AGS, Ávila RW, Morais DH, da Silva RJ. 2018. Helminths of Dermatonotus muelleri (Anura: Microhylidae) from Northeastern Brazil. J. Parasitol. 104(5):550-556. doi: https://doi.org/10.1645/16-160

Alford RA, Richards SJ. 1999. Global amphibian declines: a problem in applied ecology. Annu. Rev. Ecol. Evol. Syst. 30:133-165. doi: https://doi.org/10.1146/annurev.ecolsys.30.1.133

Amato JFR, Boeger WP, Amato SB. 1991. Protocolos para laboratório: coleta e processamento de parasitos de pescado. 1st ed. Rio de Janeiro: Seropédica, Imprensa Universitária da UFRRJ.

Amato JFR, Amato SB. 2010. Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves. In: Matter SV, Straube FC, Accordi YA, Piacentini VQ, Cândido-Junior JF, Editors. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro: Technical Books. p. 1-25.

Amorim DM, Oliveira RH, Dyna CS, Sousa DM, Santos MEP, Lima LS, Pinto LC, Ávila RW. 2019. Nematodes Parasites of Rhinella jimi (Stevaux, 2002) (Anura: bufonidae) in areas of Caatinga, Northeastern Brazil. Neotrop. Helminthol. 13:265-271.

Anderson RC. 2000. Nematode parasites of vertebrates, their development and transmission. 2nd ed. Wallingford: CABI Publishing. doi: https://doi.org/10.1079/9780851994215.0000

Andrade-Lima D. 1982. Present-day forest refuges in Northeastern Brazil. In: Prance GT, Editor. Biological diversification in the tropics. New York: Columbia University Press.

Ávila RW, Silva RJ. 2010. Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. J. venom. anim. toxins incl. trop. dis. 16(4):543-572. doi: https://doi.org/10.1590/S1678-91992010000400005

Bentz S, Sinnappah-Kang ND, Lim LHS, Lebedev B, Combes C, Verneau O. 2006. Historical biogeography of amphibian parasites, genus Polystoma (Monogenea: Polystomatidae). J. Biogeogr. 33(4):742-749. doi: https://doi.org/10.1111/j.1365-2699.2005.01402.x

Bush AO, Lafferty KD, Lotz JM, Shostak AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83(4):575-583. doi: https://doi.org/10.2307/3284227

Calil PR, Gonzalez IHL, Salgado PAB, Cruz JD, Ramos PL, Chagas CRF. 2017. Hemogregarine parasites in wild captive animals, a broad study in São Paulo Zoo. J. Entomol. Zool. Stud. 5:1378-1387.

Campião KM, Delatorre M, Rodrigues RB, da Silva RJ, Ferreira VL. 2012. The effect of local environmental variables on the helminth parasite communities of the pointed belly frog Leptodactylus podicipinus from ponds in the Pantanal wetlands. J. Parasitol. 98(2):229-235. doi: https://doi.org/10.1645/GE-2877.1

Campião KM, Morais DH, Dias OT, Aguiar A, Toledo G, Tavares LER, Silva RJ. 2014. Checklist of helminth parasites of amphibians from South America. Zootaxa 3843(1):1-93. doi: https://doi.org/10.11646/zootaxa.3843.1.1

Campião KM, de Aquino-Ribas AC, Morais DH, da Silva RJ, Tavares LER. 2015. How many parasites species a frog might have? Determinants of parasite diversity in South American anurans. Plos One 10(10):1-12. doi: https://doi.org/10.1371/journal.pone.0140577

CFMV - Conselho Federal de Medicina Veterinária. 2013. Guia brasileiro de boas práticas de eutanásia em animais. 1st ed. Brasília, Distrito Federal: Comissão de ética, bioética e bem-estar animal.

Collins JP. 2010. Amphibian decline and extinction: what we know and what we need to learn. Dis. Aquat. Org. 92(2-3):93-99. doi: https://doi.org/10.3354/dao02307

Espino-del-Castillo A, Paredes-León R., Morales-Malacara JB. 2011. Presence of intradermal chigger mite Hannemania hylae (Ewing, 1925) (Acari: Leeuwenhoekiidae) in the troglophile frog Eleutherodactylus longipes (Anura: Brachycephalidae) at Los Riscos cave, Querétaro, México. Int. J. Acarology. 37(5):427-440. doi: https://doi.org/10.1080/01647954.2010.525522

Galli P, Crosa G, Mariniello L, Ortis M, D'amelio S. 2001. Water quality as a determinant of the composition of fish parasite communities. Hydrobiologia. 452:173-179. doi: https://doi.org/10.1023/A:1011958422446

González CE, Hamann MI. 2006. Helmintos parásitos de Leptodactylus bufonius Boulenger, 1894 (Anura: Leptodactylidae) de Corrientes, Argentina. Rev. Esp. Herpetol. 20:39-46.

Hamann MI, Kehr AI, González CE. 2006. Species affinity and infracommunity ordination of helminths of Leptodactylus chaquensis (Anura: Leptodactylidae) in two contrasting environments from Northeastern Argentina. J. Parasitol. 92(6):1171-1179. doi: https://doi.org/10.1645/GE-862R1.1

Heyer WR, Donnelly MA, McDiarmid RW, Hayek LC, Foster MS. 1994 Measuring and Monitoring Biological Diversity - Standard Methods for Amphibians. Smithsonian Institution Press.

Hoogmoed MS, Borges DM, Cascon P. 1994. Three new species of the genus Adelophryne (Amphibia: Anura: Leptodactylidae) from northeastern Brazil, with remarks on the other species of the genus. Zool. Meded. 68:271–300.

Imai DM, Nadler SA, Brenner D, Donovan TA, Pessier AP. 2009. Rhabditid Nematode-Associated Ophthalmitis and Meningoencephalomyelitis in Captive Asian Horned Frogs (Megophrys montana). J Vet Diagn Invest. 21(4):568-573. doi: https://doi.org/10.1177/104063870902100427

Kelehear C, Webb JK, Hagman M, Shine R. 2011. Interactions between infective helminth larvae and their anuran hosts. Herpetologica 67(4):378-385. doi: https://doi.org/10.1655/HERPETOLOGICA-D-11-00027.1

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. doi: https://doi.org/10.1007/s10393-012-0785-3

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(1):74-80. doi: https://doi.org/10.1590/S1984-29612017013

Lourenço-de-Moraes R, Solé M, Toledo LF. 2012. A new species of Adelophryne Hoogmoed and Lescure 1984 (Amphibia: Anura: Eleutherodactylidae) from the Atlantic rainforest of southern Bahia, Brazil. Zootaxa 3441(1):59-66. doi: https://doi.org/10.11646/zootaxa.3441.1.6

MacCulloch RD, Lathrop A, Kok PJR, Minter LR, Khan SZ, Barrio-Amorós C. 2008. A new species of Adelophryne (Anura: Eleutherodactylidae) from Guyana, with additional data on A. gutturosa. Zootaxa 1884(1):36-50. doi: https://doi.org/10.11646/zootaxa.1884.1.2

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

Martins-Sobrinho PM, Silva WGDO, Santos EGD, Moura GJB, Oliveira JB. 2017. Helminths of some tree frogs of the families Hylidae and Phyllomedusidae in an Atlantic rainforest fragment, Brazil. J. Nat. Hist. 51(27-28):1639-1648. doi: https://doi.org/10.1080/00222933.2017.1337945

Mascarenhas W, Oliveira CR, Benício RA, Ávila RW, Ribeiro SC. 2021. Nematodes of Proceratophrys ararype (Anura: Odontophrynidae), an endemic frog from the Araripe Plateau, northeastern Brazil. Biota Neotrop. 21(3). doi: https://doi.org/10.1590/1676-0611-BN-2020-1164

Moravec F, Kaiser H. 1994. Trichospirura amphibiophila n. sp. (Nematoda: Rhabdochonidae) in the frog Eleutherodactylus martinicensis from La Désirade, French Antilles. J. Parasitol. 80(1):121-125. doi: https://doi.org/10.2307/3283354

Moro MF, Macedo MB, Moura-Fé MM, Castro ASF, Costa RC. 2015. Vegetation, phytoecological regions and landscape diversity in Ceará state, northeastern Brazil. Rodriguésia 66(3):717-743. doi: https://doi.org/10.1590/2175-7860201566305

Nascimento LCS, Gonçalves EC, Vasconcelos-Melo FT, Giese EG, Furtado AP, dos Santos JN. 2013. Description of Rhabdias breviensis n. sp. (Rhabditoidea: Rhabdiasidae) in two neotropical frog species. Syst. Parasitol. 86:69-75. doi: https://doi.org/10.1007/s11230-013-9432-9

Oliveira CR, Lima DC, Ávila RW, Borges-Nojosa DM. 2022a. Endoparasites of Adelophryne maranguapensis Hoogmoed, Borges & Cascon, 1994 (Anura, Eleutherodactylidae), an endemic and threatened species from an altitude swamp in northeastern Brazil. Parasitol. Res. 2022:1-5. doi: https://doi.org/10.1007/s00436-022-07458-y

Oliveira, CR, Mascarenhas W, Batista-Oliveira D, Araújo KC, Ávila RW, Borges-Nojosa DM. 2022b. Endoparasite community of anurans from an altitudinal rainforest enclave in a Brazilian semiarid area. J. Helminthol. 96:1-17. doi: https://doi.org/10.1017/S0022149X22000499

Pessier AP. 2008. Management of disease as a threat to amphibian conservation. Int. Zoo Yearb. 42(1):30-39. doi: https://doi.org/10.1111/j.1748-1090.2008.00047.x

Pizzatto L, Clulow J, Mahony M. 2016. Eye malformation and body coloration in Litoria aurea tadpoles. Salamandra 52:207-210.

Poulin R, Morand S. 2000. The diversity of parasites. Q. rev. biol. 75(3):277-293. doi: https://doi.org/10.1086/393500

Poulin R. 2007. Are there general laws in parasite ecology? Parasitology 134(6):763-776. doi: https://doi.org/10.1017/S0031182006002150

Roberto IJ, Loebmann D. 2016. Composition, distribution patterns, and conservation priority areas for the herpetofauna of the state of Ceará, northeastern Brazil. Salamandra 52:134-152.

Rózsa L, Reiczigel J, Majoros, G. 2000. Quantifying parasites in samples of hosts. J. Parasitol. 86(2):228-232. doi: https://doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2

Segalla MV, Berneck B, Canedo C, Caramaschi U, Cruz CAG, Grant PCAT, Haddad CFB, Lourenço ACC, Mott SMT, Nascimento LB, Toledo LF, Werneck FP, Langone JA. 2021. Brazilian amphibians: List of species. Herpetol. Bras. 10:121-216. doi: https://doi.org/10.5281/zenodo.4716176

Silva-Neta AD, Alcantara 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.

Silvano D, Borges-Nojosa D. c2004. Adelophryne baturitensis. The IUCN Red List of Threatened Species. [Revisada en: 10 diciembre 2021]. https://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T56300A11452255.en

Teles DA, Brito SV, Araújo-Filho JÁ, Teixeira AAM, Ribeiro SC, Mesquita DO, Almeida WO. 2017. Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the Caatinga domain of the neotropical region in Brazil. Herpetol. Notes 10:525-527.

Todd BD. 2007. Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians. Am. Nat. 170(5):793-799. doi: https://doi.org/10.1086/521958

Toledo GM, Fonseca MG, Iannacone J, Callirgos JMC, Vidaurre CUM, Silva RJ. 2017. Helmintos Parásitos de Rhinella marina (Linnaeus, 1758) (Anura: bufonidae) de Tarapoto, Perú. Biologist. 15:459-468. doi: https://doi.org/10.24039/rtb2017152203

Yoder HR, Coggins JR. 2007. Helminth communities in five species of sympatric amphibians from three adjacent ephemeral ponds in southeastern Wisconsin. J. Parasitol. 93(4):755-760. doi: https://doi.org/10.1645/GE-1077R.1

Cómo citar

APA

Batista-Oliveira, D., de Castro Araujo, K., De Oliveira, C. R., Cassiano-Lima, D. y Ávila, R. W. (2023). Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid. Caldasia, 46(1). https://doi.org/10.15446/caldasia.v46n1.100705

ACM

[1]
Batista-Oliveira, D., de Castro Araujo, K., De Oliveira, C.R., Cassiano-Lima, D. y Ávila, R.W. 2023. Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid. Caldasia. 46, 1 (ago. 2023). DOI:https://doi.org/10.15446/caldasia.v46n1.100705.

ACS

(1)
Batista-Oliveira, D.; de Castro Araujo, K.; De Oliveira, C. R.; Cassiano-Lima, D.; Ávila, R. W. Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid. Caldasia 2023, 46.

ABNT

BATISTA-OLIVEIRA, D.; DE CASTRO ARAUJO, K.; DE OLIVEIRA, C. R.; CASSIANO-LIMA, D.; ÁVILA, R. W. Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid. Caldasia, [S. l.], v. 46, n. 1, 2023. DOI: 10.15446/caldasia.v46n1.100705. Disponível em: https://revistas.unal.edu.co/index.php/cal/article/view/100705. Acesso em: 23 may. 2024.

Chicago

Batista-Oliveira, Dalilange, Kássio de Castro Araujo, Cicero Ricardo De Oliveira, Daniel Cassiano-Lima, y Robson Waldemar Ávila. 2023. «Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid». Caldasia 46 (1). https://doi.org/10.15446/caldasia.v46n1.100705.

Harvard

Batista-Oliveira, D., de Castro Araujo, K., De Oliveira, C. R., Cassiano-Lima, D. y Ávila, R. W. (2023) «Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid», Caldasia, 46(1). doi: 10.15446/caldasia.v46n1.100705.

IEEE

[1]
D. Batista-Oliveira, K. de Castro Araujo, C. R. De Oliveira, D. Cassiano-Lima, y R. W. Ávila, «Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid», Caldasia, vol. 46, n.º 1, ago. 2023.

MLA

Batista-Oliveira, D., K. de Castro Araujo, C. R. De Oliveira, D. Cassiano-Lima, y R. W. Ávila. «Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid». Caldasia, vol. 46, n.º 1, agosto de 2023, doi:10.15446/caldasia.v46n1.100705.

Turabian

Batista-Oliveira, Dalilange, Kássio de Castro Araujo, Cicero Ricardo De Oliveira, Daniel Cassiano-Lima, y Robson Waldemar Ávila. «Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid». Caldasia 46, no. 1 (agosto 9, 2023). Accedido mayo 23, 2024. https://revistas.unal.edu.co/index.php/cal/article/view/100705.

Vancouver

1.
Batista-Oliveira D, de Castro Araujo K, De Oliveira CR, Cassiano-Lima D, Ávila RW. Nematodes Infecting the Shield Frog Adelophryne baturitensis in Rainforest Enclaves of Brazilian Semiarid. Caldasia [Internet]. 9 de agosto de 2023 [citado 23 de mayo de 2024];46(1). Disponible en: https://revistas.unal.edu.co/index.php/cal/article/view/100705

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