Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-04T01:48:27.420Z Has data issue: false hasContentIssue false
  • English
  • Français

Pattern of anuran infection by acanthocephalans from the Cerrado, Northeastern Brazil with a summary for South America

Published online by Cambridge University Press:  02 February 2024

B.R. dos Santos ,
A.A.M. Teixeira Open the ORCID record for A.A.M. Teixeira [Opens in a new window] ,
J.M. do Nascimento  and
S.V. Brito
B.R. dos Santos
Affiliation:
Departamento de Biologia, Programa de Pós-Graduação em Biodiversidade e Conservação, Centro de Ciências Biológicas e da Saúde, Universidade Federal do Maranhão, Cidade Universitária Dom Delgado, CEP 65080-805, São Luís, MA, Brazil
A.A.M. Teixeira*
Affiliation:
Centro de Ciências de Chapadinha, Universidade Federal do Maranhão, Br 222, Km 04, S/N, Boa Vista, CEP 65500-000, Chapadinha, MA, Brazil
J.M. do Nascimento
Affiliation:
Centro de Ciências Biológicas e da Saúde, Programa de Pós-Graduação em Rede – Rede de Biodiversidade e Biotecnologia da Amazônia Legal – BIONORTE, Universidade Federal do Maranhão, Cidade Universitária Dom Delgado, CEP 65080-805, São Luís, MA, Brazil
S.V. Brito
Affiliation:
Centro de Ciências de Chapadinha, Universidade Federal do Maranhão, Br 222, Km 04, S/N, Boa Vista, CEP 65500-000, Chapadinha, MA, Brazil
*
Corresponding author: A.A.M. Teixeira; Email: adoniasteixeira01@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

In Brazil, acanthocephalans parasitise anurans in several biomes. In the present study, we performed an analysis of acanthocephalan infections across 175 anuran individuals from the Cerrado biome, belonging to ten species: Boana raniceps, Pithecopus hypochondrialis, Scinax fuscomarginatus, Scinax x-signatus, Leptodactylus pustulatus, Leptodactylus macrosternum, Leptodactylus vastus, Physalaemus cuvieri, Adenomera hylaedactyla, and Elachistocleis piauiensis. We also verified the specificity of the parasites using the STD* index. Additionally, we conducted a survey of acanthocephalan infection in anurans in South America. The studied assemblage in the Brazilian Cerrado presented 57 parasitised hosts of 175 specimens (overall prevalence: 32.6%). In total, 437 acanthocephalans cystacanths were recorded, among which 286 presented the same morphotype but could not be identified, 148 belonged to the genus Centrorhynchus, and three belonged to Oncicola. Unidentified acanthocephalans had a higher prevalence in L. vastus (53.85%) and the highest intensity was in L. pustulatus (17±16). The highest prevalence of Centrorhynchus sp. was in the species S. fuscomarginatus (28.57%), while the highest intensity was observed in L. vastus (111). The taxon Oncicola sp. it had a prevalence of 3.23% and an intensity of 3 only in S. x-signatus. The highest specificity was recorded for Oncicola sp. (STD*= 1), whereas the lowest was found in Centrorhynchus sp. (STD*= 2.21). Finally, according to the survey for South America, we found ten records of acanthocephalan taxa parasitizing 58 species of anurans distributed in seven countries (Brazil with the most records).

Keywords

Helminthsendoparasitesfrogs
Type
Research Paper
Information
Journal of Helminthology , Volume 98 , 2024 , e15
Copyright
© The Author(s), 2024. 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

Aguiar, A, Morais, DH, Cicchi, PJP, and Silva, RJ (2014) Evaluation of helminths associated with 14 amphibian species from a neotropical island near the southeast coast of Brazil. Herpetological Review 45, 227–236.Google Scholar
Aguiar, A, Toledo, GM, Anjos, LA, and Silva, RJ (2015) Helminth parasite communities of two Physalaemus cuvieri Fitzinger, 1826 (Anura: Leiuperidae) populations under different conditions of habitat integrity in the Atlantic Rain Forest of Brazil. Brazilian Journal of Biology 75, 963–968.CrossRefGoogle ScholarPubMed
Aguiar, A, Morais, DH, Silva, LAF, Dos Anjos, LA, Foster, OC, and Silva, RJ (2021) Biodiversity of anuran endoparasites from a transitional area between the Atlantic Forest and Cerrado biomes in Brazil: new records and remarks. Zootaxa 4948, 1–41.CrossRefGoogle ScholarPubMed
Amin, OM (2013) Classification of the Acanthocephala. Folia Parasitologica 60, 273–305. doi: 10.14411/fp.2013.031.CrossRefGoogle ScholarPubMed
Arredondo, NJ and de Pertierra, AAG (2009) Pseudoacanthocephalus lutzi (Hamann, 1891) comb. n. (Acanthocephala: Echinorhynchidae) for Acanthocephalus lutzi (Hamann, 1891), parasite of South American amphibians. Folia Parasitologica 56, 295–304.CrossRefGoogle ScholarPubMed
Bower, DS, Brannelly, LA, McDonald, C, Webb, RJ, Greenspan, SE, Vickers, M, Gardner, MG, and Greenlees, MJ (2019) A review of the role of parasites in the ecology of reptiles and amphibians. Austral Ecology 44, 433–448. doi: 10.1111/aec.12695.CrossRefGoogle Scholar
Brusca, RC, Moore, W, and Shuster, SM (2018) Invertebrados. 3rd edn. Rio de Janeiro, Guanabara Koogan.Google Scholar
Bursey, CR, Goldberg, SR, and Parmelee, JR (2001) Gastrointestinal helminths of 51 species of anurans from Reserva Cuzco Amazónico, Peru. Comparative Parasitology 68, 21–35.Google Scholar
Bursey, CR, Vrcibradic, D, Hatano, FH, and Rocha, CFD (2006) New genus, new species of Acanthocephala (Echinorhynchidae) from the Brazilian frog Hylodes phyllodes (Anura: Leptodactylidae). Journal of Parasitology 92, 353–356. doi: 10.1645/GE-3518.1.CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM, and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583. doi: 10.2307/3284227.CrossRefGoogle Scholar
Cabrera-Guzmán, E, Garrido-Olvera, L, and León-Règagnon, V (2010) Helminth parasites of the leopard frog Lithobates sp. Colima (Amphibia: Ranidae) from Colima, Mexico. Journal of Parasitology 96, 736–739. doi: 10.1645/GE-2335.1.CrossRefGoogle ScholarPubMed
Campião, KM, da Silva, ICO, Dalazen, GT, Paiva, F, and Tavares, LER (2016) Helminth parasites of 11 Anuran species from the Pantanal Wetland, Brazil. Comparative Parasitology 83, 92–100. doi: 10.1654/1525-2647-83.1.92.CrossRefGoogle Scholar
Campião, KM, Morais, DH, Dias, OT, Aguiar, A, Toledo, GM, Tavares, LER, and Silva, RJ (2014a) Checklist of helminth parasites of amphibians from South America. Zootaxa 3843, 1–93.CrossRefGoogle ScholarPubMed
Campião, KM, Silva, RJ, and Ferreira, VL (2014b) Helminth parasite communities of allopatric populations of the frog Leptodactylus podicipinus from Pantanal, Brazil. Journal of Helminthology 88, 13–19. doi: 10.1017/S0022149X12000557.CrossRefGoogle Scholar
Chakraborty, D, Reddy, M, Tiwari, S, and Umapathy, G (2019) Land use change increases wildlife parasite diversity in Anamalai Hills, Western Ghats, India. Scientific Reports 9, 11975. doi: 10.1038/s41598-019-48325-8.CrossRefGoogle ScholarPubMed
Chero, J, Cruces, C, Iannacone, J, Sáez, G, Alvariño, L, da Silva, RJ, and Morales, VR (2014) Gastrointestinal parasites in three species of Telmatobius (Anura: Telmatobiidae) in the high Andes, Peru. Neotropical Helminthology 8, 439–461.Google Scholar
Chero, J, Cruces, C, Iannacone, J, Sáez, G, Alvariño, L, Luque, J, and Morales, V (2016) Comunidad de helmintos parásitos del sapo espinoso Rhinella spinulosa (Wiegmann, 1834) (Anura: Bufonidae) de Perú. Revista de Investigaciones Veterinarias del Perú 27, 114–129.CrossRefGoogle Scholar
Climate-Data.Org Clima: Chapadinha. Available at https://pt.climate-data.org/america-do-sul/brasil/maranhao/chapadinha-44081/. Accessed January 11, 2021.Google Scholar
Combes, C (2001) Parasitism: the ecology and evolution of intimate interactions. Chicago and London, University of Chicago Press.Google Scholar
Duellman, WE and Trueb, L (1994) Biology of amphibians. Baltimore, Johns Hopkins University Press.CrossRefGoogle Scholar
Fernandez, JC and Ibarra, HG (1990) Acanthocephalus caspanensis n. sp. (Acanthocephala: Echinorhynchidae) parásito de Bufo spinulosus Wiegmann en el altiplano Chileno. Studies on Neotropical Fauna and Environment 25, 57–64. doi: 10.1080/01650529009360803.CrossRefGoogle Scholar
Frost, DR (2021) Amphibian species of the world: an online reference. Version 6.1. New York, American Museum of Natural History. Available at https://amphibiansoftheworld.amnh.org/index.php. Accessed May 20, 2021.Google Scholar
Goldberg, SR and Bursey, CR (2003) Helminths of two anuran species, Atelopus spurrelli (Bufonidae) and Dendrobates histrionicus (Dendrobatidae), from Colombia, South America. Parasitology International 52, 251–253.CrossRefGoogle Scholar
Goldberg, SR, Bursey, CR, Salgado-Maldonado, G, Báez, R, and Cañeda, C (2002) Helminth parasites of six species of anurans from Los Tuxtlas and Catemaco Lake, Veracruz, Mexico. Southwestern Naturalist 47, 293–299. doi: 10.2307/3672917.CrossRefGoogle Scholar
Gonzalez, CE and Hamann, MI (2006) Helmintos parásitos de Leptodactylus bufonius Boulenger, 1894 (Anura: Leptodactylidae) de Corrientes, Argentina. Revista Española de Herpetologia 20, 39–46.Google Scholar
Graça, RJ, Oda, FH, Lima, FS, Guerra, V, Gambale, PG, and Takemoto, RM (2017) Metazoan endoparasites of 18 anuran species from the mesophytic semideciduous Atlantic Forest in southern Brazil. Journal of Natural History 1–25. doi: 10.1080/00222933.2017.1296197.Google Scholar
Hamann, MI, González, CE, and Kehr, AI (2006) Helminth community structure of the oven frog Leptodactylus latinasus (Anura, Leptodactylidae) from Corrientes, Argentina. Acta Parasitologica 51, 294–299. doi: 10.2478/s11686-006-0045-1.CrossRefGoogle Scholar
Hamann, MI, Kehr, AI, and Gonzalez, CE (2010) Helminth community structure of Scinax nasicus (Anura: Hylidae) from a South American subtropical area. Diseases of Aquatic Organisms 93, 71–82.CrossRefGoogle ScholarPubMed
Hamann, MI, Kehr, AI, and González, CE (2012) Community structure of helminth parasites of Leptodactylus bufonius (Anura: Leptodactylidae) from northeastern Argentina. Zoological Studies 51, 1454–1463.Google Scholar
Hamann, MI, Kehr, AI, González, CE, Duré, MI, and Schaefer, EF (2009) Parasite and reproductive features of Scinax nasicus (Anura: Hylidae) from a South American subtropical area. Interciencia 34, 214–218.Google Scholar
Hernandez-Orts, JS, Kuchta, R, Semenas, L, Crespo, EA, Gonzalez, RA, and Aznar, FJ (2019) An annotated list of the Acanthocephala from Argentina. Zootaxa 4663(1), 1–64.CrossRefGoogle ScholarPubMed
Hoppe, EGL, Pedrassani, D, Hoffmann-Inocente, AC, Tebaldi, JH, Storti, LF, Zanuzzo, FS, Avancini, N, and Do Nascimento, AA (2008) Estudos ecológicos em taxocenoses helmintícas de Chaunus ictericus (Spix, 1824) e C. schneideri (Werner, 1894) (Anura: Bufonidae) simpátricos, capturados no distrito de São Cristóvão, município de Três Barras, Santa Catarina. Revista Brasileira de Parasitologia Veterinária 17, 166–169.Google Scholar
Janovy, JJ, Clopton, RE, Percival, TJ (1992) The roles of ecological and evolutionary influences in providing structure to parasite species assemblages. Journal of Parasitology 78, 630–640.CrossRefGoogle ScholarPubMed
Kennedy, CR (2006) Ecology of the Acanthocephala. New York, Cambridge University Press.CrossRefGoogle Scholar
Kiene, F, Andriatsitohaina, B, Ramsay, MS, Rakotondravony, R, Strube, C, and Radespiel, U (2021) Habitat fragmentation and vegetation structure impact gastrointestinal parasites of small mammalian hosts in Madagascar. Ecology and Evolution 11, 6766–6788. doi: 10.1002/ece3.7526.CrossRefGoogle ScholarPubMed
Leivas, PT, Leivas, FWT, and Campião, KM (2018) Diet and parasites of the anuran Physalaemus cuvieri Fitzinger, 1826 (Anura: Leiuperidae) from an Atlantic Forest fragment. Herpetology Notes 11, 109–113.Google Scholar
Martins-Sobrinho, PM, WGdO, Silva, EGd, Santos, GJBd, Moura, and JBd, Oliveira (2017) Helminths of some tree frogs of the families Hylidae and Phyllomedusidae in an Atlantic rainforest fragment, Brazil. Journal of Natural History 51, 1639–1648. doi: 10.1080/00222933.2017.1337945.CrossRefGoogle Scholar
McAllister, CT and Bursey, CR (2007) Some nematode and acanthocephalan parasites of the longnose leopard lizard, Gambelia wislizenii (Lacertilia: Crotaphytidae), from Arizona, California, and Texas, with a summary of the helminths reported from this host. Comparative Parasitology 74, 179–184. doi: 10.1654/4230.1.CrossRefGoogle Scholar
McAlpine, DF (1997) Helminth communities in bullfrogs (Rana catesbeiana), green frogs (Rana clamitans), and leopard frogs (Rana pipiens) from New Brunswick, Canada. Canadian Journal of Zoology 75, 1883–1890. doi: 10.1139/z97-818.CrossRefGoogle Scholar
McDonald, ME (1988) Key to Acanthocephala reported in waterfowl. Washington, DC, United States Fish and Wildlife Service.Google Scholar
Near, TJ (2002) Acanthocephalan phylogeny and the evolution of parasitism. Integrative and Comparative Biology 42, 668–677. doi: 10.1093/icb/42.3.668.CrossRefGoogle ScholarPubMed
Nielsen, C (2012) Animal evolution: interrelationships of the living phyla. 3rd edn. Oxford, Oxford University Press.Google Scholar
Oliveira, CR, Ávila, RW, and Morais, DH (2019) Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga biome, Brazil. Acta Parasitologica 64, 205–212. doi: 10.2478/s11686-018-00022-8.CrossRefGoogle ScholarPubMed
Oliveira, CR, Mascarenhas, W, Batista-Oliveira, D, de Castro Araújo, K, Ávila, RW, and Borges-Nojosa, DM (2022) Endoparasite community of anurans from an altitudinal rainforest enclave in a Brazilian semiarid area. Journal of Helminthology 96, e62.CrossRefGoogle Scholar
Oliveira, CR, Sousa, JGS, Carvalho, EFF, Ávila, RW, and DM, Borges‑Nojosa (2023) Effect of altitude and spatial heterogeneity on the host‑parasite relationship in anurans from a remnant humid forest in the brazilian semiarid. Parasitology Research 122, 2651–2666. doi:10.1007/s00436-023-07965-6.CrossRefGoogle ScholarPubMed
Palmer, JPS, Dib, LV, Lobão, LF, Pinheiro, JL, Ramos, RCF, Uchoa, CMA, Bastos, OMP, Silva, MEM, do Nascimento, JL, and Pissinatti, A (2020) Oncicola venezuelensis (Marteau, 1977) (Acanthocephala: Oligacanthorhynchidae) in Puma concolor in Rio de Janeiro, Brazil. Brazilian Journal of Veterinary Parasitology 29, e009620. doi: 10.1590/S1984-29612020046.Google ScholarPubMed
Paredes-Calderón, L, León-Règagnon, V, and García-Prieto, L (2004) Helminth infracommunities of Rana vaillanti Brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico. Journal of Parasitology 90, 692–696. doi: 10.1645/GE-226R.CrossRefGoogle ScholarPubMed
Parker, GA, Chubb, JC, Ball, MA, and Roberts, GN (2003) Evolution of complex life cycles in helminth parasites. Nature 425, 480–484.CrossRefGoogle ScholarPubMed
Perrot-Minnot, MJ, Cozzarolo, CS, Amin, O, Barčák, D, Bauer, A, Marijić, VF, … and Sures, B (2023) Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite 30(23).CrossRefGoogle ScholarPubMed
Pinhão, R, Wunderlich, AC, Alves dos Anjos, L, and Silva, RJ (2009) Helminths of toad Rhinella icterica (Bufonidae), from the municipality of Botucatu, São Paulo State, Brazil. Neotropical Helminthology 3, 35–40.Google Scholar
Pough, FH, Bemis, WE, McGuire, B, and Janis, CM (2023) Vertebrate life. 11th edn. New York, Oxford University Press.Google Scholar
Poulin, R, Krasnov, BR, Mouillot, D, and Thieltges, DW (2011) The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society B: Biological Sciences 366, 2379–2390. doi: 10.1098/rstb.2011.0048.CrossRefGoogle ScholarPubMed
Poulin, R and Mouillot, D (2005) Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511–514. doi: 10.1645/GE-398R.CrossRefGoogle ScholarPubMed
Queiroz, MS, Pontes, MR, Neto, MC, Campião, KM, and Anjos, LA (2020) Helminths of 8 anuran species from a remnant riparian forest in the Cerrado biome, Brazil. Herpetology Notes 13, 463–478.Google Scholar
Richardson, DJ (2013) Acanthocephala. Hoboken, NJ, John Wiley & Sons.CrossRefGoogle Scholar
Sampaio, NKS, Teixeira, AAM, Do Nascimento, JM, Ribeiro, SC, Almeida, WO, and Brito, SV (2022) Endoparasite community structure of an anuran assemblage in the Caatinga, Northeastern Neotropical Region. Journal of Helminthology 96(e78), 1–8. doi:10.1017/S0022149X22000682.CrossRefGoogle ScholarPubMed
Santos, VGT and Amato, SB (2010a) Helminth fauna of Rhinella fernandezae (Anura: Bufonidae) from the Rio Grande do Sul coastland, Brazil: analysis of the parasite community. Journal of Parasitology 96, 823–826. doi: 10.1645/GE-2388.1.CrossRefGoogle Scholar
Santos, VGT, Amato, SB, and Borges-Martins, M (2013) Community structure of helminth parasites of the “Cururu” toad, Rhinella icterica (Anura: Bufonidae) from southern Brazil. Parasitology Research 112, 1097–1103. doi: 10.1007/s00436-012-3236-8.CrossRefGoogle ScholarPubMed
Santos, VGT, Borges-Martins, M, and Amato, SB (2016) Community structure of parasites of the tree frog Scinax fuscovarius (Anura, Hylidae) from Campo Belo do Sul, Santa Catarina, Brazil. Neotropical Helminthology 10, 41–50.Google Scholar
Santos, VGTd and Amato, SB (2010b) Rhinella fernandezae (Anura, Bufonidae) a paratenic host of Centrorhynchus sp. (Acanthocephala, Centrorhynchidae) in Brazil. Revista Mexicana de Biodiversidad 81, 53–56.Google Scholar
Schaefer, EF, Hamann, MI, Kehr, AI, Gonzalez, CE, and Duré, MI (2006) Trophic, reproductive and parasitological aspects of the ecology of Leptodactylus chaquensis (Anura: Leptodactylidae) in Argentina. Herpetological Journal 16, 387–394.Google Scholar
Schmidt, GD (1985) Development and life cycles. in Crompton, DWT and Nickol, BB (Eds), Biology of the Acanthocephala. Cambridge, Cambridge University Press. 694Google Scholar
Sena, PA, Conceição, BM, Silva, PF, Silva, WG, Ferreira, WB, Júnior, VAS, Moura, GJB, and de Oliveira, JB (2018) Helminth communities of Pithecopus nordestinus (Anura: Phyllomedusidae) in forest remnants, Brazil. Herpetology Notes 11, 565–572.Google Scholar
Silva-Neta, AF, Alcantara, EP, Oliveira, CR, Carvalho, EFF, Morais, DH, Silva, RJ, and Ávila, RW (2020) Helminths associated with 15 species of anurans from the Ibiapaba plateau, northeastern Brazil. Neotropical Helminthology 14, 207–216. doi: 10.24039/rnh2020142795.Google Scholar
Silva, ALG, Martins, F, Santos, R, and JLS, Nunes (2008) Conservação da Reserva da Itamacaoca de Chapadinha/MA. in Selbach, JF and Leite, JRSA (Eds), Meio Ambiente no Baixo Parnaíba: olhos no mundo, pés na região. São Luís, Brazil, EDUFMA. 109–116Google Scholar
Silveira, EC, Mascarenhas, CS, Huckembeck, S, Müller, G, and Loebmann, D (2022) Parasitic helminths in Boana pulchella (Duméril & Bibron, 1841) (Anura: Hylidae) and their relation with host diet, body size, and habitat. Cuadernos de Herpetología 36, 155–167.Google Scholar
Smales, LR (2007a) Acanthocephala in amphibians (Anura) and reptiles (Squamata) from Brazil and Paraguay with description of a new species. Journal of Parasitology 93, 392–398. doi: 10.1645/GE-937R.1.CrossRefGoogle ScholarPubMed
Smales, LR (2007b) Acanthocephalans of amphibians and reptiles (Anura and Squamata) from Ecuador, with the description of Pandosentis napoensis n. sp (Neoechinorhynchidae) from Hyla fasciata. Zootaxa 1445, 49–56.CrossRefGoogle Scholar
Thieltges, DW, Jensen, KT, and Poulin, R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407–426. doi: 10.1017/S0031182007000248.CrossRefGoogle ScholarPubMed
Toledo, GM, Aguiar, A, Silva, RJ, and Anjos, LA (2013) Helminth fauna of two species of Physalaemus (Anura: Leiuperidae) from an undisturbed fragment of the Atlantic rainforest, Southeastern Brazil. Journal of Parasitology 99. doi: 10.1645/GE-3212.1.CrossRefGoogle ScholarPubMed
Toledo, GDM, Fonseca, MG, Iannacone, J, Cardenas Callirgos, JM, Pineda Castillo, C, and da Silva, RJ (2017) Infection with Pseudoacanthocephalus lutzi (Hamann, 1891) (Acanthocephala: Echinorhynchidae) in Rhinella marina (Linnaeus, 1758) (Amphibia: Bufonidae) in Peru. Neotropical Helminthology 11, 405–411.Google Scholar
Toledo, GM, Schwartz, HO, Nomura, HAQ, Aguiar, A, Velota, RAMV, Silva, RJ, and Anjos, LA (2017) Helminth community structure of 13 species of anurans from Atlantic rainfores tremnants, Brazil. Journal of Helminthology 92, 438–444. doi: 10.1017/S0022149X17000608.CrossRefGoogle Scholar
Torres, P and Puga, S (1996) Occurrence of cystacanths of Centrorhynchus sp. (Acanthocephala: Centrorhynchidae) in toads of the genus Eupsophus in Chile. Memorias do Instituto Oswaldo Cruz 91, 717–719.CrossRefGoogle ScholarPubMed
Valdujo, PH, Silvano, DL, Colli, G, and Martins, M (2012) Anuran species composition and distribution patterns in Brazilian Cerrado, a Neotropical hotspot. South American Journal of Herpetology 7, 63–78. doi: 10.2994/057.007.0209.CrossRefGoogle Scholar
Van Cleave, HJ (1923) A key to the genera of Acanthocephala. Transactions of the American Microscopical Society 42, 184–191.CrossRefGoogle Scholar
Velazquez-Urrieta, MY and León-Règagnon, V (2018) Helminths of two species of leopard frogs (Amphibia: Ranidae) from Chiapas, Mexico. Comparative Parasitology 85, 141–152. doi: 10.1654/1525-2647-85.2.141.CrossRefGoogle Scholar