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Helminths associated with Norops fuscoauratus (Squamata, Dactyloidae) in highland marshes of the Brazilian semi-arid
Published online by Cambridge University Press: 11 May 2020
Abstract
Helminthological studies may contribute with valuable information on host biology and conservation. Herein, we provide new data on helminths infecting the lizard Norops fuscoauratus, testing one of the factors considered most important in parasitic ecology: host size. We analysed 25 specimens of N. fuscoauratus from three highland marshes in the Brazilian semi-arid. Eight taxa of helminths belonging to Nematoda, Trematoda and Acanthocephala were found. Physaloptera sp. showed the higher prevalence (40%), with a mean intensity of infection of 3.3 ± 1.46 (1–16) and mean abundance 1.32 ± 0.65 (0–16). Norops fuscoauratus represents four new host records for the helminths Cyrtosomum sp., Pharyngodon travassosi, Strongyloides sp. and Centrorhynchus sp. There is no relationship of host body size (P = 0.79) and mass (P = 0.50) with parasite richness. In addition, the present study contributes to the knowledge of the parasitic fauna of N. fuscoauratus and the Neotropical region.
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References
Adelman, JS and Martin, LB (2009) Vertebrate sickness behaviors: adaptive and integrated neuroendocrine immune responses. Integrative and Comparative Biology 49, 202–214.CrossRefGoogle ScholarPubMed
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
Aho, JM (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding pattern and process. pp. 157–195in Esch, GW, Bush, AO and Aho, JM (Eds) Parasite communities: patterns and processes. London, Chapman and Hall.CrossRefGoogle Scholar
Albuquerque, S, Ávila, RW and Bernarde, PS (2012) Occurrence of helminths in lizards (Reptilia: Squamata) at lower Moa river forest, Cruzeiro do Sul, Acre, Brazil. Comparative Parasitology 79, 64–68.CrossRefGoogle Scholar
Amorim, DM and Ávila, RW (2019) Infection patterns of helminths in Norops brasiliensis (Squamata, Dactyloidae) from a humid forest, northeastern Brazil and their relation with body mass, sex, host size, and season. Helminthologia 56, 168–174.CrossRefGoogle ScholarPubMed
Anderson, RC (2000) Nematode parasites of vertebrates, their development and transmission. 2nd edn. 650 pp. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the nematode parasites of vertebrates. 463 pp. London, U.K., Archival Volume, CABI Publishing.CrossRefGoogle Scholar
Anjos, LA, Rocha, CFD, Vrcibradic, D and Vicente, JJ (2005) Helminths of the exotic lizard Hemidactylus mabouia from a rock outcrop area in southeastern Brazil. Journal of Helminthology 79, 307–313.CrossRefGoogle ScholarPubMed
Anjos, LA, Bezerra, CH, Passos, DC, Zanchi, D and Galdino, CAB (2011) Helminth fauna of two gecko lizards, Hemidactylus agrius and Lygodactylus klugei (Gekkonidade) from Caatinga biome, northeastern Brazil. Neotropical Helminthology 5, 285–290.Google Scholar
Araujo Filho, JA, Ribeiro, SC, Brito, SV, Teles, DA, Sousa, JGG, Ávila, RW and Almeida, WO (2014) Parasitic nematodes of Polychrus acutirostris (Polychrotidae) in the Caatinga biome, northeastern Brazil. Brazilian Journal of Biology 74, 939–942.CrossRefGoogle ScholarPubMed
Araujo Filho, JA, Brito, SV, Lima, VF, Pereira, AMA, Mesquita, DO, Albuquerque, RL and Almeida, WO (2016) Influence of temporal variation and host condition on helminth abundance in the lizard Tropidurus hispidus from north-eastern Brazil. Journal of Helminthology 91, 312–319.CrossRefGoogle Scholar
Avila-Pires, TCS (1995) Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen 299, 1–706.Google Scholar
Ávila, RW and Silva, RJ (2010) Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. The Journal of Venomous Animals and Toxins including Tropical Diseases 16, 543–572.CrossRefGoogle Scholar
Ávila, RW and Silva, RJ (2013) Helminths of lizards from the municipality of Aripuana in the southern Amazon region of Brazil. Journal of Helminthology 87, 12–16.CrossRefGoogle ScholarPubMed
Ávila, RW, Cardoso, MW, Oda, FH and Silva, RJ (2011) Helminths from lizards (Reptilia: Squamata) at the Cerrado of Goiás state, Brazil. Comparative Parasitology 78, 120–129.CrossRefGoogle Scholar
Ávila, RW, Anjos, LA, Ribeiro, SC, Morais, DH, Silva, RJ and Almeida, WO (2012) Nematodes of lizards (Reptilia: Squamata) from Caatinga biome, northeastern Brazil. Comparative Parasitology 79, 56–64.CrossRefGoogle Scholar
Barreto-Lima, AF, Toledo, GM and Anjos, LA (2011) The nematode community in the Atlantic rainforest lizard Enyalius perditus Jackson, 1978 from south-eastern Brazil. Journal of Helminthology 86, 395–400.CrossRefGoogle Scholar
Bezerra, CH, Pinheiro, LT, Melo, GC, Braga, RR, Anjos, LA and Borges-Nojosa, DM (2020) How epidemiological patterns shift across populations in an exotic lizard. Journal of Helminthology 94, 1–6.CrossRefGoogle Scholar
Brito, SV, Ferreira, FS, Ribeiro, SC, Anjos, LA, Almeida, WO, Mesquita, DO and Vasconcellos, A (2014a) Spatial-temporal variation of parasites in Cnemidophorus ocellifer (Teiidae) and Tropidurus hispidus and Tropidurus semitaeniatus (Tropiduridae) from Caatinga areas in northeastern Brazil. Parasitology Research 113, 1163–1169.CrossRefGoogle Scholar
Brito, SV, Corso, G, Almeida, AM, Ferreira, FS, Almeida, WO, Anjos, LA and Vasconcellos, A (2014b) Phylogeny and micro-habitats utilized by lizards determine the composition of their endoparasites in the semiarid Caatinga of Northeast Brazil. Parasitology Research 113, 3963–3972.CrossRefGoogle Scholar
Brooks, DR, León-Règagnon, V, McLennan, DA and Zelmer, D (2006) Ecological fitting as a determinant of the community structure of Platyhelminth parasites of anurans. Ecology 87, S76–S85.CrossRefGoogle ScholarPubMed
Bursey, CR, Goldberg, SR Jr and Telford, SR (2003) Rhabdias anolis n. sp.(Nematoda: Rhabdiasidae) from the lizard, Anolis frenatus (Sauria: Polychrotidae), from Panama. Journal of Parasitology 89, 113–117.CrossRefGoogle Scholar
Bursey, CR, Goldberg, SR and Miller, CL (2004) Two new species of Falcaustra and comments on helminths of Norops tropidolepis (Sauria: Polychrotidae) from Costa Rica. Journal of Parasitology 90, 598–603.CrossRefGoogle ScholarPubMed
Bursey, CR, Goldberg, SR and Parmelee, JR (2005) Gastrointestinal helminths from 13 species of lizards from Reserva Cuzco Amazónico, Peru. Comparative Parasitology 72, 50–69.CrossRefGoogle Scholar
Bursey, CR, Goldberg, SR, Telford, SR and Vitt, LJ (2012) Metazoan endoparasites of 13 species of Central American anoles (Sauria: Polychrotidae: Anolis) with a review of the helminth communities of Caribbean, Mexican, North American, and South American anoles. Comparative Parasitology 79, 75–133.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Cabral, AN, Teles, DA, Brito, SV, Oliveira Almeida, W, Anjos, LA, Guarnieri, MC and Ribeiro, SC (2018) Helminth parasites of Mabuya arajara Rebouças-Spieker, 1981 (Lacertilia: Mabuyidae) from Chapada do Araripe, northeastern Brazil. Parasitology Research 117, 1185–1193.CrossRefGoogle ScholarPubMed
Cabrera-Guzmán, E and Garrido-Olvera, L (2014) Helminth parasites of the Lesser Scaly Anole, Anolis uniformis (Squamata: Dactyloidae), from Los Tuxtlas, Southern Mexico: evidence of diet and habitat use. South American Journal of Herpetology 9, 183–190.CrossRefGoogle Scholar
Campião, KM, Morais, DH, Dias, OT, Aguiar, A, Toledo, G, Tavares, LER and Silva, RJ (2014) Checklist of helminth parasites of amphibians from South America. Zootaxa 3843, 1–93.CrossRefGoogle ScholarPubMed
Campião, KM, Aquino Ribas, AC, Morais, DH, Silva, RJ and Tavares, LER (2015) How many parasites species a frog might have? Determinants of parasite diversity in South American anurans. PLoS ONE 10, 1–12.CrossRefGoogle ScholarPubMed
Cardia, DFF, Camossi, LG, Fornazari, F, Babboni, SD, Teixeira, CR and Bresciani, KDS (2016) First report of Strongyloides sp.(Nematoda, Strongyloididae) in Lutreolina crassicaudata (Didelphimorphia: Didelphidae). Brazilian Journal of Biology 76, 884–887.CrossRefGoogle Scholar
Carvalho-Pereira, T, Souza, FN, Santos, LR, Walker, R, Pertile, AC, Oliveira, DS and Reis, MG (2018) The helminth community of a population of Rattus norvegicus from an urban Brazilian slum and the threat of zoonotic diseases. Parasitology 145, 797–806.CrossRefGoogle ScholarPubMed
Dobson, AP, Pacala, SV, Roughgarden, JD, Carper, ER and Harris, EA (1992) The parasites of Anolis lizards in the northern Lesser Antilles. Oecologia 91, 110–117.CrossRefGoogle ScholarPubMed
Fournié, G, Goodman, SJ, Cruz, M, et al. (2015) Biogeography of parasitic nematode communities in the Galápagos giant tortoise: implications for conservation management. PLoS ONE 10, 1–18.CrossRefGoogle ScholarPubMed
Galdino, CA, Ávila, RW, Bezerra, CH, Passos, DC, Melo, GC and Zanchi-Silva, D (2014) Helminths infection patterns in a lizard (Tropidurus hispidus) population from a semiarid Neotropical area: associations between female reproductive allocation and parasite loads. Journal of Parasitology 100, 864–867.CrossRefGoogle Scholar
Gibbons, IM (2010) Keys to the nematode parasites of vertebrates. Supplementary volume. 416 pp. London, CABI Publishing.Google Scholar
Goldberg, SR and Bursey, CR (2008) Helminths from fifteen species of frogs (Anura, Hylidae) from Costa Rica. Phyllomedusa 7, 23–33.CrossRefGoogle Scholar
Goldberg, SR, Bursey, CR and Vitt, LJ (2006a) Helminths of the brown-eared anole, Norops fuscoauratus (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Phyllomedusa. Journal of Helminthology 5, 83–86.Google Scholar
Goldberg, S, Bursey, C and Vitt, L (2006b) Parasites of two lizard species, Anolis punctatus and Anolis transversalis (Squamata: Polychrotidae) from Brazil and Ecuador. Amphibia-Reptilia 27, 575–579.Google Scholar
Goldberg, SR, Bursey, CR and Vitt, LJ (2010) Helminths from three species of anoles: the humble anole, Anolis humilis; the border anole, Anolis limifrons; and the lion anole, Anolis lionotus (Squamata: Polychrotidae), from Nicaragua. Comparative Parasitology 77, 242–247.CrossRefGoogle Scholar
Ibrahim, MM and Soliman, MFM (2005) Factors affecting helminths community structure of the Egyptian lizard Chalcides ocellatus (Forskal, 1775). Parasite 12, 317–323.CrossRefGoogle Scholar
Ipece (2018a) Instituto de Pesquisa e Estratégia Econômicas do Ceará. Perfil municipal Ubajara. Disponível em. Available at https://www.ipece.ce.gov.br/wpcontent/uploads/sites/45/2018/09/Ubajara_2017.pdf (accessed 5 September 2019).Google Scholar
Ipece (2018b) Instituto de Pesquisa e Estratégia Econômicas do Ceará. Perfil municipal Maranguape. Disponível em. Available at https://www.ipece.ce.gov.br/wp-content/uploads/sites/45/2018/09/Maranguape_2017.pdf (accessed 5 September 2019).Google Scholar
Ipece (2018c) Instituto de Pesquisa e Estratégia Econômicas do Ceará. Perfil municipal Guaramiranga. Disponível em. Available at https://www.ipece.ce.gov.br/wp-content/uploads/sites/45/2018/09/Guaramiranga_2017.pdf (accessed 5 September 2019).Google Scholar
Jorge, F and Poulin, R (2018) Poor geographical match between the distributions of host diversity and parasite discovery effort. Proceedings of the Royal Society B 285, 20180072.CrossRefGoogle ScholarPubMed
Kamiya, T, O'Dwyer, K, Nakagawa, S and Poulin, R (2014) What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Reviews 89, 123–134.CrossRefGoogle ScholarPubMed
Kelehear, C, Saltonstall, K and Torchin, ME (2019) Negative effects of parasitic lung nematodes on the fitness of a Neotropical toad (Rhinella horribilis). Parasitology 146, 928–936.CrossRefGoogle Scholar
Koprivnikar, J, Marcogliese, DJ, Rohr, JR, Orlofske, SA, Raffel, TR and Johnson, PTJ (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9, 342–360.CrossRefGoogle ScholarPubMed
Kuzmin, Y (2013) Review of Rhabdiasidae (Nematoda) from the Holarctic. Zootaxa 3639, 1–76.CrossRefGoogle ScholarPubMed
Loebmann, D and Haddad, CFB (2010) Amphibians and reptiles from a highly diverse area of the Caatinga domain: composition and conservation implications. Biota Neotropica 10, 227–256.CrossRefGoogle Scholar
Luque, JL, Pereira, FB, Alves, PV, Oliva, ME and Timi, JT (2016) Helminth parasites of South American fishes: current status and characterization as a model for studies of biodiversity. Journal of Helminthology 91, 150–164.CrossRefGoogle ScholarPubMed
Marcogliese, DJ (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1, 151–164.CrossRefGoogle Scholar
Martin, JE, Llorente, GA, Roca, V, Carretero, MA, Montori, A, Santos, X and Romeu, R (2005) Relationship between diet and helminths in Gallotia caesaris (Sauria: Lacertidae). Zoology 108, 121–130.CrossRefGoogle Scholar
Mati, VLT, Pinto, HÁ and Melo, AL (2013) Strongyloides cruzi (Rhabditida: Strongyloididae) in Ophiodes Striatus (Squamata: Anguidae) from Brazil: new host and locality records with taxonomic comments on Strongyloides of Lizards. Neotropical Helminthology 7, 327–333.Google Scholar
Mihalca, AD, Micl˘uş, V and Lefkaditis, M (2010) Pulmonary lesions caused by the nematode Rhabdias fuscovenosa in a grass snake, Natrix natrix. Journal of Wildlife Diseases 46, 678–681.CrossRefGoogle Scholar
Müller, MI, Morais, DH, Costa-Silva, GJ, Aguiar, A, Ávila, RW and Silva, RJ (2018) Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): evidence for cryptic speciation. Zoologica Scripta 47, 1–13.CrossRefGoogle Scholar
Oitaven, LPC, Silva Ribeiro, F, Moura, GJB and Oliveira, JB (2019) Parasites of Gymnodactylus darwinii Gray, 1845 (Squamata, Phyllodactylidae) from an Atlantic Rainforest fragment. Acta Tropica 192, 123–128.CrossRefGoogle Scholar
Oliveira, BHS, Teixeira, AAM, Queiroz, RNM, Araujo-Filho, JA, Teles, DA, Brito, SV and Mesquita, DO (2017) Nematodes infecting Anotosaura vanzolinia (Squamata: Gymnophthalmidae) from Caatinga, northeastern Brazil. Acta Herpetologica 12, 103–108.Google Scholar
Pagano, MC and Araújo, FS (2010) Semiarid vegetation in Brazil: biodiversity, impacts and management. pp. 99–114in Degenovine, KM (Ed.) Semi-arid environments: agriculture, water supply and vegetation. New York, Nova Publishers.Google Scholar
Pianka, ER and Vitt, LJ (2003) Lizards: windows to the evolution of diversity. 343 pp. Berkeley, University of California Press.Google Scholar
Poulin, R (2004) Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423–434.CrossRefGoogle Scholar
Poulin, R (2005) Structure of parasite communities. pp. 309–315in Rohde, K (Ed.) Marine parasitology. Wallingford, CABI Publishing.Google Scholar
Poulin, R and George-Nascimento, M (2007) The scaling of total parasite biomass with host body mass. International Journal for Parasitology 37, 359–364.CrossRefGoogle ScholarPubMed
Preston, D and Johnson, P (2012) Ecological consequences of parasitism. Nature Education Knowledge 3, 47.Google Scholar
R Core Team (2018) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing, Available at https://www.r-project.org/ (accessed 5 October 2019).Google Scholar
Ribeiro-Junior, MA (2015) Catalogue of distribution of lizards (Reptilia: Squamata) from the Brazilian Amazonia. I. Dactyloidae, Hoplocercidae, Iguanidae, Leiosauridae, Polychrotidae, Tropiduridae. Zootaxa 3983, 1–110.CrossRefGoogle ScholarPubMed
Ribeiro, SC, Ferreira, FS, Brito, SV, Teles, DA, Ávila, RW, Almeida, WO and Guarnieri, M (2012) Pulmonary infection in two sympatric lizards, Mabuya arajara (Scincidae) and Anolis brasiliensis (Polychrotidae) from a cloud forest in Chapada do Araripe, Ceará, Northeastern Brazil. Brazilian Journal of Biology 72, 929–933.CrossRefGoogle ScholarPubMed
Roca, V and Hornero, MJ (1992) Podarcis pityusensis (Sauria: Lacertidae). Folia Parasitologica 39, 369–373.Google Scholar
Silva, LA, Manoel, PS, Uieda, VS, Ávila, RW and Silva, RJD (2019) Spatio-temporal variation in diet and its association with parasitic helminths in Ameivula pyrrhogularis (Squamata: Teiidae) from northeast. Herpetological Conservation And Biology 14, 325–336.Google Scholar
Silva Neta, AF and Ávila, RW (2018) Helminths of the lizard Colobosauroides cearensis (Squamata, Gymnophthalmidae) in an area of Caatinga, northeastern Brazil. Acta Herpetologica 13, 95–100.Google Scholar
Souza, GT, Ribeiro, TS, Antonucci, AM, Ueda, BH, Carniel, MK, Karling, LC and Pavanelli, GC (2015) Endoparasite fauna of wild capybaras (Hydrochoerus hydrochaeris) (Linnaeus, 1766) from the Upper Parana River floodplain, Brazil. Aquatic Mammals 41, 213–221.CrossRefGoogle Scholar
Teixeira, AAM, Brito, SV, Teles, DA, Ribeiro, SC, Araujo-Filho, JA, Lima, VF and Almeida, WO (2017) Helminths of the lizard Salvator merianae (Squamata, Teiidae) in the caatinga, northeastern Brazil. Brazilian Journal of Biology 77, 312–317.CrossRefGoogle ScholarPubMed
Teixeira, AAM, Silva, RJ, Brito, SV, Teles, DA, Araujo-Filho, JA, Franzini, LD, Mesquita, DO, et al. (2018) Helminths infecting Dryadosaura nordestina (Squamata: Gymnophthalmidae) from Atlantic Forest, northeastern Brazil. Helminthologia 55, 286–291.CrossRefGoogle ScholarPubMed
Vicente, JJ, Rodrigues, HO, Gomes, DC and Pinto, RM (1991) Nematóides do Brasil. 2a parte: nematóides de Anfíbios. Revista Brasileira de Zoologia 7, 549–626.CrossRefGoogle Scholar
Vitt, LJ, Avila-Pires, TCS, Zani, PA, Sartorius, SS and Espósito, MC (2003) Life above ground: ecology of Anolis fuscoauratus in the Amazon rain forest, and comparisons with its nearest relatives. Canadian Journal of Zoology 81, 142–156.CrossRefGoogle Scholar
Vitt, LJ, Magnusson, WE, Avila-Pires, TCS and Lima, AP (2008) Guide to the lizards of Reserva Adolpho Ducke, central Amazonia. 176 pp. Manaus, Áttema Design Editorial.Google Scholar
Yamaguti, S (1961) Systema helminthum - nematodes. Vol. III. Part I e II. London, Interscience Publishers.Google Scholar
Yamaguti, S (1963) Systema helminthum - acanthocephalans. Vol. V. 423 pp. London, Interscience Publishers.Google Scholar