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

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Summary

Climatic and ecological factors can influence the parasite load of a host. Variation in rainfall, body size, and sex of the hosts may be related to the abundance of parasites. This study investigated the helminth fauna associated with a population of Norops brasiliensis, together with the effect of host biology (sex, body size, and mass) and variation in rainfall regime on the abundance of helminths. Species of three groups of endoparasites were found (Nematoda, Cestoda, and Trematoda), with nematodes as the most representative taxa with eight species, prevalence of 63.2 %, mean intensity of 4.0 ± 0.58 (1 – 25), and mean abundance of 2.66 ± 0.44 (0 – 25). Nine helminth species are new host records for N. brasiliensis. The nematode Rhabdias sp. had the highest prevalence (53.3 %). There was no significant relationship between abundance of the trematode Mesocoelium monas and host sex or season, although the abundance of this parasite increased significantly with host body size and mass, while abundance of nematodes was related to season and host mass. This study increases the knowledge about the diversity of helminth fauna associated with N. brasiliensis, revealing infection levels of hosts from northeastern Brazil.

Aho, J.M. (1990): Helminth communities of amphibians and reptiles: comparative approaches to understanding pattern and process. In: Esch GW, Bush AO, Aho JM (eds) Parasite communities: patterns and processes. Chapman and Hall, London, pp 157 – 195

Amo, L. Fargalo, J.A., Martinez-Padilla J., Millán J., López, P., Martín, J. (2005): Prevalence and intensity of blood and intestinal parasites in a field population of a Mediterranean lizard, Lacerta lepida. Parasitol. Res., 96(6): 413-417. DOI: 10.1007/s00436-005-1355-1

Almeida, W.O., Ribeiro, S.C., Santana, G.G., Vieira, W.L.S., Anjos., L.A., Sales, D.L. (2009): Lung infection rates in two sympatric Tropiduridae lizard species by pentastomids and nematodes in northeastern Brazil. Braz. J. Biol., 69: 963 – 967. DOI: 10.1590/S1519-69842009000400027

Amorim, D.M., Silva, L.A.F., Morais, D.H., Silva, R.J., Ávila, R.W. (2017): Aplectana nordestina n. sp. (Nematoda: Cosmocercidae) parasitizing Leposternon polystegum (Squamata: Amphisbaenidae) from Northeastern, Brazil. Zootaxa., 4247: 83 – 88. DOI: 10.11646/zootaxa.4247.1.12

Anderson, R.C. (2000): Nematode Parasites of Vertebrates, their Development and Transmission. 2nd Edition, Walingford, UK, CABI Publishing, 650 pp.

Araújo-Filho, J.A., Brito, S.V., Lima, V.F., Pereira, A.M.A., Mesquita, D.O., Albuquerque, R.L., Almeida, W.O. (2016): Influence of temporal variation and host condition on helminth abundance in the lizard Tropidurus hispidus from north-eastern Brazil. J. Helminthol., 4:1 – 8. DOI: 10.1017/S0022149X16000225

Ávila, RW, Cardoso, M.W., Oda, F.H., Silva, R.J. (2011): Helminths from lizards (Reptilia: Squamata) at the Cerrado of Goiás state, Brazil. Comp. Parasitol., 78(1):120 – 128. DOI: 10.1654/4472.1

Ávila, R.W., Silva, R.J. (2013): Helminths of lizards from the municipality of Aripuanã in the southern Amazon region of Brazil. J. Helminthol., 87(01):12 – 16. DOI: 10.1017/S0022149X11000769

Ávila, R.W., Silva, R.J. (2010): Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. J. Venom. Anim. Toxins. Incl. Trop. Dis. 16:1 – 30. DOI: 10.1590/S1678-91992010000400005

Ávila, R.W., Anjos, L.A., Ribeiro, S.C., Morais, D.H., Silva, R.J., Almeida, W.O. (2012): Nematodes of lizards (Reptilia: Squamata) from Caatinga biome, northeastern Brazil. Comp. Parasitol., 79(1):56 – 63. DOI: 10.1654/4518.1

Ávila-Pires, T.C.S. (1995): Lizards of Brazilian Amazonia (Reptilia: Squamata). Zool. Verh., 299: 1 – 706

Brito, S.V., Ferreira, F.S., Ribeiro, S.C., Anjos, L.A., Almeida, W.O., Mesquita, D.O., Vasconcellos, A. (2014): Spatial-temporal variation of parasites in Cnemidophorus ocellifer (Teiidae) and Tropidurus hispidus and Tropidurus semitaeniatus (Tropiduridae) from Caatinga areas in northeastern Brazil. Parasitol. Res., 113:1163 – 1169. DOI: 10.1007/s00436-014-3754-7

Bush, A.O., Laferty, K.D., Lotz, J.M., Shostak, A.W. (1997): Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol., 83(4): 575 – 583. DOI: 10.2307/3284227

Bursey, C.R., Goldberg, S.R., Vitt, L.J. (2007): New species of Rhabdias (Nematoda: Rhabdiasidae) and other helminths from Norops capito (Sauria: Polychrotidae) from Nicaragua. J. Parasitol., 93: 129 – 131. DOI: 10.1645/GE-887R.1

Cabral, N.A., Teles, D.A., Brito, S.V., Almeida, W.O., Anjos, L.A., Guarnieri, M.C., Ribeiro, S.C. (2018): Helminth parasites of Mabuya arajara Rebouças-Spieker, 1981 (Lacertilia: Mabuyidae) from Chapada do Araripe, northeastern Brazil. Parasitol. Res., 117(4), 1185-1193. DOI: 10.1007/s00436-018-5797-7

Cabrera-Guzmán, E., 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. S. Am. J. Herpetol., 9: 183 – 189. DOI: 10.2994/SAJH-D-14-00035.1

Campião, K.M., Morais, D.H., Dias, O.T., Aguiar, A., Toledo, G., Tavares, L.E.R., Silva, R.J. (2014): Checklist of helminth parasites of amphibians from South America. Zootaxa 3843: 1 – 93. DOI: 10.11646/zootaxa.3843.1.1

Dorigo, T. A., Maia-Carneiro, T., Almeida-Gomes, M., Siqueira, C.C., Vrcibradic, D., Van Sluys, M., Rocha, C.F.D. (2014): Diet and helminths of Enyalius brasiliensis (Lacertilia, Iguania, Leiosauridae) in an Atlantic Rainforest remnant in southeastern Brazil. Brazil. Braz. J. Biol., 74: 199 – 204. DOI: 10.1590/1519-6984.07612

Escudero, M.B., Murillo, S.A. (2007): Tremátodos Digéneos de Chaunus marinus (Anura: Bufonidae) en el Municipio de Quibdó, Chocó [Digenetic Trematodes of Chaunus marinus (Anura: Bufonidae) in the Quibdó Municipality, Chocó]. Rer. Inst Univ Tecnol del Chocó Investig Biodivers y Desarrollo., 26: 13 – 17. DOI: 10.18636/biodesarrollo.v26i2.475 (In Spanish)

Franco, L.F., Salomão, M.G. (2002): Técnicas de coleta e preparação de vertebrados para fins científicos e didáticos [Techniques collection and preparation of vertebrates for scientific and educational purposes]. São Paulo: Instituto Pau Brasil de História Natural. 348 pp. (In Portuguese)

Fundação Cearense de Meteorologiae Recursos Hídricos (2016): Funceme [Foundation of Meteorology and Hydric Resources of Ceará State]. In: Zoneamento Geoambiental do Ceará: Mesorregião do Sul cearense [Geoenvironmental zoning of Ceará state: southern Mesor-region of Ceará]. Retrieved December 26, 2018 from http://www.funceme.br/ Retrieved December 26, 2018 (In Portuguese)

George-Nascimento, M., Muñoz, G., Marquet, P.A., Poulin, R. (2004): Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecology Letters., 7: 527 – 531. DOI: 10.1111/j.1461-0248.2004.00609.x

Goldberg, S.R., Bursey, C.R., Vitt, L.J. (2006): Parasites of two lizard species, Anolis punctatus and Anolis transversalis (Squamata: Polychrotidae) from Brazil and Ecuador. Amphibia–Reptilia., 27: 575 – 579. DOI: 10.1163/156853806778877068

Hafer, N., Milinski, M. (2016): Inter-and intraspecific conflicts between parasites over host manipulation. Proc. R. Soc., B 28: 1 – 9. DOI: /10.1098/rspb.2015.2870

Huey, R.B., Pianka, E.R. (1981): Ecological consequences of foraging mode. Ecology 62: 991 – 999. DOI: 10.2307/1936998

Ipece – Instituto de Pesquisa e Estatística Econômica do Ceará [Institute of Research and Economic Strategy of Ceará] (2015): Perfil básico municipal: Crato [Basic profile of the municipality of Crato]. Retrieved November 07, 2017 from http://www.ipece.ce.gov.br/perfil_basico_municipal/2016/Aiuaba.pdf (In Portuguese)

Lozano, G.A. (1991): Optimal foraging theory: a possible role for parasites. Oikos., 60: 391 – 395. DOI: 10.1111/ecog.01720

Macedo, L.C., Gardner, S.L., Melo, F.T.V., Giese, E.G., Santos, J.N. (2017): Nematodes Parasites of Teiid Lizards from the Brazilian Amazon Rainforest. J. Parasitol., 103(2), 176 – 182. DOI: 10.1645/16-69

Maia-Carneiro, T., Motta-Tavares, T., Ávila, R.W., Rocha, C.F. (2017): Helminth infections in a pair of sympatric congeneric lizard species. Parasitol. Res., 1 – 8. DOI: 10.1007/s00436-017-5672-y

Martin, L.B., Weil, Z.M., Nelson, R.J. (2008): Seasonal changes in vertebrate immune activity: mediation by physiological tradeoffs. Philos. T. R. Soc. B., 363(1490): 321 – 339. DOI: 10.1098/rstb.2007.2142

Mesquita, D.O., Costa, G.C., Figueredo, A.S., França, F.G., Garda, A.A., Bello Soares, A.H., Werneck, F.P. (2015): The autecology of Anolis brasiliensis (Squamata, Dactyloidae) in a Neotropical Savanna. Herpetol. J., 25: 233 – 244

Oliveira, B.H.S., Teixeira, A.A.M., Queiroz, R.N.M., Araujo-Filho, J.A., Teles, D.A., Brito, S.V., Mesquita, D.O. (2017): Nematodes infecting Anotosaura vanzolinia (Squamata: Gymnophthalmidae) from Caatinga, northeastern Brazil. Acta Herpetol., 12: 103 – 108. DOI: 10.13128/Acta_Herpetol-18765

Pereira, F.B., Gomides, S.C., Sousa, B.M., De Souza Lima, S., Luque, J.L. (2012): The relationship between nematode infections and ontogeny and diet of the lizard Tropidurus torquatus (Wied, 1820) (Squamata: Tropiduridae) from the Atlantic Rainforest in south-eastern Brazil. J. Helminthol., 87: 364 – 370. DOI: 10.1017/S0022149X12000466

Poulin, R., George-Nascimento, M. (2007): The scaling of total parasite biomass with host body mass. Int. J. Parasitol., 37: 359 – 364. DOI: 10.1016/j.ijpara.2006.11.009

R Development Core Team R. (2012): A language and environment for statistical computing: R Foundation for Statistical Computing version 2.15.1 [computer software]. Austria. URL http://nbcgib.uesc.br/mirrors/cran/

Ribeiro, S.C., Ferreira, F.S., Brito, S.V., Teles, D.A., Ávila, R.W., Almeida, W.O., Anjos, L.A., Guarnieri, M.C. (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. Braz. J. Biol., 72(4):929 – 933. DOI: 10.1590/S1519-69842012000500021

Roberts, M.L., Buchanan, K.L., Evans, M.R. (2004): Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim. Behav., 68(2):227 – 239. DOI: 10.1016/j.anbehav. 2004.05.001

Roberto, I.J., Loebmann, D. (2016): Composition, distribution patterns, and conservation priority areas for the herpetofauna of the state of Ceará, northeastern Brazil. Salamandra., 52: 134 – 152.

Roca, V., Galdón, M.A. (2010): Haemogregarine blood parasites in the lizards Podarcis bocagei (Seoane) and P. carbonelli (Pérez-Mellado) (Sauria: Lacertidae) from NW Portugal. Syst. Parasitol., 75: 75 – 79. DOI: 10.1007/s11230-009-9206-6

Sowemimo, O.A., Oluwafemi, T.A. (2017): A Survey of Helminth Parasites of the Lizard, Agama agama in Ile–Ife and Ibadan Southwest Nigeria. J. Bacteriol. Parasitol., 8: 1 – 6

Thomas, F., Poulin, R., Brodeur, J. (2010): Host manipulation by parasites: a multidimensional phenomenon. Oikos., 119: 1217 – 1223. DOI: 10.1111/j.1600-0706.2009.18077.x

Vanzolini, P.E., Williams, E.E. (1970): South American anoles: the geographic differentiation and evolution of the Anolis chrysolepis species group (Sauria, Iguanidae). Arq. Zool., 19: 1 – 298

Vitt, L.J., Shepard, D.B., Vieira, G.H., Caldwell, J.P., Colli, G.R., Mesquita, D.O. (2008): Ecology of Anolis nitens brasiliensis in Cerrado woodlands of Cantao. Copeia., 2008: 144 – 153. DOI: 10.1643/CP-06-251

Vrcibradic, D., Vicente, J.J., Bursey, C.R. (2007): Helminths infecting the lizard Enyalius bilineatus (Iguanidae; Leiosaurinae) from an Atlantic Rainforest area in Espírito Santo state, southeastern Brazil. Amphib-Reptil 28: 166 – 169. DOI: 10.1163/156853807779799009

Zuk, M., Mckean, K.A. (1996): Sex differences in parasite infection: patterns and processes. Int. J. Parasitol., 26: 1009 – 1024

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