Hostname: page-component-745bb68f8f-5r2nc Total loading time: 0 Render date: 2025-01-27T01:31:37.208Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of temporal variation and host condition on helminth abundance in the lizard Tropidurus hispidus from north-eastern Brazil

Published online by Cambridge University Press:  28 April 2016

J.A. Araujo Filho ,
S.V. Brito ,
V.F. Lima ,
A.M.A. Pereira ,
D.O. Mesquita ,
R.L. Albuquerque  and
W.O. Almeida
J.A. Araujo Filho*
Affiliation:
Programa de Pós-graduação em Bioprospecção Molecular, Universidade Regional do Cariri – URCA, R. Cel Antônio Luis, 1161, Pimenta, CEP 63100-000, Crato, CE, Brazil
S.V. Brito
Affiliation:
Departamento de Química Biológica, Universidade Regional do Cariri – URCA, R. Cel. Antônio Luiz, 1161, Pimenta, CEP 63105-000, Crato, CE, Brazil
V.F. Lima
Affiliation:
Programa de Pós-graduação em Bioprospecção Molecular, Universidade Regional do Cariri – URCA, R. Cel Antônio Luis, 1161, Pimenta, CEP 63100-000, Crato, CE, Brazil
A.M.A. Pereira
Affiliation:
Programa de Pós-graduação em Bioprospecção Molecular, Universidade Regional do Cariri – URCA, R. Cel Antônio Luis, 1161, Pimenta, CEP 63100-000, Crato, CE, Brazil
D.O. Mesquita
Affiliation:
Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, João Pessoa, PB 58051-900, Brazil
R.L. Albuquerque
Affiliation:
Department of Biology, University of California, Riverside, 900 University Avenue, Riverside 90521, California, USA
W.O. Almeida
Affiliation:
Departamento de Química Biológica, Universidade Regional do Cariri – URCA, R. Cel. Antônio Luiz, 1161, Pimenta, CEP 63105-000, Crato, CE, Brazil
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Ecological characteristics and environmental variation influence both host species composition and parasite abundance. Abiotic factors such as rainfall and temperature can improve parasite development and increase its reproduction rate. The comparison of these assemblages between different environments may give us a more refined analysis of how environment affects the variation of helminth parasite abundance. The aim of the present study was to evaluate how temporal variation, host size, sex and reproduction affect helminth abundance in the Tropidurus hispidus lizard in Caatinga, Restinga and Atlantic Forest environments. Overall, larger-sized lizards showed higher helminth abundance. We found a monthly variation in the helminth species abundance in all studied areas. In the Caatinga area, monoxenic and heteroxenic parasites were related to the rainy season and to the reproductive period of lizards. In Restinga, monoxenic and heteroxenic helminth species were more abundant during the driest months. In the Atlantic Forest, the rainy and host reproductive season occurred continuously throughout the year, so parasite abundance was relatively constant. Nevertheless, heteroxenic species were more abundant in this area. The present results showed that the temporal variation, body size, sex, reproductive period and habitat type influence the abundance and composition of helminth species in T. hispidus.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 3 , May 2017 , pp. 312 - 319
Copyright
Copyright © Cambridge University Press 2016 

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

Aho, J.M. (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. pp 157–196 in Esch, G.W., Bush, A.O. & Aho, J.M. (Eds) Parasite communities: Patterns and processes. London, Chapman & Hall.CrossRefGoogle Scholar
Almeida, W.O., Freire, E.M.X. & Lopes, S.G. (2008) A new species of Pentastomida infecting Tropidurus hispidus (Squamata: Tropiduridae) from Caatinga in Northeastern Brazil. Brazilian Journal of Biology 68, 631–637.CrossRefGoogle ScholarPubMed
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. & Rohani, P. (2006) Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.CrossRefGoogle ScholarPubMed
Anderson, R.C. (2000) Nematode parasites of vertebrates: Their development and transmission. Wallingford, Oxon, CABI.CrossRefGoogle Scholar
Anjos, L.A., Ávila, R.W., Ribeiro, S.C., Almeida, W.O. & Silva, R.J. (2012) Gastrointestinal nematodes of the lizard Tropidurus hispidus (Squamata: Tropiduridae) from a semi-arid region of Northeastern Brazil. Journal of Helminthology 4, 1–7.Google Scholar
Brito, S.V., Ferreira, F.S., Ribeiro, S.C., Anjos, L.A., Almeida, W.O., Mesquita, D.O. & 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 3, 1163–1169.CrossRefGoogle Scholar
Brito, S.V., Corso, G., Almeida, A.M., Ferreira, F.S., Almeida, W.O., Anjos, L.A., Mesquita, D.O. & 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 11, 3963–3972.CrossRefGoogle Scholar
Brooks, D.R., León-Règagnon, V., McLennan, D.A. & Zelmer, D. (2006) Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87, 76–85.CrossRefGoogle ScholarPubMed
Bush, A.O., Aho, J.M. & Kennedy, C.R. (1990) Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology 4, 1–20.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostaki, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Bush, A.O., Fernández, J.C., Esch, G.W. & Seed, J.R. (2001) Parasitism: The diversity and ecology of animal parasites. 1st edn. 531 pp. Cambridge, Cambridge University Press.Google Scholar
Carvalho, A.R. & Luque, J.L. (2011) Seasonal variation in metazoan parasites of Trichiurus lepturus (Perciformes: Trichiuridae) of Rio de Janeiro, Brazil. Brazilian Journal of Biology 71, 771–782.CrossRefGoogle ScholarPubMed
Dunlap, K.D. & Schall, J.J. (1995) Hormonal alteration and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum . Physiological Zoology 68, 608–621.CrossRefGoogle Scholar
Folstad, I. & Karter, A.J. (1992) Parasites, bright males, and immunocompetence handicap. The American Naturalist 139, 603–622.CrossRefGoogle Scholar
Fontes, A.F.F., Vicente, J.J., Kiefer, M.C. & Sluys, M.V. (2003) Parasitism by helminths in Eurolophosaurus nanuzae (Lacertilia: Tropiduridae) in an area of rocky outcrops in Minas Gerais state, Southeastern Brazil. Journal of Herpetology 37, 736–741.CrossRefGoogle Scholar
Frost, D.R., Rodrigues, M.T., Grant, T. & Titus, T.A. (2001) Phylogenetics of the lizard genus Tropidurus (Squamata: Tropiduridae: Tropidurinae): direct optimization, descriptive efficiency, and sensitivity analysis of congruence between molecular data and morphology. Molecular Phylogenetics and Evolution 21, 352–371.CrossRefGoogle ScholarPubMed
Galdino, C.A.B., Ávila, R.W., Bezerra, C.H., Passos, D.C., Melo, G.C. & 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
Gambhir, R.K., Oinam, S. & Lakshmipyari, W. (2012) Seasonal dynamics of Thelandros maplestonei infection in the wall lizard, Hemidactylus flaviviridis in Imphal Valley, Manipur, India. Journal of Parasitology Disease 37, 192–195.CrossRefGoogle ScholarPubMed
Gomes, F.F.A., Caldas, F.L.S., Santos, R.A., Silva, B.D., Santana, D.O., Rocha, S.M., Ferreira, A.S. & Faria, R.G. (2015) Patterns of space, time and trophic resource use by Tropidurus hispidus and T. semitaeniatus in an area of Caatinga, Northeastern Brazil. Herpetological Journal 25, 27–39.Google Scholar
Griffiths, A.D., Jones, H.I. & Christia, K.A. (1998) Effect of season on oral and gastric nematodes in the frillneck lizard from Australia. Journal of Wildlife Diseases 34, 381–385.CrossRefGoogle ScholarPubMed
Hamann, M.I., Kehr, A.I. & González, C.E. (2006) Species affinity and infracommunity ordination of helminths of Leptodactylus chaquensis (Anura: Leptodactylidae) in two contrasting environments from northeastern Argentina. Journal of Parasitology 92, 1171–1179.CrossRefGoogle ScholarPubMed
Hamann, M.I., Kehr, A.I. & González, C.E. (2014) Helminth community structure in the Argentinean bufonid Melanophryniscus klappenbachi: importance of habitat use and season. Parasitology Research 113, 3639–3649.CrossRefGoogle ScholarPubMed
Hamilton, W.D. & Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.CrossRefGoogle Scholar
Harwood, P.D. (1936) The effect of soil types on the helminths parasitic in the ground lizard, Leiolopisma laterale (Say). Ecology 17, 694–698.Google Scholar
Hawkins, B.A., Field, R., Cornell, H.V., Currie, D.J., Guégan, J.F., Kaufman, D.M., Kerr, J.T., Mittelbach, G.G., Oberdorff, T., O'Brien, E.M., Porter, E.E. & Turner, J.R.G. (2003) Energy, water, and broad-scale geographic patterns of species richness. Ecology 84, 3105–3117.CrossRefGoogle Scholar
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.CrossRefGoogle Scholar
IBGE (Instituto Brasileiro de Geografia e Estatística). (1985) Atlas Nacional do Brasil: Região Nordeste. Rio de Janeiro, IBGE.Google Scholar
IDEMA (Instituto de Desenvolvimento Sustentável e Meio Ambiente). (2000) Rio Grande do Norte. Available at http://www.idema.rn.gov.br (accessed 2 February 2015).Google Scholar
Janovy, J., Clopton, R.E. & Percival, T.J. (1992) The roles of ecological and evolutionary influences in providing structure to parasite species assemblages. Journal of Parasitology 78, 630–640.CrossRefGoogle ScholarPubMed
Kamiya, T., O'Dwyer, K., Nakagawa, S. & Poulin, R. (2014) What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Review 89, 123–134.CrossRefGoogle ScholarPubMed
Kolodiuk, M.F., Ribeiro, L.B. & Freire, E.M.X. (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata: Tropiduridae) living in sympatry in the Caatinga of northeastern Brazil. Zoologia 26, 581–585.CrossRefGoogle Scholar
Levri, E.P. (1999) Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection? Behavioral Ecology 10, 234–241.CrossRefGoogle Scholar
MacArthur, R.H. & Wilson, E.O. (1967) The theory of island biogeography. 201 pp. Princeton, New Jersey, Princeton University Press.Google Scholar
Martínez-Padilha, J., Mougeot, F., Rodríguez-Pérez, L. & Bortolotti, G.R. (2007) Nematode parasites reduce carotenoid-based signaling in male red grouse. Biological Letters 3, 161–164.CrossRefGoogle Scholar
Minguez, L. & Giambérini, L. (2012) Seasonal dynamics of zebra mussel parasite populations. Aquatic Biology 15, 145–151.CrossRefGoogle Scholar
Møller, A.P., Erritzøe, J. & Saino, N. (2003) Seasonal changes in immune response and parasite impact on hosts. The American Naturalist 161, 657–671.CrossRefGoogle ScholarPubMed
Narayanan, E.S., Rao, S.B.R. & Thontadaraya, T.S. (1961) Effect of temperature and humidity on the rate of development of the immature stages of Apanteles angaleti Muesebeck (Braconidae: Hymenoptera). Proceedings of the National Academy of Sciences, India 28, 150–163.Google Scholar
Nimer, E. (1989) Climatologia do Brasil. 421 pp. Rio de Janeiro, Instituto Brasileiro de Geografia e Estatística.Google Scholar
Pereira, F.B., Sousa, B.M. & Lima, S.S. (2012) Helminth community structure of Tropidurus torquatus (Squamata: Tropidurus) in a rocky outcrop area of Minas Gerais state, Southeastern Brazil. Journal of Parasitology 98, 6–10.CrossRefGoogle Scholar
Pereira, F.B., Gomides, S.C., Sousa, B.M., Lima, S.S. & Luque, J.L. (2013) The relationship between nematode infection and ontogeny and diet of the lizard Tropidurus torquatus (Squamata: Tropiduridae) from the Atlantic Rainforest in Southeastern Brazil. Journal of Helminthology 87, 364–370.CrossRefGoogle Scholar
Poulin, R. (1997) Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
Poulin, R. (2004) Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423–434.CrossRefGoogle Scholar
Poulin, R. & Nascimento, M.G. (2007) The scaling of total parasite biomass with host body mass. International Journal for Parasitology 37, 359–364.CrossRefGoogle ScholarPubMed
Poulin, R. & Valtonen, E.T. (2001) Nested assemblages resulting from host size variation: the case of endoparasite communities in fish hosts. International Journal for Parasitology 31, 1194–1204.CrossRefGoogle ScholarPubMed
Poulin, R., Guilhaumon, F., Randhawa, H.S., Luque, J.L. & Mouillot, D. (2010) Identifying hotspots of parasite diversity from species–area relationships: host phylogeny versus host ecology. Oikos 1, 1–8.Google Scholar
Riley, J. (1986) The biology of pentastomids. Advances in Parasitology 25, 45–128.CrossRefGoogle ScholarPubMed
Roca, V., Carretero, M.A., Llorene, G.A., Montori, A. & Martin, J.E. (2005) Helminth communities of two lizard populations (Lacertidae) from Canary Islands (Spain): host diet–parasite relationships. Amphibia–Reptilia 26, 535–542.CrossRefGoogle Scholar
Rodrigues, M.T. (1987) Sistemática, ecologia e Zoogeografia dos Tropidurus do grupo Torquatus ao sul do Rio Amazonas (Sauria: Iguanidae). Arquivos de Zoologia 3, 105–230.CrossRefGoogle Scholar
Roulin, A., Riols, C., Dijkstra, C. & Ducrest, A.L. (2001) Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behavioral Ecology 12, 103–110.CrossRefGoogle Scholar
Salvador, A., Veiga, J.P., Martin, J., Lopez, P., Abelenda, M. & Marisa, P. (1996) The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation. Behavioral Ecology 7, 145–150.CrossRefGoogle Scholar
Schall, J.J. & Dearing, M.D. (1987) Malarial parasitism and male competition for mates in the western fence lizard, Sceloporus occidetalis . Oecologia 73, 389–392.CrossRefGoogle Scholar
Ter Braak, C.J.F. (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67, 1167–1179.CrossRefGoogle Scholar
Thieltges, D.W., Jensen, K.T. & Poulin, R. (2008) The role of biotic factors in the transmission of freeliving endohelminth stages. Parasitology 135, 407–426.CrossRefGoogle ScholarPubMed
Vasconcellos, A., Andreazze, R., Almeida, A.M., Araujo, H.F.P., Oliveira, E. & Oliveira, U. (2010) Seasonality of insects in the semi-arid Caatinga of Northeastern Brazil. Revista Brasileira de Entomologia 54, 471–476.CrossRefGoogle Scholar
Vitt, L.J. (1995) The ecology of tropical lizards in the Caatinga of Northeast Brazil. Oklahoma Museum of Natural History 1, 1–29.Google Scholar
Zuk, M. & McKean, K.A. (1996) Sex differences in parasite infection: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle ScholarPubMed