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Absence of haemoparasite infection in the fossorial amphisbaenian Trogonophis wiegmanni

Published online by Cambridge University Press:  25 May 2016

JOSÉ MARTÍN ,
MARIO GARRIDO ,
JESÚS ORTEGA ,
ROBERTO GARCÍA-ROA ,
ALEJANDRO IBÁÑEZ  and
ALFONSO MARZAL
JOSÉ MARTÍN*
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain
MARIO GARRIDO
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel
JESÚS ORTEGA
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain
ROBERTO GARCÍA-ROA
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain
ALEJANDRO IBÁÑEZ
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain Department of Evolutionary Biology, Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany
ALFONSO MARZAL
Affiliation:
Departamento de Anatomía, Biología Celular y Zoología, Universidad de Extremadura, 06071 Badajoz, Spain
*
*Corresponding author: Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain. E-mail: [email protected]
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Summary

Blood parasites such as haemogregarines and haemosporidians have been identified in almost all groups of vertebrates. However, very little is known about biodiversity of these parasites and their effects on some major groups of reptiles such as amphisbaenians, a distinctive group with many morphological and ecological adaptations to fossorial life. Conditions of the fossorial environment might also affect host–parasite relationships. We investigated the presence and the potential prevalence of three genera of haemoparasitic aplicomplexan blood parasites (Hepatozoon, Plasmodium and Haemoproteus) in the amphisbaenian Trogonophis wiegmanni, a fossorial worm lizard species from North West Africa. Blood parasite infection was not detected in T. wiegmanni, both in visual surveys of blood smears and using molecular methods to detect DNA of such parasites in the blood of the potential amphisbaenian hosts. We discuss how conditions of the fossorial environment might affect blood parasitaemias in amphisbaenians as well as in other fossorial reptiles.

Keywords

amphisbaeniansfossorial environmenthaemoparasitesreptiles
Type
Research Article
Information
Parasitology , Volume 143 , Issue 11 , September 2016 , pp. 1433 - 1436
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Amo, L., López, P. and Martín, J. (2004). Prevalence and intensity of haemogregarinid blood parasites in a population of the Iberian rock lizard, Lacerta monticola . Parasitology Research 94, 290–293.Google Scholar
Amo, L., Fargallo, J. A., Martínez-Padilla, J., Millán, J., López, P. and Martín, J. (2005). Prevalence and intensity of blood and intestinal parasites in a field population of a Mediterranean lizard, Lacerta lepida . Parasitology Research 96, 413–417.Google Scholar
Bennett, G. F., Montgomerie, R. and Seutin, G. (1992). Scarcity of haematozoa in birds breeding on the Arctic tundra of North America. The Condor 94, 289–292.Google Scholar
Davies, A. J. and Johnston, M. R. (2000). The biology of some intraerythrocytic parasites of fishes, amphibia and reptiles. Advances in Parasitology 45, 1–107.Google Scholar
Davis, A. K., Benz, A. C., Ruyle, L. E., Kistler, W. M., Shock, B. C. and Yabsley, M. J. (2013). Searching before it is too late: a survey of blood parasites in Ctenosaura melanosterna, a critically endangered reptile of Honduras. ISRN Parasitology 2013, Article ID 495304, 1–6.Google Scholar
Dietrich, M., Gómez-Díaz, E. and McCoy, K. D. (2011). Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tick-borne pathogens. Vector-Borne and Zoonotic Diseases 11, 453–470.Google Scholar
Gans, C. (1978). The characteristics and affinities of the Amphisbaenia. Transactions of the Zoological Society of London 34, 347–416.Google Scholar
Gans, C. (2005). Checklist and bibliography of the amphisbaenia of the World. Bulletin of the American Museum of Natural History. 280, 1–130.Google Scholar
García, L. V., Marañón, T., Ojeda, F., Clemente, L. and Redondo, R. (2002). Seagull influence on soil properties, chenopod shrub distribution, and leaf nutrient status in semi-arid Mediterranean islands. Oikos 98, 75–86.Google Scholar
Garrido, M. and Pérez-Mellado, V. (2013). Prevalence and intensity of blood parasites in insular lizards. Zoologischer Anzeiger – A Journal of Comparative Zoology 252, 588–592.Google Scholar
Goater, T. M., Goater, C. P. and Esch, G. W. (2014). Parasitism. The Diversity and Ecology of Animal Parasites, 2nd edn. Cambridge University Press, Cambridge.Google Scholar
Harris, D. J., Maia, J. P. M. C. and Perera, A. (2011). Molecular characterization of Hepatozoon species in reptiles from the Seychelles. Journal of Parasitology 97, 106–110.Google Scholar
Hellgren, O., Waldenström, J. and Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797–802.Google Scholar
Jacobson, E. (2007). lnfectious Diseases and Pathology of Reptiles. CRC Press, Florida.Google Scholar
Klein, T. A., Young, D. G., Telford, S. R. and Kimsey, R. (1987). Experimental transmission of Plasmodium mexicanum by bites of infected Lutzomyia vexator (Diptera: Psychodidae). Journal of the American Mosquito Control Association 3, 154–164.Google Scholar
Lainson, R. (2003). Some coccidial parasites of the lizard Amphisbaena alba (Reptilia: Amphisbaenia: Amphisbaenidae). Memórias do Instituto Oswaldo Cruz 98, 927–936.Google Scholar
Little, R. M. and Earlé, R. A. (1994). Lack of avian haematozoa in the Phasianinae of Robben Island. Ostrich 65, 343–344.Google Scholar
Martín, J., Polo-Cavia, N., Gonzalo, A., López, P. and Civantos, E. (2011). Structure of a population of the amphisbaenian Trogonophis wiegmanni in North Africa. Herpetologica 67, 250–257.Google Scholar
Martín, J., López, P. and García, L. V. (2013 a). Soil characteristics determine microhabitat selection of the fossorial amphisbaenian Trogonophis wiegmanni . Journal of Zoology 290, 265–272.Google Scholar
Martín, J., Ortega, J., López, P., Pérez-Cembranos, A. and Pérez-Mellado, V. (2013 b). Fossorial life does not constrain diet selection in the amphisbaenian Trogonophis wiegmanni . Journal of Zoology 291, 226–233.Google Scholar
Martín, J., López, P., Gutiérrez, E. and García, L. V. (2015). Natural and anthropogenic alterations of the soil affect body condition of the fossorial amphisbaenian Trogonophis wiegamnni in North Africa. Journal of Arid Environments 122, 30–36.Google Scholar
Martínez-Abraín, A., Esparza, B. and Oro, D. (2004). Lack of blood parasites in bird species: does absence of blood parasite vectors explain it all. Ardeola 51, 225–232.Google Scholar
Medeiros, M. C. I., Hamer, G. L. and Ricklefs, R. E. (2013). Host compatibility rather than vector-host-encounter rate determines the host range of avian Plasmodium parasites. Proceedings of the Royal Society of London, Series B 280, 2947–2954.Google Scholar
Megía-Palma, R., Martínez, J., Acevedo, I., Martín, J., García-Roa, R., Ortega, J., Peso-Fernández, M., Albaladejo, G., Cooper, R. D., Paranjpe, D. A., Sinervo, B. R. and Merino, S. (2015). Phylogeny of the reptilian Eimeria: are Choleoeimeria and Acroeimeria valid generic names? Zoologica Scripta 44, 684–692.Google Scholar
Mendes, L., Piersma, T., Lecoq, M., Spaans, B. and Ricklefs, R. E. (2005). Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396–404.Google Scholar
Papenfuss, T. J. (1982). The ecology and systematics of the amphisbaenian genus Bipes . Occasional Papers of the Californian Academy of Sciences 136, 1–42.Google Scholar
Perkins, S. L. and Keller, A. K. (2001). Phylogeny of nuclear small subunit rRNA genes of hemogregarines amplified with specific oligonucleotídeos. Journal of Parasitology 87, 870–876.Google Scholar
Pessoa, S. B. (1968). Sobre uma hemogregarina de Amphisbaena alba . Gazeta Médica da Bahia 68, 75–78.Google Scholar
Piersma, T. (1997). Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80, 623–631.Google Scholar
Quillfeldt, P., Arriero, E., Martínez, J., Masello, J. F. and Merino, S. (2011). Prevalence of blood parasites in seabirds – a review. Frontiers in Zoology 8, 26.Google Scholar
Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences of the United States of America 89, 4722–4725.Google Scholar
Sambrook, J., Fritch, F. J. and Maniatis, T. (2002). Molecular Cloning, a Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.Google Scholar
Schall, J. J. (1990). Virulence of lizard malaria: the evolutionary ecology of an ancient parasite-host association. Parasitology 100, S35–S52.Google Scholar
Smith, T. G. (1996). The genus Hepatozoon (Apicomplexa; Adeleina). Journal of Parasitology 82, 565–585.Google Scholar
Telford, S. R. (1984). Haemoparasites of reptiles. In Diseases of Amphibians and Reptiles (ed. Hoff, G. L., Frye, F. L. and Jacobson, E. R.), pp. 385–517. Plenum Press, New York.Google Scholar
Telford, S. R. (2008). Hemoparasites of the Reptilia: Color atlas and text. CRC Press, Boca Raton, Florida.Google Scholar
Ujvari, B., Madsen, T. and Olsson, M. (2004). High prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in wáter pythons (Liasis fuscus) from tropical Australia. Journal of Parasitology 90, 670–672.Google Scholar
Vardo-Zalik, A. M. and Schall, J. J. (2008). Clonal diversity within infections and the virulence of a malaria parasite, Plasmodium mexicanum . Parasitology 135, 1363–1372.Google Scholar
Wozniak, E. J., Kazacos, K. R., Telford, S. R. and Mclaughlin, G. (1996). Characterization of the clinical and anatomical pathological changes associated with Hepatozoon mocassini infections in unnatural reptilian hosts. International Journal of Parasitology 26, 141–146.Google Scholar