Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T16:31:09.289Z Has data issue: false hasContentIssue false
  • English
  • Français

Vector abundance determines Trypanosoma prevalence in nestling blue tits

Published online by Cambridge University Press:  18 April 2013

J. MARTÍNEZ–DE LA PUENTE ,
J. MARTÍNEZ ,
J. RIVERO-DE-AGUILAR ,
S. DEL CERRO  and
S. MERINO
J. MARTÍNEZ–DE LA PUENTE*
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), C\ José Gutiérrez Abascal, 2. E-28006, Madrid, Spain
J. MARTÍNEZ
Affiliation:
Departamento de Microbiología y Parasitología, Universidad de Alcalá, Alcalá de Henares, Spain
J. RIVERO-DE-AGUILAR
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), C\ José Gutiérrez Abascal, 2. E-28006, Madrid, Spain
S. DEL CERRO
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), C\ José Gutiérrez Abascal, 2. E-28006, Madrid, Spain
S. MERINO
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), C\ José Gutiérrez Abascal, 2. E-28006, Madrid, Spain
*
*Corresponding author. Departamento de Ecología de Humedales, Estación Biológica de Doñana (EBD-CSIC), C/ Américo Vespucio, s/n. E-41092, Seville, Spain. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The effect of insect vectors on avian exposure to infection by pathogens remains poorly studied. Here, we used an insect repellent treatment to reduce the number of blood-sucking flying insects in blue tit Cyanistes caeruleus nests and examined its effect on nestling health status measured as body mass, nestling phytohaemagglutinin (PHA) response and blood parasite prevalence. We found that (i) the insect repellent treatment significantly reduced the number of blood-sucking flying insects in nests and (ii) the number of blood-sucking flying insects had a significant effect on the prevalence of the blood parasite Trypanosoma independently of the treatment. In addition, we found support for an adverse effect of parasite infections on nestling PHA response. Nestlings infected by Trypanosoma mounted a weaker response against PHA than non-parasitized ones. In addition, the number of blowflies in the nest was negatively associated with nestling PHA response. Overall, we found support for the hypothesis that blood-sucking flying insects attacking nestlings increase their exposure to parasite infections. Our results further substantiate the adverse effect of parasites on nestling condition.

Keywords

biting midge Culicoidesblack fliesLeucocytozoonPHA response
Type
Research Article
Information
Parasitology , Volume 140 , Issue 8 , July 2013 , pp. 1009 - 1015
Copyright
Copyright © Cambridge University Press 2013 

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

REFERENCES

Arriero, E., Moreno, J., Merino, S. and Martínez, J. (2008). Habitat effects on physiological stress response in nestling blue tits are mediated through parasitism. Physiological and Biochemical Zoology 81, 195–203.CrossRefGoogle ScholarPubMed
Atkinson, C. T. and van Riper, C. III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoan, and Haemoproteus. In Bird–Parasite Interactions: Ecology, Evolution and Behaviour (ed. Loye, J. E. and Zuk, M.), pp. 19–48. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Baker, J. R. (1956). Studies on Trypanosoma avium Danilewsky 1885. III. Life cycle in vertebrate and invertebrate hosts. Parasitology 46, 335–352.CrossRefGoogle ScholarPubMed
Bennett, G. F. (1961). On the specificity and transmission of some avian trypanosomes. Canadian Journal of Zoology 39, 17–33.CrossRefGoogle Scholar
Cosgrove, C. L., Knowles, S. C., Day, K. P. and Sheldon, B. C. (2006). No evidence for avian malaria infection during the nestling phase in a passerine bird. Journal of Parasitology 92, 1302–1304.CrossRefGoogle Scholar
Fallis, A. M. and Bennett, G. F. (1961). Sporogony of Leucocytozoon and Haemoproteus in simuliids and ceratopogonids and a revised classification of the Haemosporidiida. Canadian Journal of Zoology 39, 215–228.CrossRefGoogle Scholar
Fargallo, J. A. and Merino, S. (2004). Clutch size and haemoparasite species richness in adult and nestling blue tits. Ecoscience 11, 168–174.CrossRefGoogle Scholar
Figuerola, J. (1999). Effects of salinity on rates of infestation of waterbirds by haematozoa. Ecography 22, 681–685.CrossRefGoogle Scholar
Fitze, P. S., Clobert, J. and Richner, H. (2004). Long-term life-history consequences of ectoparasite-modulated growth and development. Ecology 85, 2018–2026.CrossRefGoogle Scholar
González, G., Sorci, G., Moller, A. P., Ninni, P., Haussy, C. and de Lope, F. (1999). Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). Journal of Animal Ecology 68, 1225–1234.CrossRefGoogle Scholar
Griffing, S. M., Kilpatrick, A. M., Clark, L. and Marra, P. P. (2007). Mosquito landing rates on nesting American robins (Turdus migratorius). Vector-borne and Zoonotic Diseases 7, 437–443.CrossRefGoogle ScholarPubMed
Hoi-Leitner, M., Romero-Pujante, M., Hoi, H. and Pavlova, A. (2001). Food availability and immune capacity in serin (Serinus serinus) nestlings. Behavioral Ecology and Sociobiology 49, 333–339.CrossRefGoogle Scholar
Hõrak, P., Tegelmann, L., Ots, I. and Møller, A. P. (1999). Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 121, 316–322.CrossRefGoogle ScholarPubMed
Hunter, D. B., Rohner, C. and Currie, D. C. (1997). Mortality in fledgling great horned owls from black fly hematophaga and leucocytozoonosis. Journal of Wildlife Diseases 33, 486–491.CrossRefGoogle ScholarPubMed
Hurtrez-Boussès, S., Perret, P., Renaud, F. and Blondel, J. (1997). High blowfly parasitic loads affect breeding success in a Mediterranean population of blue tits. Oecologia 112, 514–517.CrossRefGoogle Scholar
Lalubin, F., Bize, P., van Rooyen, J., Christe, P. and Glaizot, O. (2012). Potential evidence of parasite avoidance in an avian malarial vector. Animal Behaviour 84, 539–545.CrossRefGoogle Scholar
Lehane, M. (2005). The Biology of Blood-sucking in Insects, 2nd Edn. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Lehmann, T. (1993). Ectoparasites: direct impact on host fitness. Parasitology Today 9, 8–13.CrossRefGoogle ScholarPubMed
Lochmiller, R. L., Vestey, M. R. and Boren, J. C. (1993). Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110, 503–510.CrossRefGoogle Scholar
Martin, L. B., Han, P., Lewittes, J., Kuhlman, J. R., Klasing, K. C. and Wikelski, M. (2006). Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Functional Ecology 20, 290–299.CrossRefGoogle Scholar
Martínez, J., Martínez-de la Puente, J., Herrero, J., del Cerro, S., Lobato, E., Rivero-de Aguilar, J., Vásquez, R. A. and Merino, S. (2009). A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Parasitology 136, 713–722.CrossRefGoogle ScholarPubMed
Martínez-Abrain, 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
Martínez-de la Puente, J., Merino, S., Lobato, E., Rivero-de Aguilar, J., del Cerro, S. and Ruiz-de-Castañeda, R. (2009 a). Testing the use of a citronella-based repellent as an effective method to reduce the prevalence and abundance of biting flies in avian nests. Parasitology Research 104, 1233–1236.CrossRefGoogle ScholarPubMed
Martínez-de la Puente, J., Merino, S., Tomás, G., Moreno, J., Morales, J., Lobato, E., Talavera, S. and Sarto i Monteys, V. (2009 b). Factors affecting Culicoides species composition and abundance in avian nests. Parasitology 136, 1033–1041.CrossRefGoogle ScholarPubMed
Martínez-de la Puente, J., Merino, S., Lobato, E., Rivero-de Aguilar, J., del Cerro, S., Ruiz-de-Castañeda, R. and Moreno, J. (2010). Nest-climatic factors affect the abundance of biting flies and their effects on nestling condition. Acta Oecologica 36, 543–547.CrossRefGoogle Scholar
Martínez-de la Puente, J., Merino, S., Tomás, G., Moreno, J., Morales, J., Lobato, E. and Martínez, J. (2011). Nest ectoparasites increase physiological stress in breeding birds: an experiment. Naturwissenschaften 98, 99–106.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Merino, S. (2010). Immunocompetence and parasitism in nestlings from wild populations. Open Ornithology Journal 3, 27–32.CrossRefGoogle Scholar
Merino, S., Potti, J. and Moreno, J. (1996). Maternal effort mediates the prevalence of trypanosomes in the offspring of a passerine bird. Proceedings of the National Academy of Sciences, USA 93, 5726–5730.CrossRefGoogle ScholarPubMed
Merino, S., Martínez, J., Barbosa, A., Møller, A. P., de Lope, F., Pérez, J. and Rodríguez-Caabeiro, F. (1998). Increase in a heat shock protein from blood cells in response of nestling house martins (Delichon urbica) to parasitism: an experimental approach. Oecologia 116, 343–347.CrossRefGoogle Scholar
Merino, S., Martínez, J., Møller, A. P., Sanabria, L., de Lope, F., Pérez, J. and Rodríguez-Caabeiro, F. (1999). Phytohaemagglutinin injection assay and physiological stress in nestling house martins. Animal Behaviour 58, 219–222.CrossRefGoogle ScholarPubMed
Merino, S., Møller, A. P. and de Lope, F. (2000 a). Seasonal changes in cell-mediated immunocompetence and mass gain in nestlings barn swallows: a parasite-mediated effect? Oikos 90, 327–332.CrossRefGoogle Scholar
Merino, S., Moreno, J., Sanz, J. J. and Arriero, E. (2000 b). Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London, B 267, 2507–2510.CrossRefGoogle Scholar
Merino, S., Martínez, J., Møller, A. P., Barbosa, A., de Lope, F. and Rodríguez-Caabeiro, F. (2001). Physiological and haematological consequences of a novel parasite on the red-rumped swallow Hirundo daurica. International Journal for Parasitology 31, 1187–1193.CrossRefGoogle ScholarPubMed
Miltgen, F. and Landau, I. (1982). Culicoides nubeculosus, an experimental vector of a new trypanosome from psittaciforms: Trypanosoma barkeri n. sp. Annales de Parasitologie Humaine et Comparee 57, 423–428. [Article in French]CrossRefGoogle ScholarPubMed
Møller, A. P. (1997). Parasitism and the evolution of host life history. In Host–Parasite Evolution: General Principles and Avian Models (ed. Clayton, D. H. and Moore, J.), pp. 105–127. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Molyneux, D. H. (1973). Trypanosoma bouffardi of West African Ploceidae (Aves). Parasitology 66, 215–230.CrossRefGoogle ScholarPubMed
Moreno, J., Sanz, J. J. and Arriero, E. (1999). Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied flycatchers Ficedula hypoleuca. Proceedings of the Royal Society of London, B 266, 1105–1109.CrossRefGoogle Scholar
Moreno, J., Merino, S., Lobato, E., Ruiz-De-Castañeda, R., Martínez-de la Puente, J., del Cerro, S. and Rivero-de Aguilar, J. (2009). Nest-dwelling ectoparasites of two sympatric hole-nesting passerines in relation to nest composition: an experimental study. Ecoscience 16, 418–427.CrossRefGoogle Scholar
Morn, T., Matsui, T., Iijima, T. and Fujinaga, F. (1984). Infectivity of Leucocytozoon caulleryi sporozoites developed in vitro and in vivo. International Journal for Parasitology 14, 135–139.CrossRefGoogle Scholar
Navarro, C., Marzal, A., de Lope, F. and Møller, A. P. (2003). Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos 101, 291–298.CrossRefGoogle Scholar
Ortego, J. and Cordero, P. J. (2010). Factors associated with the geographic distribution of leucocytozoa parasitizing nestling eagle owls (Bubo bubo): a local spatial-scale analysis. Conservation Genetics 11, 1479–1487.CrossRefGoogle Scholar
Puchala, P. (2004). Detrimental effects of larval blow flies (Protocalliphora azurea) on nestlings and breeding success of tree sparrows (Passer montanus). Canadian Journal of Zoology 82, 1285–1290.CrossRefGoogle Scholar
Reardon, J. T. and Norbury, G. (2004). Ectoparasite and hemoparasite infection in a diverse temperate lizard assemblage at Macraes Flat, South Island, New Zealand. Journal of Parasitology 90, 1274–1278.CrossRefGoogle Scholar
Saino, N., Calza, S. and Møller, A. P. (1997). Immunocompetence of nestling barn swallows in relation to brood size and parental effort. Journal of Animal Ecology 66, 827–836.CrossRefGoogle Scholar
Saino, N., Suffritti, C., Martinelli, R., Rubolini, D. and Møller, A. P. (2003). Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behavioral Ecology 14, 318–325.CrossRefGoogle Scholar
Sánchez, S., Cuervo, J. J. and Moreno, E. (2007). Does habitat structure affect body condition of nestlings? A case study with woodland great tits Parus major. Acta Ornithologica 42, 200–204.CrossRefGoogle Scholar
Smith, A., Telfer, S., Burthe, S., Bennett, M. and Begon, M. (2005). Trypanosomes, fleas and field voles: ecological dynamics of a host-vector–parasite interaction. Parasitology 131, 355–365.CrossRefGoogle ScholarPubMed
Smits, J. E., Bortolotti, G. R. and Tella, J. L. (1999). Simplifying the phytohemagglutinin skin testing technique in studies of avian immunocompetence. Functional Ecology 135, 567–572.CrossRefGoogle Scholar
Sol, D., Jovani, R. and Torres, J. (2000). Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307–314.CrossRefGoogle Scholar
Super, P. E. and van Riper, C. III (1995). A comparison of avian hematozoan epizootiology in two California coastal scrub communities. Journal of Wildlife Diseases 31, 447–461.CrossRefGoogle ScholarPubMed
Tomás, G., Merino, S., Martínez-de la Puente, J., Moreno, J., Morales, J. and Lobato, E. (2008 a). A simple trapping method to estimate abundances of blood-sucking flying insects in avian nests. Animal Behaviour 75, 723–729.CrossRefGoogle Scholar
Tomás, G., Merino, S., Martínez-de la Puente, J., Moreno, J., Morales, J. and Lobato, E. (2008 b). Determinants of abundance and effects of blood-sucking flying insects in the nest of a hole-nesting bird. Oecologia 156, 305–312.CrossRefGoogle ScholarPubMed
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Votýpka, J. and Svobodová, M. (2004). Trypanosoma avium: experimental transmission from black flies to canaries. Parasitology Research 92, 147–151.CrossRefGoogle ScholarPubMed
Votýpka, J., Synek, P. and Svobodová, M. (2009). Endophagy of biting midges attacking cavity-nesting birds. Medical and Veterinary Entomology 23, 277–280.CrossRefGoogle ScholarPubMed
Wood, M. J., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C., Day, K. P. and Sheldon, B. C. (2007). Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273.CrossRefGoogle ScholarPubMed