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Long-term epidemiology, effect on body condition and interspecific interactions of concomitant infection by nasopharyngeal bot fly larvae (Cephenemyia auribarbis and Pharyngomyia picta, Oestridae) in a population of Iberian red deer (Cervus elaphus hispanicus)

Published online by Cambridge University Press:  23 August 2004

J. VICENTE ,
Y. FIERRO ,
M. MARTÍNEZ  and
C. GORTÁZAR
J. VICENTE
Affiliation:
Instituto de Investigación en Recursos Cinegéticos (CSIC-UCLM-JCCM), Ronda de Toledo s/n., E-13005 Ciudad Real, Spain
Y. FIERRO
Affiliation:
Yolfi Properties S.L., Abenójar, Ciudad Real, Spain
M. MARTÍNEZ
Affiliation:
Instituto de Investigación en Recursos Cinegéticos (CSIC-UCLM-JCCM), Ronda de Toledo s/n., E-13005 Ciudad Real, Spain
C. GORTÁZAR
Affiliation:
Instituto de Investigación en Recursos Cinegéticos (CSIC-UCLM-JCCM), Ronda de Toledo s/n., E-13005 Ciudad Real, Spain
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Abstract

We studied the pattern of infection and the inter-annual variation and individual factors affecting the infection of 2 species of nasopharyngeal bot flies, Cephenemyia auribarbis and Pharyngomyia picta (Diptera: Oestridae), in a population of Iberian red deer (Cervus elaphus hispanicus) from south central Spain (10 annual periods between 1990 and 2003). Mean prevalence±S.E.95%CI of infection was 35·19±4·24% (n=486). The frequency distribution of the parasites was markedly aggregated (K: 0·213, mean abundance±S.D.: 5·49±12·12). Parasite load of Oestridae peaked at calf and subadult age groups and declined thereafter, which suggests that acquired immunity may be acting. In common with other host–parasite relationships, male hosts were found to have higher prevalence and abundance levels than females. The prevalence of P. picta was positively affected by the presence of C. auribarbis whereas the intensity of infection of P. picta was negatively affected by the presence of C. auribarbis. Intensity of P. picta in concomitant infections with C. auribarbis was lower than in pure P. picta infections, whilst the intensity of C. auribarbis infections did not change. This provides good evidence of interspecific competence, which could be dealt with by parasites by means of asynchronous life-cycles and different maturation periods. Weather also affects the dynamics and transmission rates of these parasites. Previous annual rainfalls positively affected the level of infection with oestrids. Yearly autumn rainfalls affected positively P. picta, possibly due to an effect on the pupal stage survival. Infection of Oestridae affected body condition in calves and subadults, suggesting that oestrids could have sublethal effects on Iberian red deer. Future research is needed to investigate the effect of parasites on the dynamics of the Iberian red deer.

Keywords

nasopharyngeal bot flyinter-annual variationsbody conditionCephenemyia auribarbisCervus elaphus hispanicusconcomitant infectionPharyngomyia picta
Type
Research Article
Information
Parasitology , Volume 129 , Issue 3 , September 2004 , pp. 349 - 361
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

ALBON, S. D., MITCHELL, B. & STAINES, B. W. ( 1983). Fertility and body-weight in female red deer. A density-dependent relationship. Journal of Animal Ecology 52, 969–980.Google Scholar
ALBON, S. D., STIEN, A., IRVINE, R. J., LANGVATN, R., ROPSTAD, E. & HALVORSEN, O. ( 2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London, B 269, 1625–1632.CrossRefGoogle Scholar
ALEXANDER, J. & STIMSON, W. H. ( 1988). Sex hormones and the course of parasitic infection. Parasitology Today 4, 189–193.CrossRefGoogle Scholar
ANDERSON, J. R., NILSSEN, A. C. & FOLSTAD, I. ( 1994). Mating behavior and thermoregulation of the reindeer warble fly, Hypoderma tarandi (Diptera, Oestridae). Journal of Insect Behavior 7, 679–706.CrossRefGoogle Scholar
ANDERSON, R. C. & MAY, R. M. ( 1978). Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.Google Scholar
BREYEV, K. A. ( 1973). Some general principles of the control of parasitic arthropods as exemplified by the control of warble flies. Entomological Review 52, 142–151.Google Scholar
BUENO-DE LA FUENTE, M. L., MORENO, V., PEREZ, J. M., RUIZ-MARTÍNEZ, I. & SORIGUER, R. C. ( 1998). Oestrosis in red deer from Spain. Journal of Wildlife Diseases 34, 820–824.CrossRefGoogle Scholar
CAMERON, A. E. ( 1932). The nasal bot fly, Cephenemyia auribarbis Meig. (Diptera: Tachinidae) of the red deer, Cevus elaphus L. Parasitology 24, 185–195.Google Scholar
CLUTTON-BROCK, T. H., ALBON, S. D. & GUINNESS, F. E. ( 1987). Interactions between population density and maternal characteristics affecting fecundity and juvenile survival in red deer. Journal of Animal Ecology 56, 857–871.CrossRefGoogle Scholar
CRAWLEY, M. J. ( 1993). GLIM for Ecologists. Blackwell, London.
COGLEY, T. P. ( 1987). Effects of Cephenemyia spp. (Diptera: Oestridae) on the nasopharynx of black-tailed deer (Odocoileus hemionus columbianus). Journal of Wildlife Diseases 23, 596–605.Google Scholar
COX, F. E. ( 2001). Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38.CrossRefGoogle Scholar
DE LA FUENTE, C., SAN MIGUEL, J. M., SANTIN, M., ALUNDA, J. M., DOMINGUEZ, I., LOPEZ, A., CARBALLO, M. & GONZALEZ, A. ( 2000). Pharyngeal bot flies in Cervus elaphus in central Spain: prevalence and population dynamics. Journal of Parasitology 86, 33–37.CrossRefGoogle Scholar
FESTA-BIANCHET, M. ( 1989). Individual differences, parasites and the costs of reproduction for bighorn ewes (Ovis canadensis). Journal of Animal Ecology 58, 785–795.CrossRefGoogle Scholar
FIERRO, Y., GORTAZAR, C., LANDETE-CASTILLEJOS, T., VICENTE, J., GARCÍA, A. & GALLEGO, L. ( 2002). Baseline values for cast antlers of Iberian red deer (Cervus elaphus hispanicus). Zeitschrift für Jagdwissenschaft 48, 244–251.CrossRefGoogle Scholar
FOLSTAD, I. & KARTER, A. J. ( 1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622.CrossRefGoogle Scholar
FOLSTAD, I., NILSSEN, A. C., HALVORSEN, O. & ANDERSEN, J. ( 1989). Why do male reindeer (Rangifer tarandus) have higher abundance of 2nd and 3rd instar larvae of Hypoderma tarandi than females? Oikos 55, 87–92.Google Scholar
FOREYT, W. J., LEATHERS, C. W. & HATTAN, G. ( 1994). Bot fly larvae (Cephenemyia jellisoni) as a cause of neurologic signs in an elk. Journal of Wildlife Diseases 30, 470–471.CrossRefGoogle Scholar
GIL COLLADO, J. ( 1955). Las especies españolas de estridos (sensu latu). Revista Ibérica de Parasitología. Vol. (ext.), 411–420.Google Scholar
GIL COLLADO, J., VALLS, J. L. & FIERRO, Y. ( 1985). Estudio de las larvas de Oestridae parasitas de Cervidae en España. Boletim de la Sociedade Portuguesa de Entomología 1, 467–475.Google Scholar
GULLAND, F. M. ( 1992). The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105, 493–503.Google Scholar
GULLAND, F. M. D. ( 1995). Impact of infectious diseases on wild animals. In Ecology of Infectious Diseases in Natural Populations ( ed. Grenfell, B. T. & Dobson, A. P. ), pp. 20–51. Cambridge University Press, Cambridge.CrossRef
GULLAND, F. M. D., ALBON, S. D., PEMBERTON, J. M., MOOREIOJT, P. R. & CLUTTON-BLOCK, T. H. ( 1993). Parasite-associated polymorphism in a cyclic ungulate population. Proceedings of the Royal Society of London, B 254, 7–13.CrossRefGoogle Scholar
HAMILTON, W. D. & ZUK, M. ( 1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 383–387.Google Scholar
HUDSON, P. J. & DOBSON, A. P. ( 1995). Macroparasites: observed patterns. In Ecology of Infectious Diseases in Natural Populations ( ed. Grenfell, B. T. & Dobson, A. P. ), pp. 144–176. Cambridge University Press, Cambridge.CrossRef
HUDSON, P. J., DOBSON, A. P. & NEWBORN, D. ( 1985). Cyclic and non-cyclic populations of red grouse: a role for parasitism? In Ecology and Genetics of Hosts–parasite Interactions ( ed. Rollinson, D. & Anderson, R. M. ), pp. 77–90. Academic Press, London.
HUDSON, P. J., DOBSON, A. P. & NEWBORN, D. ( 1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle Scholar
HUDSON, P. J., NEWBORN, D. & DOBSON, A. P. ( 1992). Regulation and stability of a free-living host–parasite system: Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. Journal of Animal Ecology 61, 681–692.Google Scholar
KLEIN, S. L. ( 2000). Hormones and mating system affect sex and species differences in immune function among vertebrates. Behavioral Processes 51, 149–166.CrossRefGoogle Scholar
KLEVEZAL', G. A. & KLEINENBERG, S. E. ( 1967). Age determination of mammals from annual layers in teeth and bones. USSR Academy of Sciences, Severtsov Inst. Anim. Morphol. Clearinghouse Fed. Sci. Tech. Inf. U.S. Dep. Commer, Springfield (Translated from Russian).
LLOYD, S. ( 1995). Environmental influences on host immunity. In Ecology of Infectious Diseases in Natural Populations ( ed. Grenfell, B. T. & Dobson, A. P. ), pp. 327–361. Cambridge University Press, Cambridge.CrossRef
McMAHON, D. C. & BUNCH, T. D. ( 1989). Bot fly larvae (Cephenemyia spp., Oestridae) in Mule Deer (Odocoilus hemionus) from Utah. Journal of Wildlife Diseases 25, 636–638.Google Scholar
MARGOLIS, L., ESCH, G. W., HOLMES, J. C., KURIS, A. M. & SCHAD, G. A. ( 1982). The use of ecological terms in parasitology (report of an ad hoc Committee of the American Society of Parasitologists). Journal of Parasitology 68, 131–133.CrossRefGoogle Scholar
MARTIN, S. W., MEEK, A. H. & WILLEBERG, P. ( 1987). Veterinary Epidemiology. Iowa State University Press, Ames.
NILSSEN, A. C. & HAUGERUD, R. E. ( 1995). Epizootiology of the reindeer nose bot fly, Cephenemyia trompe (Modeer) (Diptera: Oestridae), in reindeer, Rangifer tarandus (L.), in Norway. Canadian Journal of Zoology 73, 1024–1036.CrossRefGoogle Scholar
NILSSEN, A. C. ( 1997). Effect of temperature on pupal development and eclosion dates in the reindeer oestrids Hypoderma tarandi and Cephenemyia trompe (Diptera: Oestridae). Physiological and Chemical Ecology 26, 296–306.CrossRefGoogle Scholar
POULIN, R. ( 1996). Sexual inequalities in helminth infection: a cost of being male? American Naturalist 147, 287–295.Google Scholar
RUIZ MARTINEZ, I. & PALOMARES, F. ( 1993). Occurrence and overlapping of pharyngeal bot flies Pharyngomyia picta and Cephenemyia auribarbis (Oestridae) in red deer of southern Spain. Veterinary Parasitology 47, 119–127.CrossRefGoogle Scholar
RUIZ, I., SORIGUER, R. C. & PEREZ, J. M. ( 1993). Pharyngeal bot flies (Oestridae) from sympatric wild cervids in southern Spain. Journal of Parasitology 79, 623–626.CrossRefGoogle Scholar
SCOTT, M. E. ( 1987). Regulation of mouse colony abundance by Heligmosomoides polygyrus. Parasitology 95, 111–124.CrossRefGoogle Scholar
SHAW, D. J., GRENFELL, B. T. & DOBSON, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle Scholar
SHAW, D. J. & DOBSON, A. P. ( 1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S133.CrossRefGoogle Scholar
STIEN, A, IRVINE, R. J., ROPSTAD, E., HALVORSEN, O., LANGVATN, R. & ALBON, D. ( 2002). The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. Journal of Animal Ecology 71, 937–945.CrossRefGoogle Scholar
SUGÁR, L. ( 1974). The occurrence of nasal throat bot flies (Oestridae) in wild ruminants in Hungary. Parasitologia Hungarica 7, 181–189.Google Scholar
SUGÁR, L. ( 1976). Seasonal incidence of larvae of Pharyngomyia picta (Meigen) 1824 and Cephenemyia auribarbis (Meigen) 1824 (Oestridae) in red deer (Cervus elaphus hippelaphus) in Hungary. Parasitologia Hungarica 9, 73–84.Google Scholar
WILSON, K., GRENFELL, B. T. & SHAW, D. J. ( 1996). Analysis of aggregated parasite distributions: a comparison of methods. Functional Ecology 10, 592–601.CrossRefGoogle Scholar
WILSON, K. & GRENFELL, B. T. ( 1997). Generalised linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle Scholar
WILSON, K., BJORNSTAD, O. N., DOBSON, A. P., MERLER, S., POGLAYEN, G., RANDOLPH, S. E., READ, A. F. & SKORPING, A. ( 2001). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases ( ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P. ), pp. 6–44. Oxford University Press, Oxford.
ZUK, M. & McKEAN, K. A. ( 1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.CrossRefGoogle Scholar
ZUMPT, F. ( 1965). Myiasis in man and animals in the old world. Butterworths, London.