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Synchronization of host-parasite cycles by means of diapause: host influence and parasite response to involuntary host shifting

Published online by Cambridge University Press:  28 August 2008

M. A. CALERO-TORRALBO  and
F. VALERA
M. A. CALERO-TORRALBO*
Affiliation:
Estación Experimental de Zonas Áridas (CSIC), General Segura 1, E-04001 Almería, Spain
F. VALERA
Affiliation:
Estación Experimental de Zonas Áridas (CSIC), General Segura 1, E-04001 Almería, Spain
*
*Corresponding author: Tel: +34 950281045. Fax: +34 950277100. E-mail: calero@eeza.csic.es
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Summary

Many parasites require synchronization of their infective phases with the appearance of susceptible host individuals and, for many species, diapause is one of the mechanisms contributing to such coincidence. A variety of ecological factors, like changes in host temperature produced by involuntary host shifting (substitution of the usual host by an infrequent one), can modify host-parasite synchronization of diapausing ectoparasites of endothermic species. To understand the influence of host shifting on the mechanisms of parasite synchronization, we conducted experiments using the system formed by the ectoparasitic fly Carnus hemapterus and its avian hosts. We simulated the occurrence of the usual host and natural cases of host shifting by exposing overwintering carnid pupae from Bee-eater nests (Merops apiaster) to the earlier incubation periods of two Carnus host species that frequently reoccupy Bee-eater nests. Pupae exposed to host shifting treatments advanced the mean date of emergence and produced an earlier and faster rate of emergence in comparison with pupae exposed both to the control (absence of any host) and Bee-eater treatments. The effect was more evident for the treatment resembling the host with the most dissimilar phenology to the one of the usual host. Our results show that host temperature is an environmental cue used by this nest-dwelling haematophagous ectoparasite and reveal that Carnus hemapterus has some potential to react to involuntary host shifting by means of plasticity in the termination of diapause.

Keywords

Carnus hemapterusdiapauseectoparasitehost temperaturehost-shiftinglife cyclephenotypic plasticity
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 11 , September 2008 , pp. 1343 - 1352
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Andres, J. and Cordero, A. (1998). Effects of water mites on the damselfly Ceriagrion tenellum. Ecological Entomology 23, 103–109.CrossRefGoogle Scholar
Ar, A. and Piontkewitz, Y. (1992). Nest ventilation explains gas composition in the nest chamber of the European bee-eater. Respiration Physiology 87, 407–418.CrossRefGoogle ScholarPubMed
Baker, H. G. (1965). Characteristics and modes of origin of weeds. In The Genetics of Colonizing Species. (ed. Baker, H. G. and Stebbins, G. L.), pp. 147–168. Academic Press, New York, USA.Google Scholar
Blanckenhorn, W. U. (1998). Altitudinal differentiation in the diapause response of two species of dung flies. Ecological Entomology 23, 1–8.CrossRefGoogle Scholar
Broufas, G. D. and Koveos, D. S. (2000). Threshold temperature for post-diapause development and degree-days to hatching of winter eggs of the European red mite (Acari: Tetranychidae) in Northern Greece. Environmental Entomology 29, 710–713.CrossRefGoogle Scholar
Carroll, S. P. and Boyd, C. (1992). Host race radiation in the Soapberry bug: natural history with the history. Evolution 46, 1052–1069.CrossRefGoogle ScholarPubMed
Casas-Crivillé, A. and Valera, F. (2005). The European bee-eater (Merops apiaster) as an ecosystem engineer in arid environments. Journal of Arid Environments 60, 227–238.CrossRefGoogle Scholar
Cramp, S. (1985). Handbook of the Birds of Europe, Middle East and North Africa, Vol. IV. Oxford University Press, Oxford, UK.Google Scholar
Danks, H. V. (1987). Insect Dormancy: an Ecological Perspective. Biological Survey of Canada No. 1, Ottawa, Ontario, Canada.Google Scholar
Danks, H. V. (1992). Long life-cycles in insects. Canadian Entomologist 124, 167–187.CrossRefGoogle Scholar
Danks, H. V. (2006). Key themes in the study of seasonal adaptations in insects II. Life-cycle patterns. Applied Entomology and Zoology 41, 1–13.CrossRefGoogle Scholar
Feder, J. L., Hunt, T. A. and Bush, L. (1993). The effects of climate, host-plant phenology and host fidelity on the genetics of apple and hawthorn infesting races of Rhagoletis pomonella. Entomologia Experimentalis et Applicata 69, 117–135.CrossRefGoogle Scholar
Feder, J. L., Stolz, U., Lewis, K. M., Perry, W., Roethele, J. B. and Rogers, A. (1997). The effects of winter length on the genetics of apple and hawthorn races of Rhagoletis pomonella (Diptera: Tephritidae). Evolution 51, 1862–1876.CrossRefGoogle Scholar
Filchak, K. E., Roethele, J. B. and Feder, J. L. (2000). Natural selection and sympatric divergence in the Apple maggot Rhagoletis pomonella. Nature, London 407, 739–742.CrossRefGoogle ScholarPubMed
Giorgi, M. S., Arletazz, R., Guillaume, F., Nussle, S., Ossola, C., Vogel, P. and Christe, P. (2004). Causal mechanism underlying host specificity in bat ectoparasites. Oecologia 138, 648–654.CrossRefGoogle ScholarPubMed
Grimaldi, D. (1997). The birds flies, Genus Carnus: species revision, generic relationships and a fossil Meoneura in amber (Diptera: Carnidae). American Museum Novitates 3190, 1–30.Google Scholar
Guiguen, C., Launay, H. and Beaucournu, J. C. (1983). Ectoparasites des oiseaux en Bretagne. I. Rèpartition et écologie d'un diptère hematophage nouveau pour la France: Carnus hemapterus Nitzsch. Revue Francaise d'Entomologie 5, 54–62.Google Scholar
Hodek, I. (2002). Controversial aspects of diapause development. European Journal of Entomology 99, 163–173.CrossRefGoogle Scholar
Hoffmann, A. A., Sorensen, J. G. and Loeschcke, V. (2003). Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology 28, 175–216.CrossRefGoogle Scholar
Kemp, W. P. and Bosch, J. (2005). Effect of temperature on Osmia lignaria (Hymenoptera: Megachilidae) prepupa – adult development, survival, and emergence. Journal of Economical Entomology 98, 1917–1923.CrossRefGoogle ScholarPubMed
Kostal, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
Leather, S. R., Walters, K. A. and Bale, J. S. (1993). The Ecology of Insect Overwintering. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Liker, A., Markus, M., Vozár, A., Zemankovics, E. and Rózsa, L. (2001). Distribution of Carnus hemapterus in a starling colony. Canadian Journal of Zoology 79, 574–580.CrossRefGoogle Scholar
Lill, A. and Fell, P. J. (2007). Microclimate of nesting burrows of the Rainbow Bee-eater. Emu 107, 108–114.CrossRefGoogle Scholar
Marshall, A. G. (1981). The Ecology of Ectoparasitic Insects. Academic Press, London, UK.Google Scholar
Martín-Vivaldi, M., Palomino, J. J., Soler, M. and Soler, J. J. (1999). Determinants of reproductive success in the Hoopoe Upupa epops, a hole-nesting non-passerine bird with asynchronous hatching. Bird Study 46, 205–216.CrossRefGoogle Scholar
Masaki, S. (2002). Ecophysiological consequences of variability in diapause intensity. European Journal of Entomology 99, 143–154.CrossRefGoogle Scholar
Nijhout, H. F. (1999). Control mechanism of polyphonic development in insects. BioScience 49, 181–192.CrossRefGoogle Scholar
Nyman, T. (2002). The willow bud galler Euura mucronata Hartig (Hymenoptera: Tenthredinidae): one polyphage or many monophages? Heredity 88, 288–295.CrossRefGoogle ScholarPubMed
Poulin, R. (1998). Evolutionary Ecology of Parasites. Chapman and Hall. London, UK.Google Scholar
Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129 (Suppl.), S37–S65.CrossRefGoogle ScholarPubMed
Rolff, J. (2000). Water mite parasitism in damselflies during emergence: Two hosts, one pattern. Ecography 23, 273–282.CrossRefGoogle Scholar
Roulin, A. (1998). Cycle de reproduction et abundance du diptére parasite Carnus hemapterus dans le niches de chouettes effraies Tyto alba. Alauda 66, 265–272.Google Scholar
Smith, B. P. and McIver, S. (1984). The patterns of mosquito emergence (Diptera: Culicida; Aedes spp.): their influence on host selection by parasitic mites (Acari: Arrenuridae; Arrenurus spp.). Canadian Journal of Zoology 62, 1106–1113.CrossRefGoogle Scholar
Tauber, C. A. and Tauber, M. J. (1981). Insect seasonal cycles: genetics and evolution. Annual Review of Ecology and Systematics 12, 281–308.CrossRefGoogle Scholar
Tauber, M. J., Tauber, C. A. and Masaki, S. (1986). Seasonal Adaptations of Insects. Oxford University Press, Oxford, UK.Google Scholar
Teixeira, L. A. F. and Polavarapu, S. (2002). Phenological differences between populations of Rhagoletis mendax (Diptera: Tephritidae). Environmental Entomology 31, 1103–1109.CrossRefGoogle Scholar
Tikkanen, O. P. and Lyytikainen – Saarenmaa, P. (2002). Adaptation of a generalist moth, Operophtera brumata, to variable budburst phenology of host plants. Entomologia Experimentalis et Applicata 103, 123–133.CrossRefGoogle Scholar
Tripet, F. and Richner, H. (1999). Dynamics of hen flea Ceratophyllus gallinae subpopulations in blue tit nests. Journal of Insect Behaviour 12, 159–174.CrossRefGoogle Scholar
Valera, F., Casas-Crivillé, A. and Hoi, H. (2003). Interspecific parasite exchange in a mixed colony of birds. Journal of Parasitology 89, 245–250.CrossRefGoogle Scholar
Valera, F., Casas-Crivillé, A. and Calero-Torralbo, M. A. (2006 a). Prolonged diapause in the ectoparasite Carnus hemapterus (Diptera: Cyclorrapha, Acalyptratae) – how frequent is it in parasites? Parasitology 133, 179–186.CrossRefGoogle Scholar
Valera, F., Martín-Vivaldi, M. and Carles-Tolrá, M. (2006 b). Life-history variation in three coexisting species of Carnid flies (Diptera: Carnidae), Carnus hemapterus, Hemeromyia anthracina and Hemeromyia longirostris. European Journal of Entomology 103, 347–353.CrossRefGoogle Scholar
Von Ende, C. N. (2001). Repeated-measures analysis: growth and other time-dependent measures. In Design and Analysis of Ecological Experiments (ed. Scheiner, S. M. and Gurevitch, J.), pp. 134–157. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Weinig, C. and Schmitt, J. (2004). Environmental effects on the expression of quantitative trait loci and implications for phenotypic evolution. Bioscience 54, 627–635.CrossRefGoogle Scholar
Webb, D. R. (1987). Thermal tolerance of avian embryos: a review. Condor 89, 874–898.CrossRefGoogle Scholar
West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. Oxford University Press, New York, UK.CrossRefGoogle Scholar
Wetzel, E. J. and Weigl, P. D. (1994). Ecological implications for Flying Squirrels (Glaucomys spp.) of effects of temperature on the in-vitro depelopment and behaviour of Strongyloides robustus. American Midland Naturalist 131, 43–54.CrossRefGoogle Scholar
Wharton, D. A. (1999). Parasites and low temperatures. Parasitology 119 (Suppl.), S7–S17.CrossRefGoogle ScholarPubMed