Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T17:33:51.716Z Has data issue: false hasContentIssue false

Prolonged diapause in the ectoparasite Carnus hemapterus (Diptera: Cyclorrhapha, Acalyptratae) – how frequent is it in parasites?

Published online by Cambridge University Press:  20 April 2006

F. VALERA
Affiliation:
Estación Experimental de Zonas Áridas (CSIC), General Segura 1, E-04001, Almería, Spain
A. CASAS-CRIVILLÉ
Affiliation:
Konrad Lorenz Institut for Ethology, Austrian Academy of Sciences, Savoyenstrasse 1a, A-1160, Vienna, Austria
M. A. CALERO-TORRALBO
Affiliation:
Estación Experimental de Zonas Áridas (CSIC), General Segura 1, E-04001, Almería, Spain

Abstract

Prolonged diapause is usually interpreted as an adaptation to unpredictable environmental conditions and resource availability. Many parasites usually face highly unpredictable environments, therefore prolonged diapause should be common among these organisms. Here we examine the occurrence and frequency of prolonged diapause in the ectoparasite Carnus hemapterus (Diptera: Cyclorrhapha, Acalyptratae). We found that the studied population is polymorphic with respect to diapause duration. Emergence of carnid flies after 2 and 3 wintering seasons was therefore detected in around 17% and 21% of the samples respectively. The number of flies with prolonged diapause ranked 0·88–50% with respect to the number of flies emerging during the first spring. Both the occurrence of prolonged diapause and the number of flies with a long life-cycle are related to the number of flies emerging during the first spring. The emergence pattern of flies with prolonged diapause was very similar to that observed for flies with a short cycle and occurred in synchrony with the occurrence of hosts. Prolonged diapause has been frequently reported in plant-feeding insects and in some host-parasitoid systems, but this is, to our knowledge, the second report ever on prolonged diapause in true parasites of animals. We discuss the reasons for the apparent rarity of prolonged diapause among these organisms.

Type
Research Article
Copyright
2006 Cambridge University Press

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

Baird, C. R. ( 1975). Larval development of the rodent botfly, Cuterebra tenebrosa, in bushy-tailed wood rats and its relationship to pupal diapause. Canadian Journal of Zoology 53, 17881798.CrossRefGoogle Scholar
Bohonak, A. J. and Jenkins, D. G. ( 2003). Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecology Letters 6, 783796.CrossRefGoogle Scholar
Capelle, K. J. and Whitworth, T. L. ( 1973). The distribution and avian hosts of Carnus hemapterus (Diptera: Milichiidae) in North America. Journal of Medical Entomology 10, 525526.CrossRefGoogle Scholar
Clauss, M. J. and Venable, D. L. ( 2000). Seed germination in desert annuals: an empirical test of adaptive bet hedging. American Naturalist 155, 168186.CrossRefGoogle Scholar
Danks, H. V. ( 1987). Insect dormancy: an ecological perspective. Biological Survey of Canada No. 1, Ottawa, Ontario.
Danks, H. V. ( 1992). Long life cycles in insects. Canadian Entomologist 124, 167187.CrossRefGoogle Scholar
Dawson, R. D. and Bortolotti, G. R. ( 1997). Ecology of parasitism of nestling American Kestrels by Carnus hemapterus (Diptera, Carnidae). Canadian Journal of Zoology 75, 20212026.CrossRefGoogle Scholar
Debouzie, D. and Menu, F. ( 1992). Prolonged diapause frequency in experimental chestnut weevil Curculio elephas populations. Acta Oecologica 13, 315324.Google Scholar
Enright, J. T. ( 1970). Ecological aspects of endogenous rhythmicity. Annual Review of Ecology and Evolution 1 (Suppl.), S221S238.CrossRefGoogle Scholar
Fenton, A. and Hudson, P. J. ( 2002). Optimal infection strategies: should macroparasites hedge their bets? Oikos 96, 92101.Google Scholar
Grimaldi, D. ( 1997). The bird flies, Genus Carnus: species revision, generic relationships and a fossil Meoneura in amber (Diptera: Carnidae). American Museum Novitates 3190, American Museum of Natural History, New York, USA.
Guiguen, C., Launay, H. and Beaucournu, J. C. ( 1983). Ectoparasites des oiseaux en Bretagne. I. Répartition et écologie d'un diptère hematophage nouveau pour la France: Carnus hemapterus Nitzsch. Revue française d'Entomologie 5, 5462.Google Scholar
Hairston, N. G. ( 2000). Temporal dispersal: ecological and evolutionary implications of prolonged egg diapause. American Zoologist 40, 10391040.Google Scholar
Hairston, N. G. and Kearns, C. M. ( 2002). Temporal dispersal: ecological and evolutionary aspects of zooplankton egg banks and the role of sediment mixing. Integrative and Comparative Biology 42, 481491.CrossRefGoogle Scholar
Hanski, I. ( 1988). Four kinds of extra long diapause in insects: a review of theory and observations. Annales Zoologici Fennici 25, 3753.Google Scholar
Hakalahti, T., Hakkinen, H. and Valtonen, E. T. ( 2004). Ectoparasitic Argulus coregoni (Crustacea: Branchiura) hedge their bets – studies on egg hatching dynamics. Oikos 107, 295302.CrossRefGoogle Scholar
Hopper, K. R. ( 1999). Risk-spreading and bet-hedging in insect population biology. Annual Review of Entomology 44, 535560.CrossRefGoogle Scholar
Jones, R. E. ( 2001). Mechanisms for locating resources in space and time: impacts on the abundance of insect herbivores. Austral Ecology 26, 518524.CrossRefGoogle Scholar
Kirkpatrick, C. E. and Colvin, B. A. ( 1989). Ectoparasitic fly Carnus hempaterus (Diptera: Carnidae) in a nesting population of common barn-owls (Strigiformes: Tytonidae). Journal of Medical Entomology 26, 109112.CrossRefGoogle Scholar
Leather, S. R., Walters, K. F. A. and Bale, J. S. ( 1993). The Ecology of Insect Overwintering. Cambridge University Press, Cambridge.CrossRef
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, 574580.CrossRefGoogle Scholar
Loye, J. E. and Carroll, S. P. ( 1998). Ectoparasite behavior and its effects on avian nest site selection. Annals of the Entomological Society of America 91, 159163.CrossRefGoogle 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, 205216.CrossRefGoogle Scholar
Menu, F. ( 1993). Strategies of emergence in the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia 96, 383390.CrossRefGoogle Scholar
Menu, F. and Debouzie, D. ( 1993). Coin-flipping plasticity and prolonged diapause in insects: example of the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia 93, 367373.CrossRefGoogle Scholar
Menu, F. and Desouhant, E. ( 2002). Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause. Oecologia 132, 167174.CrossRefGoogle Scholar
Menu, F., Roebuck, J. P. and Viala, M. ( 2000). Bet-hedging diapause strategies in stochastic environments. American Naturalist 155, 724734.Google Scholar
Philippi, T. ( 1993 a). Bet-hedging germination of desert annuals – beyond the 1st year. American Naturalist 142, 474487.Google Scholar
Philippi, T. ( 1993 b). Bet-hedging germination of desert annuals – variation among populations and maternal effects in Lepidium lasiocarpum. American Naturalist 142, 488507.Google Scholar
Powell, J. A. ( 1989). Synchronized, mass-emergences of a yucca moth, Prodoxus y-inversus (Lepidoptera: Prodoxidae), after 16 and 17 years in diapause. Oecologia 81, 490493.CrossRefGoogle Scholar
Powell, J. A. ( 2001). Longest insect dormancy: yucca moth larvae (Lepidoptera: Prodoxidae) metamorphose after 20, 25, and 30 years in diapause. Annals of the Entomological Society of America 94, 677680.CrossRefGoogle Scholar
Reiczigel, J. and Rózsa, L. ( 2001). Quantitative Parasitology 2.0. Distributed by the authors. Budapest, Hungary.
Rózsa, L., Reiczigel, J. and Majoros, G. ( 2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228232.CrossRefGoogle Scholar
Roulin, A. ( 1998). Cycle de reproduction et abondance du diptère parasite Carnus hemapterus dans les nichées de chouettes effraies Tyto alba. Alauda 66, 265272.Google Scholar
Roulin, A. ( 1999). Fécondité de la mouche Carnus hemapterus, ectoparasite des jeunes chouettes effraies Tyto alba. Alauda 67, 205212.Google Scholar
Smith, B. P. and McIver, S. ( 1984). The patterns of mosquito emergence (Diptera: Culicidae; Aedes spp.): their influence on host selection by parasitic mites (Acari: Arrenuridae; Arrenurus spp.). Canadian Journal of Zoology 62, 11061113.Google Scholar
Seger, J. and Brockmann, H. J. ( 1987). What is bet-hedging? Oxford Survey in Evolutionary Biology 4, 182211.Google Scholar
Soula, B. and Menu, F. ( 2003). Variability in diapause duration in the chestnut weevil: mixed ESS, genetic polymorphism or bet-hedging? Oikos 100, 574580.Google Scholar
Soula, B. and Menu, F. ( 2005). Extended life cycle in the chestnut weevil: prolonged or repeated diapause? Entomologia Experimentalis et Applicata 115, 333340.Google Scholar
Southwood, T. R. E. ( 1977). Habitat, the templet for ecological strategies. Journal of Animal Ecology 46, 337365.CrossRefGoogle Scholar
STATSOFT, INC. ( 2001). STATISTICA for Windows. StatSoft, Inc., Tulsa, OK, USA.
Tauber, C. A. and Tauber, M. J. ( 1981). Insect seasonal cycles: genetics and evolution. Annual Review of Ecology and Systematics 12, 281308.CrossRefGoogle Scholar
Tauber, M. J., Tauber, C. A. and Masaki, S. ( 1986). Seasonal Adaptations of Insects. Oxford University Press, Oxford.
Valera, F., Casas-Crivillé, A. and Hoi, H. ( 2003). Interspecific parasite exchange in a mixed colony of birds. Journal of Parasitology 89, 245250.CrossRefGoogle Scholar
Valera, F., Martín-Vivaldi, M. and Carles-Tolrá, M. ( 2006). Life-history variation in three coexisting species of Carnid flies (Diptera: Carnidae), Carnus hemapterus, Hemeromyia anthracina and Hemeromyia longirostris. European Journal of Entomology (in the Press).CrossRefGoogle Scholar
Ward, S. A., Leather, S. R., Pickup, J. and Harrington, R. (1998). Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology 67, 763773.Google Scholar