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Mixed life-history strategies in a local population of the ectoparasitic fly Carnus hemapterus

Published online by Cambridge University Press:  01 May 2012

M. AMAT-VALERO ,
R. VÁCLAV ,
T. MARTÍNEZ  and
F. VALERA
M. AMAT-VALERO*
Affiliation:
Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. Sacramento s/n, La Cañada de San Urbano, 04120 Almería, Spain
R. VÁCLAV
Affiliation:
Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9, 84506 Bratislava, Slovakia
T. MARTÍNEZ
Affiliation:
C/Catavieja 31. 1°B, 04007 Almería, Spain
F. VALERA
Affiliation:
Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. Sacramento s/n, La Cañada de San Urbano, 04120 Almería, Spain
*
*Corresponding author: Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Ctra. Sacramento s/n, La Cañada de San Urbano, 04120 Almería, Spain. E-mail: amat@eeza.csic.es
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Summary

A major issue for the proper understanding of the evolution of life-cycle histories is the regulation of voltinism and its variation. Diapause characteristics are known to regulate voltinism, but the underlying mechanisms are poorly understood. This paper studies diapause duration and voltinism variation in a haematophagous diptera parasitizing 2 sympatric hosts with very different breeding phenologies. We hypothesize that bivoltinism will be more frequent in carnid flies parasitizing an early breeding, multi-brooded species than in flies parasitizing a late breeder, single-brooded species. We obtained evidence of the co-occurrence of uni- and bivoltinism in both clutches of the multi-brooded Spotless starling (Sturnus unicolor) as well as in clutches of the single-brooded European roller (Coracias garrulus). Unexpectedly, the proportion of bivoltine flies was similar in both host species. A remarkable degree of host-parasite synchronization at the population level was found for bivoltine flies. Our findings reveal the facultative nature of diapause in Carnus. We discuss the influence of abiotic conditions and host availability on polymorphism in life-history cycles and the consequences both for the parasite and the host.

Keywords

Carnus hemapterusvoltinismdiapauselife-history strategiesphenotypic plasticity
Type
Research Article
Information
Parasitology , Volume 139 , Issue 8 , July 2012 , pp. 1045 - 1053
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Bradford, M. J. and Roff, D. A. (1993). Bet hedging and the diapause strategies of the cricket Allonemobius fasciatus. Ecology (Washington D C) 74, 1129–1135.Google Scholar
Calero-Torralbo, M. A. and Valera, F. (2008). Synchronization of host-parasite cycles by means of diapause: host influence and parasite response to involuntary host shifting. Parasitology 135, 1343–1352.CrossRefGoogle ScholarPubMed
Campbell, A. and Mackauer, M. (1975). Thermal constants for development of the pea aphid (homoptera: aphididae) and some of its parasites. The Canadian Entomologist 107, 419–423.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, 525–526.CrossRefGoogle ScholarPubMed
Cramp, S. (1998). Handbook of the Birds of Europe, Middle East and North Africa. Vol.IV. Oxford University Press, Oxford, UK.Google Scholar
Danforth, B. N. (1999). Emergence dynamics and bet hedging in a desert bee, Perdita portalis. Proceedings of the Royal Society of London, B 266, 1985–1994.CrossRefGoogle 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. (2002). The range of insect dormancy responses. European Journal of Entomology 99, 127–142.CrossRefGoogle Scholar
Danks, H. V. and Foottit, R. G. (1989). Insects of the boreal zone of Canada. Canadian Entomologist 121, 625–690.CrossRefGoogle Scholar
Dawson, R. D. and Bortolotti, G. R. (1997). Ecology of parasitism of nestling American Kestrels by Carnus hemapterus (Diptera, Carnidae). Canasian Journal of Zoology 75, 2021–2026.CrossRefGoogle Scholar
Denlinger, D. L. and Bradfield, J. Y. IV. (1981). Duration of pupal diapause in the tobacco hornworm is determined by number of short days received by the larva. Journal of Experimental Biology 91, 331–337.CrossRefGoogle Scholar
Gag, S. H. and Haynes, D. L. (1975). Emergence under natural and manipulated conditions of Tetrastichus julis, an introduced larval parasite of the cereal leaf beetle, with reference to regional population management. Environmental Entomology 4, 425–434.CrossRefGoogle Scholar
Gerber, G. H. (1984). Influence of date of oviposition on egg hatching and embryo survival in the red turnip beetle, Entomoscelis americana (Coleoptera: Chrysomelidae). Canadian Entomologist 116, 645–652.CrossRefGoogle Scholar
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
He, X. Z., Wang, Q., Walker, J. T. S., Rogers, D. J. and Lo, P. L. (2010). A sophisticated life history strategy in a parasitoid wasp: Producing univoltine and multivoltine phenotypes in a local population. Biological Control 54, 276–284.CrossRefGoogle Scholar
Hilbert, D. W, Logan, J. A. and Swift, D. M. (1985). A unifying hypothesis of temperature effects on egg development and diapause of the migratory grasshopper, Melanoplus sanguinipes (Orthoptera: Acrididae). Journal of Theoretical Biology 112, 827–838.CrossRefGoogle Scholar
Hopper, K. R. (1999). Risk-spreading and bet-hedging in insect population biology. Annual Review of Entomology 44, 535–560.CrossRefGoogle ScholarPubMed
Kivelä, S. M., Välimäki., P., Oksanen, J., Kaitala, A. and Kaitala, V. (2009). Clines of evolutionary stable reproductive effort in insects. The American Naturalist 174, 526–536.CrossRefGoogle ScholarPubMed
Kostal, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
Kurota, H. and Shimada, M. (2001). Photoperiod- and temperature-dependent induction of larval diapause in a multivoltine bruchid, Bruchidius dorsalis. Entomologia Experimentalis et Applicata 99, 361–369.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
López-Rull, I., Gil, M. and Gil, D. (2007). Spots in starling Sturnus unicolor eggs are good indicators of ectoparasite load by Carnus hemapterus (Diptera: Carnidae). Ardeola 54, 131–134.Google Scholar
Masaki, S. (1980). Summer diapause. Annual Review of Entomology 25, 1–25.CrossRefGoogle Scholar
Matyukhin, A. V. and Krivosheina, M. G. (2008). To the knowledge of Diptera (Insecta)- Parasites of birds. Zoologichesky Zhurnal 87, 124–125.Google Scholar
Menu, F. (1993). Strategies of emergence in the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia, Berlin 96, 383–390.CrossRefGoogle ScholarPubMed
Menu, F. and Debouzie, D. (1993). Coin-flipping plasticity and prolonged diapause in insects: example of the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia, Berlin 93, 367–373.CrossRefGoogle ScholarPubMed
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, Berlin 132, 167–174.CrossRefGoogle ScholarPubMed
Menu, F., Roebuck, J. P. and Viala, M. (2000). Bet-hedging diapause strategies in stochastic environments. American Naturalist 155, 724–734.CrossRefGoogle ScholarPubMed
Papp, L. (1998). Family Carnidae. Manual of Palaearctic Diptera 3, 211–217.Google Scholar
Parrish, D. S. and Davis, D. W. (1978). Inhibition of diapause in Bathyplectes curculionis, a parasite of the alfalfa weevil. Annals of the Entomological Society of America 71, 103–107.CrossRefGoogle Scholar
Peris, A. S. (1984). Descripción y desarrollo del pollo del estornino negro. Ardeola 31, 3–16.Google Scholar
Price, T. D., Qvarnstrom, A. and Irwin, D. E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society of London, B 270, 1433–1440.CrossRefGoogle ScholarPubMed
Reiczigel, J., Abonyi-Tóth, Z. and Singer, J. (2008). An exact confidence set for two binomial proportions and exact unconditional confidence intervals for the difference and ratio of proportions. Computational Statistics and Data Analysis 52, 5046–5053.CrossRefGoogle Scholar
Reiczigel, J. and Rozsa, L. (2005). Quantitative Parasitology 3.0. Budapest, Hungary. Distributed by the authors.Google Scholar
Roff, D. (1980). Optimizing development time in a seasonal environment: the ‘ups and downs’ of clinal variation. Oecologia, Berlin 45, 202–208.CrossRefGoogle Scholar
Roff, D. (1983). Phenological adaptation in a seasonal environment: a theoretical perspective. Series Entomologica, Dordrecht 23, 253–270.Google 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
Sabelis, M. W. and Janssen, A. (1994). Evolution of life-history patterns in the Phytoseiidae. In Mites: Ecological and Evolutionary Analyses of Life-History Patterns (ed. Houck, M. A.), pp. 70–98. Chapman and Hall; New York, USA and London, UK.CrossRefGoogle Scholar
Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24, 35–68.CrossRefGoogle Scholar
Schlichting, C. D. and Pigliucci, M. (1998). Phenotypic Evolution: a Reaction Norm Perspective. Sinauer Asociates, Sinauer, MA, USA.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, 574–580.CrossRefGoogle Scholar
Sota, T. (1988). Ecology of a gall-forming thrips, Ponticulothrips diospyrosi: colony development and gall-associated arthropod community (Thysanoptera: Phaleothripidae). Applied Entomology and Zoology 23, 345–352.CrossRefGoogle Scholar
Stearns, S. C. (1976). Life history tactics: a review of the ideas. Quarterly Review of Biology 51, 3–47.CrossRefGoogle ScholarPubMed
Takafuji, A. and Morimoto, N. (1983). Diapause attributes and seasonal occurrences of two populations of the citrus red mite, Panonychus citri (McGregor) on pear (Acarina: Tetranychidae). Applied Entomology and Zoology 18, 525–532.CrossRefGoogle Scholar
Tauber, M. J. and Tauber, C. A. (1970). Adult diapause in Chrysopa carnea: Stages sensitive to photoperiodic induction. Journal of Insect Physiology 16, 2075–2080.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
Taylor, F. and Spalding, J. B. (1988). Fitness functions for alternative developmental pathways in the timing of diapause induction. The American Naturalist 131, 678–699.CrossRefGoogle Scholar
Tillman, P. G. and Powell, J. E. (1991). Developmental time in relation to temperature for Microplitis croceipes, M. Demolitor, Cotesia kazak (Hymenoptera: Braconidae), and Hyposoter didymator (Hymenoptera: Ichneumonidae), endoparasites of the tobacco budworm (Lepidoptera: Noctuidae). Environmental Entomology 20, 61–64.CrossRefGoogle Scholar
Tyshchenko, V. P. and Kind, T. V. (1983). Neuroendocrine mechanisms regulating the seasonal cycles. Trudy Vsesoyuznogo Entomologicheskogo Obshchestva 64, 82–117.Google Scholar
Václav, R., Valera, F. and Martínez, T. (2010). Social information in nest colonisation and occupancy in a long-lived, solitary breeding bird. Oecologia 165, 617–627.CrossRefGoogle Scholar
Valera, F., Casas-Crivillé, A. and Hoi, H. (2003). Interespecific 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). Prolonged diapause in the ectoparasite Carnus hemapterus (Diptera: Cyclorrapha, Acalyptratae) – how frequent is it in parasites? Parasitology 133, 179–186.CrossRefGoogle Scholar
Valimaki, P., Kivela, S. M. and Jaaskelainen, L. (2008). Divergent timing of egg-laying may maintain life history polymorphism in potentially multivoltine insects in seasonal environments. Journal of Evolutionary Biology 21, 1711–1723.CrossRefGoogle ScholarPubMed
Via, S. (1992). Adaptive phenotypic plasticity: target or by-product of selection in a variable environment? The American Naturalist 142, 352–365.CrossRefGoogle Scholar
Winterhalter, W. E. and Mousseau, T. A. (2007). Patterns of phenotypic and genetic variation for the plasticity of diapause incidence. Proceedings of the Royal Society of London, B 274, 1211–1217.Google Scholar