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Temperature during the free-living phase of an ectoparasite influences the emergence pattern of the infective phase

Published online by Cambridge University Press:  22 July 2013

M. AMAT-VALERO ,
M. A. CALERO-TORRALBO  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
M. A. CALERO-TORRALBO
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
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

Understanding the population dynamics and co-evolution of host–parasite systems requires detailed knowledge of their phenology which, in turn, requires a deep knowledge of the effect of abiotic factors on the life cycles of organisms. Temperature is known to be a key environmental influence that participates in the regulation of diapause. Yet, not much is known about the effect of temperature on the free-living stages of true parasites and how it may influence host–parasite interactions. Here we experimentally study the effect of ambient temperature on overwintering pupae of Carnus hemapterus (Diptera, Carnidae), an ectoparasitic fly of various bird species. We also test whether chilling is a prerequisite for completion of diapause in this species. In the course of three winter seasons we experimentally exposed carnid pupae from nests of various host species to spring temperatures with and without chilling and recorded the emergence patterns in experimental and control groups. Experimental groups showed an advanced emergence date, a lower emergence rate and, consequently, a protracted emergence period. Chilling had no obvious effect on the start of emergence but it did advance the mean emergence date, shortened the length of the emergence period when compared with the control treatment and increased the emergence rate when compared with the spring treatment. This study identifies an environmental cue, namely temperature during the free-living stage, affecting the emergence of a widespread parasite and demonstrates the plasticity of diapause in this parasite. Our findings are of potential significance in understanding host–parasite interactions.

Keywords

Carnus hemapterusdiapauseemergenceparasitehost–parasite synchronizationlife cycleplasticitytemperature
Type
Research Article
Information
Parasitology , Volume 140 , Issue 11 , September 2013 , pp. 1357 - 1367
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Amat-Valero, M., Vaclav, R., Martínez, T. and Valera, F. (2012). Mixed life-history strategies in a local population of the ectoparasitic fly Carnus hemapterus. Parasitology 139, 1045–1053.CrossRefGoogle Scholar
Anderson, J. F. and Kaya, H. K. (1975). Influence of temperature on diapause termination in Ooencyrtus ennomus, an ELM spanworm egg parasitoid. Annals of the Entomological Society of America 68, 671–672.CrossRefGoogle Scholar
Anderson, R. L. (1970). Temperature acclimation in Tribolium confusum and Musca domestica: rate of acclimation measured at locomotory, metabolic and enzyme levels. Journal of Insect Physiology 17, 2205–2219.CrossRefGoogle Scholar
Bequaert, J. (1942). Carnus hemapterus Nitzsch, an ectoparasitic fly of birds, new to America (Diptera). Bulletin of the Brooklyn Entomological Society 37, 140–149.Google Scholar
Biron, D., Langlet, X., Boivin, G. and Brunel, E. (1998). Expression of early and late emerging phenotypes in both diapausing and non-diapausing Delia radicum L. pupae. Entomologia Experimentalis et Applicata 87, 119–124.CrossRefGoogle Scholar
Blanckenhorn, W. U. (1998). Adaptive phenotypic plasticity in growth, development, and body size in the yellow dung fly. Evolution 52, 1394–1407.CrossRefGoogle ScholarPubMed
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
Bush, A. O., Fernandez, J. C. and Esch, G. W. (2001). Parasitism: the Diversity and Ecology of Animal Parasites. Cambridge University Press, New York, USA.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
Calero-Torralbo, M. A., Václav, R. and Valera, F. (2013). Intra-specific variability in life-cycle synchronization of an ectoparasitic fly to its avian host. Oikos 122, 274–284.CrossRefGoogle Scholar
Cramp, S. and Perrins, C. M. (1994). Handbook of the Birds of Europe, the Middle East and North Africa, Vol. VIII. Oxford University Press, Oxford, UK.Google Scholar
Danks, H. V. (1987). Insect Dormancy: an Ecological Perspective. Biological Survey of Canada No. 1, Ottawa, ON, Canada.Google Scholar
Dawson, R. D., Hillen, K. K. and Whitworth, T. L. (2005). Effects of experimental variation in temperature on larval densities of parasitic Protocalliphora (Diptera: Calliphoridae) in nests of tree swallows (Passeriformes: Hirundinidae). Environmental Entomology 34, 563–568.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
Gray, D. R., Ravlin, F. W. and Braine, J. A. (2001). Diapause in the gypsy moth: a model of inhibition and development. Journal of Insect Physiology 47, 173–184.CrossRefGoogle 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, 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
Hance, T., van Baaren, J., Vernon, P. and Boivin, G. (2007). Impact of extreme temperatures on parasitoids in a climate change perspective. Annual Review of Entomology 52, 107–126.CrossRefGoogle Scholar
Hodek, I. (1983). Role of environmental factors and endogenous mechanisms in the seasonality of reproduction in insects diapausing as adults. Series Entomologica (Dordrecht) 23, 9–33.Google Scholar
Hodek, I. (1996). Diapause development, diapause termination and the end of diapause. European Journal of Entomology 93, 475–487.Google Scholar
Hodek, I. (2002). Controversial aspects of diapause development. European Journal of Entomology 99, 163–173.CrossRefGoogle Scholar
Hopper, K. R. (1999). Risk-spreading and bet-hedging in insect population biology. Annual Review of Entomology 44, 535–560.CrossRefGoogle ScholarPubMed
Kato, Y. and Sakate, S. (1981). Studies on summer diapause in pupae of Antheraea yamamai (Lepidoptera, saturniidae).·3. Influence of photoperiod in the larval stage. Applied Entomology and Zoology 16, 499–500.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 Economic Entomology 98, 1917–1923.CrossRefGoogle ScholarPubMed
Kostal, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
Langer, A. and Hance, T. (2000). Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera : Braconidae : Aphidiinae). Journal of Insect Physiology 46, 671–676.CrossRefGoogle ScholarPubMed
Leather, S. R., Walters, K. F. A. and Bale, J. S. (1993). The Ecology of Insect Overwintering. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Lees, A. D. (1950). The physiology of diapause. Science Progress 38, 735–742.Google 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
Masaki, S. (2002). Ecophysiological consequences of variability in diapause intensity. European Journal of Entomology 99, 143–154.CrossRefGoogle Scholar
Masaki, S., Ando, Y. and Watanabe, A. (1979). High temperature and diapause termination in the eggs of Teleogryllus commodus (Orthoptera: Gryllidae). Kontyu 47, 493–504.Google Scholar
Menu, F., Roebuck, J. P. and Viala, M. (2000). Bet-hedging diapause strategies in stochastic environments. American Naturalist 155, 724–734.CrossRefGoogle ScholarPubMed
Merino, S. and Potti, J. (1996). Weather dependent effects of nest ectoparasites on their bird hosts. Ecography 19, 107–113.CrossRefGoogle Scholar
Milonas, P. G. and Savopoulou-Soultani, M. (2000). Diapause induction and termination in the parasitoid Colpoclypeus florus (Hymenoptera : Eulophidae): role of photoperiod and temperature. Annals of the Entomological Society of America 93, 512–518.CrossRefGoogle Scholar
Nechols, J. R., Tauber, M. J. and Helgesen, R. G. (1980). Environmental-control of diapause and post-diapause development in Tetrastichus julis (Hymenoptera, eulophidae), a parasite of the cereal leaf beetle, Oulema melanopus (Coleoptera, chrysomelidae). Canadian Entomologist 112, 1277–1284.CrossRefGoogle Scholar
Pitts, K. M. and Wall, R. (2006). Cold shock and cold tolerance in larvae and pupae of the blow fly, Lucilia sericata. Physiological Entomology 31, 57–62.CrossRefGoogle Scholar
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, S37–S65.CrossRefGoogle ScholarPubMed
Reiczigel, J. and Rozsa, L. (2005). Quantitative Parasitology 3.0. Budapest, Hungary.Google Scholar
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
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
Shimoda, M. and Kiuchi, M. (1997). Effect of chilling of diapause pupa on adult emergence in the sweet potato hornworm, Agrius convolvuli (Lepidoptera; Sphingidae). Applied Entomology and Zoology 32, 617–624.CrossRefGoogle Scholar
Tauber, M. J. and Tauber, C. A. (1975). Natural daylengths regulate insect seasonality by two mechanisms. Nature 258, 711–712.CrossRefGoogle ScholarPubMed
Tauber, M. J., Tauber, C. A. and Masaki, S. (1986). Seasonal Adaptation 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
Teixeira, L. A. F. and Polavarapu, S. (2005). Evidence of a heat-induced quiescence during pupal development in Rhagoletis mendax (Diptera: Tephritidae). Environmental Entomology 34, 292–297.CrossRefGoogle Scholar
Thomas, M. B. and Blanford, S. (2003). Thermal biology in insect-parasite interactions. Trends in Ecology and Evolution 18, 344–350.CrossRefGoogle Scholar
Václav, R., Valera, F. and Martínez, T. (2011). 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). 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). Prolonged diapause in the ectoparasite Carnus hemapterus (Diptera: Cyclorrapha, Acalyptratae) – how frequent is it in parasites? Parasitology 133, 179–186.CrossRefGoogle Scholar
van Dijk, J. and Morgan, E. R. (2008). The influence of temperature on the development, hatching and survival of Nematodirus battus larvae. Parasitology 135, 269–283.CrossRefGoogle ScholarPubMed
von Ende, C. N. (2001). Repeated-measures analysis: growth and other time dependent measures. In The Design and Analysis of Ecological Experiments (ed. Scheiner, S. and Gurevitch, I.), pp. 134–157. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Waldbauer, G. P. (1978). Phenological Adaptation and the Polymodal Emergence Patterns of Insects. Springer-Verlag, New York, USA.CrossRefGoogle Scholar
Waldbauer, G. P. and Sternburg, J. G. (1986). The bimodal emergence curve of adult Hyalophora cecropia: conditions required for the initiation of development by second mode pupae. Entomologia Experimentalis et Applicata 41, 315–317.CrossRefGoogle Scholar
Wall, R., French, N. and Morgan, K. L. (1992). Effects of temperature on the development and abundance of the sheep blowfly Lucilia sericata (Diptera: Calliphoridae). Bulletin of Entomological Research 82, 125–131.CrossRefGoogle Scholar
Wharton, D. A. (1999). Parasites and low temperatures. Parasitology 119(Suppl.), S7–S17.CrossRefGoogle ScholarPubMed
William, C. M. and Adkisson, P. L. (1964). Physiology of insect diapause. XIV. An endocrine mechanism for the photoperiod control of pupal diapause in the Oak silkworm, Anthieraea pernyi. Biological Bulletin 127, 511–525.CrossRefGoogle Scholar
Zar, J. (1984). Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, NJ, USA.Google Scholar