Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T00:06:16.524Z Has data issue: false hasContentIssue false
  • English
  • Français

Unexpected seasonal variation in offspring size and performance in a viviparous ectoparasite

Published online by Cambridge University Press:  12 October 2012

LAURA HÄRKÖNEN ,
EIJA HURME  and
ARJA KAITALA
LAURA HÄRKÖNEN*
Affiliation:
Department of Biology, University of Oulu, PO Box 3000, FI-90014 Oulu, Finland
EIJA HURME
Affiliation:
Department of Biology, University of Oulu, PO Box 3000, FI-90014 Oulu, Finland
ARJA KAITALA
Affiliation:
Department of Biology, University of Oulu, PO Box 3000, FI-90014 Oulu, Finland
*
*Corresponding author: University of Oulu, Department of Biology, PO Box 3000, FI-90014 Oulu, Finland. Tel: +358 8 553 1221. Fax: +358 8 553 1061. E-mail: laura.harkonen@oulu.fi
Get access Rights & Permissions [Opens in a new window]

Summary

Offspring size and performance in invertebrates often decrease with maternal age or as a response to seasonal environment. In viviparous ectoparasites maternal provision may wholly determine offspring performance outside the host. The viviparous deer ked (Lipoptena cervi), an ectoparasite of cervids, breeds from autumn to spring. We reared deer ked pupae through the reproductive period to investigate whether offspring size and performance vary according to maternal age and offspring environment. We expected that, in autumn, young females would produce the largest offspring to ensure that early-born pupae would survive a long period of winter diapause, and that offspring size would decrease with maternal age and decreasing diapause length. Diapause was associated with a significant weight loss, which reduced survival through post-diapause development. It was thus surprising that the early-born offspring were the smallest, and that size and survival (eventually) increased towards the spring. The variability among offspring in the length of off-host period seems to be an important component of life-history evolution in this ectoparasite, and should be studied further. Unexpected seasonal variation in the offspring size of this blood-feeding ectoparasite may result from changes in female resources due to weakening host condition as the winter progresses.

Keywords

Hippoboscidaehost effectmooseoff-host survivalseasonalityviviparity
Type
Research Article
Information
Parasitology , Volume 140 , Issue 2 , February 2013 , pp. 229 - 236
Copyright
Copyright © Cambridge University Press 2012

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

Bequaert, J. C. (1953). The hippoboscidae or louse–flies (Diptera) of mammals and birds. Part 1. Structure, physiology and natural history. Entomologica Americana 32, 1–209.Google Scholar
Bownds, C., Wilson, R. and Marshall, D. J. (2010). Why do colder mothers produce larger eggs? An optimality approach. The Journal of Experimental Biology 213, 3796–3801.CrossRefGoogle ScholarPubMed
Clutton–Brock, T. H. (1984). Reproductive effort and terminal investment in iteroparous animals. The American Naturalist 123, 212–229.CrossRefGoogle Scholar
Clutton–Brock, T. H. (1991). The Evolution of Parental Care. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Colinet, H., Hance, T. and Vernon, P. (2006). Water relations, fat reserves, survival and longevity of a cold-exposed parasitic wasp Aphidius colemani (Hymenoptera: Aphidiinae). Environmental Entomology 35, 228–236. doi: 10.1603/0046-225X-35.2.228.CrossRefGoogle Scholar
Fischer, K., Brakefield, P. M. and Zwaan, B. J. (2003). Plasticity in butterfly egg size: Why larger offspring at lower temperatures? Ecology 84, 3138–3147.CrossRefGoogle Scholar
Fox, C. W. (1993). The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculates (Coleoptera: Bruchidae). Oecologia 96, 139–146.CrossRefGoogle Scholar
Fox, C. W. (1994). The influence of egg size on offspring performance in the seed beetle, Callosobruchus maculatus. Oikos 71, 321–325.CrossRefGoogle Scholar
Haarløv, N. (1964). Life cycle and distribution pattern of Lipoptena cervi (L.) (Dipt., Hippobosc.) on Danish deer. Oikos 15, 93–129.CrossRefGoogle Scholar
Härkönen, L. (2012). Seasonal variation in the life-histories of a viviparous ectoparasite, the deer ked. Ph.D. thesis, University of Oulu, Finland.Google Scholar
Härkönen, L., Härkönen, S., Kaitala, A., Kaunisto, S., Kortet, R., Laaksonen, S. and Ylönen, H. (2010). Predicting range expansion of an ectoparasite – the effect of spring and summer temperatures on deer ked (Lipoptena cervi) performance along a latitudinal gradient. Ecography 33, 906–912.CrossRefGoogle Scholar
Härkönen, L., Kaitala, A., Kaunisto, S. and Repo, T. (2012). High cold tolerance through four seasons and all free-living stages in an ectoparasite. Parasitology 139, 926–935. doi:10.1017/S0031182012000091CrossRefGoogle Scholar
Ivanov, V. I. (1981). Spread of the deer ked Lipoptena cervi L. (Diptera, Hippoboscidae) in Belarus, its biology and deleterious effects. Ph.D. thesis, Institute of Parasitology and Trophic Medicine, Veterinary Academy of Moscow. (In Russian.)Google Scholar
Kaunisto, S., Kortet, R., Härkönen, L., Härkönen, S., Ylönen, H. and Laaksonen, S. (2009). New bedding site examination-based method to analyse deer ked (Lipoptena cervi) infection in cervids. Parasitology Research 104, 919–925.CrossRefGoogle ScholarPubMed
Kaunisto, S., Välimäki, P., Kortet, R., Koskimäki, J., Härkönen, S., Kaitala, A., Laaksonen, S., Härkonen, L. and Ylönen, H. (2012). Avian predation on a parasitic fly of cervids during winter: can host–related cues increase the predation risk? Biological Journal of the Linnean Society 106, 275–286.CrossRefGoogle Scholar
Kennedy, J. A., Smith, J. R. and Smyth, M. (1975). Diapause in Ornithomya biloba dufour (Diptera: Hippoboscidae) parasitic on fairy martins in South Australia. Journal of Parasitology 61, 369–372.CrossRefGoogle ScholarPubMed
Kindsvater, H. K., Alonzo, S. H., Mangel, M. and Bonsall, M. B. (2010). Effects of age- and state-dependent allocation on offspring size and number. Evolutionary Ecology Research 12, 327–346.Google Scholar
Kortet, R., Härkönen, L., Hokkanen, P., Härkönen, S., Kaitala, A., Kaunisto, S., Laaksonen, S., Kekäläinen, J. and Ylönen, H. (2010). Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bulletin of Entomological Research 100, 279–285.CrossRefGoogle ScholarPubMed
Landa, K. (1992). Adaptive seasonal variation in grasshopper offspring size. Evolution 46, 1553–1558.CrossRefGoogle ScholarPubMed
Langley, P. A. and Clutton-Brock, T. H. (1998). Does reproductive investment change with age in tsetse flies, Glossina morsitans morsitans (Diptera: Glossinidae)? Functional Ecology 12, 866–870.CrossRefGoogle Scholar
Leather, S. R., Walters, K. F. A. and Bale, J. S. (1993). The Ecology of Insect Overwintering. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Marshall, D. J., Heppell, S. S, Munch, S. B. and Warner, R. R. (2010). The relationship between maternal phenotype and offspring quality: Do older mothers really produce the best offspring? Ecology 91, 2862–2873.CrossRefGoogle ScholarPubMed
Marshall, D. J. and Uller, T. (2007). When is a maternal effect adaptive? Oikos 116, 1957–1963.CrossRefGoogle Scholar
Matsuo, Y. (2006). Costs of prolonged diapause and its relationship to body size in a seed predator. Functional Ecology 20, 300–306.CrossRefGoogle Scholar
Mousseau, T. A. and Dingle, H. (1991). Maternal effects in insect life histories. Annual Review of Entomology 36, 511–534. doi: 10.1146/annurev.en.36.010191.002455.CrossRefGoogle Scholar
Paakkonen, T., Mustonen, A.-M., Roininen, H., Niemelä, P., Ruusila, V., and Nieminen, P. (2010). Parasitism of the deer ked, Lipoptena cervi, on the moose, Alces alces, in eastern Finland. Medical and Veterinary Entomology 24, 411–417.CrossRefGoogle ScholarPubMed
Parker, G. A. and Begon, M. (1986). Optimal egg size and clutch size: effects of environment and maternal phenotype. American Naturalist 128, 573–592.CrossRefGoogle Scholar
Peters, R. H. (1983). The Ecological Implications of Body Size. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Plaistow, S., Clair, J. St., Grant, J. and Benton, T. (2007). How to put all your eggs in one basket: empirical patterns of offspring provisioning throughout a mother's lifetime. American Naturalist 170, 520–529.CrossRefGoogle ScholarPubMed
Roff, D. A. (1992). The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York, USA.Google Scholar
Roulin, A., Brinkhof, M. W. G., Bize, P., Richner, H., Jungi, T. W., Bavoux, C., Boileau, N. and Burneleau, G. (2003). Which chick is tasty to parasites? The importance of host immunology vs. parasite life history. Journal of Animal Ecology 72, 75–81.CrossRefGoogle Scholar
Sæther, B.-E. and Gravem, A. J. (1988). Annual variation in winter body condition of Norwegian moose calves. Journal of Wildlife Management 52, 333–336.CrossRefGoogle Scholar
Schrader, M. and Travis, J. (2008). Testing the viviparity–driven–conflict hypothesis: parent–offspring conflict and the evolution of reproductive isolation in a poeciliid fish. American Naturalist 172, 806–817.CrossRefGoogle Scholar
Smith, C. C. and Fretwell, S. D. (1974). The optimal balance between size and number of offspring. American Naturalist 108, 499–506.CrossRefGoogle Scholar
Stearns, S. C. (1992). The Evolution of Life Histories. Oxford University Press, Oxford, UK.Google Scholar
Tauber, M. J., Tauber, C. A. and Masaki, S. (1986). Seasonal Adaptations of Insects. Oxford University Press, New York, USA.Google Scholar
Tinsley, C. R. (1999). Overview: extreme temperatures. Parasitology 119 (Suppl.), S1–S6.CrossRefGoogle Scholar
Tschirren, B., Bischoff, L. L., Saladin, V. and Richner, H. (2007). Host condition and host immunity affect parasite fitness in a bird–ectoparasite system. Functional Ecology 21, 372–378.CrossRefGoogle Scholar
Välimäki, P., Kaitala, A., Madslien, K., Härkönen, L., Várkonyi, G., Heikkilä, J., Jaakola, M., Ylönen, H., Kortet, R. and Ytrehus, B. (2011). Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness. Oecologia 166, 985–995. doi: 10.1007/s00442-011-1951-y.CrossRefGoogle ScholarPubMed