Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-18T18:09:39.377Z Has data issue: false hasContentIssue false
  • English
  • Français

Early-life temperature modifies adult encapsulation response in an invasive ectoparasite

Published online by Cambridge University Press:  04 June 2015

SIRPA KAUNISTO ,
LAURA HÄRKÖNEN ,
MARKUS J. RANTALA  and
RAINE KORTET
SIRPA KAUNISTO*
Affiliation:
Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu, Finland
LAURA HÄRKÖNEN
Affiliation:
Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu, Finland Department of Biology, University of Oulu, P.O. Box 3000, FI-90014 Oulu, Finland
MARKUS J. RANTALA
Affiliation:
Department of Biology, University of Turku, Turku Brain and Mind Center, FI-20014 Turku, Finland
RAINE KORTET
Affiliation:
Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu, Finland
*
*Corresponding author. Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu, Finland. E-mail: sirpa.kaunisto@uef.fi
Get access Rights & Permissions [Opens in a new window]

Summary

Immunity of parasites has been studied amazingly little, in spite of the fact that parasitic organisms, especially the arthropod parasites, need immunity to survive their own infections to successfully complete life cycles. Long-term effects of challenging environmental temperatures on immunity have remained unstudied in insects and parasites. Our study species, the deer ked (Lipoptena cervi; Linnaeus 1758), is an invasive, blood-feeding parasitic fly of cervids. Here, it was studied whether thermal stress during the pupal diapause stage could modify adult immunity (encapsulation capacity) in L. cervi. The effect of either a low temperature or high temperature peak, experienced during winter dormancy, on encapsulation response of active adult was tested. It was found that low temperature exposure during diapause, as long as the temperature is not too harsh, had a favourable effect on adult immunity. An abnormal, high temperature peak during pupal winter diapause significantly deteriorated the encapsulation capacity of emerged adults. The frequency and intensity of extreme weather events such as high temperature fluctuations are likely to increase with climate change. Thus, the climate change might have previously unknown influence on host-ectoparasite interactions, by affecting ectoparasite's immune defence and survival.

Keywords

CervidaediapauseectoparasiteencapsulationHippoboscidaeimmunityinvasive speciesthermal stress
Type
Research Article
Information
Parasitology , Volume 142 , Issue 10 , September 2015 , pp. 1290 - 1296
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

Abramoff, M. D., Magalhaes, P. J. and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International 11, 36–42.Google Scholar
Benelli, E. F. (1998). Ecological and adaptive aspects of immunocompetence in a social insect . Ph.D. thesis. Dep. Environ. Sci., ETH, Zürich, Switzerland.Google Scholar
Boehm, T. (2012). Evolution of vertebrate immunity. Current Biology 22, R722–R732.CrossRefGoogle ScholarPubMed
Catalán, T. P., Wozniak, A., Niemeyer, H. M., Kalergis, A. M. and Bozinovic, F. (2012). Interplay between thermal and immune ecology: effect of environmental temperature on insect immune response and energetic costs after an immune challenge. Journal of Insect Physiology 58, 310–317.CrossRefGoogle ScholarPubMed
Denlinger, D. L. and Lee, R. E. (2010). Low Temperature Biology of Insects. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Franke, K. and Fischer, K. (2013). Effects of inbreeding and temperature stress on life history and immune function in a butterfly. Journal of Evolutionary Biology 26, 517–528.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. and Kaitala, A. (2013). Months of asynchrony in offspring production but synchronous adult emergence: the role of diapause in an ectoparasite's life cycle. Environmental Entomology 42, 1408–1414.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, 926–933.CrossRefGoogle Scholar
Härkönen, L., Hurme, E. and Kaitala, A. (2013). Unexpected seasonal variation in offspring size and performance in a viviparous ectoparasite. Parasitology 140, 229–236.CrossRefGoogle Scholar
Haynie, D. T. (2008). Biological Thermodynamics. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Hillyer, J. F. (2010). Mosquito immunity. In Invertebrate Immunity (ed. Söderhäll, K.), pp. 218–238. Springer Science & Business Media, New York, USA.CrossRefGoogle Scholar
Hoffmann, J. A. (1995). Innate immunity of insects. Current Opinion in Immunology 7, 4–10.CrossRefGoogle ScholarPubMed
Karl, I., Stoks, R., De Block, M., Janowitz, S. A. and Fischer, K. (2011). Temperature extremes and butterfly fitness: conflicting evidence from life history and immune function. Global Change Biology 17, 676–687.CrossRefGoogle 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
Korhonen, E. M., Pérez-Vera, C., Pulliainen, A. T., Sironen, T., Aaltonen, K., Kortet, R., Härkönen, L., Härkönen, S., Paakkonen, T., Nieminen, P., Mustonen, A. M., Ylönen, H. and Vapalahti, O. (2014). Molecular detection of Bartonella spp. in deer ked pupae, adult keds and moose blood in Finland. Epidemiology and Infection 5, 1–8.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
Krams, I., Daukšte, J., Kivleniece, I., Krama, T. and Rantala, M. J. (2013). Previous encapsulation response enhances within individual protection against fungal parasite in the mealworm beetle Tenebrio molitor . Insect Science 20, 771–777.CrossRefGoogle ScholarPubMed
Kynkäänniemi, S. M., Kettu, M., Kortet, R., Härkönen, L., Kaitala, A., Paakkonen, T., Mustonen, A. M., Nieminen, P., Härkönen, S., Ylönen, H. and Laaksonen, S. (2014). Acute impacts of the deer ked (Lipoptena cervi) infestation on reindeer (Rangifer tarandus tarandus) behaviour. Parasitology Research 113, 1489–1497.CrossRefGoogle ScholarPubMed
Lehane, M. J., Aksoy, S. and Levashina, E. (2004). Immune responses and parasite transmission in blood-feeding insects. Trends in Parasitology 20, 433–439.CrossRefGoogle ScholarPubMed
Lemaitre, B. and Hoffmann, J. (2007). The host defense of Drosophila melanogaster . Annual Review of Immunology 25, 697–743.CrossRefGoogle ScholarPubMed
Mandrioli, M. (2012). Someone like it hot? Effects of global warming on insect immunity and microbiota. Invertebrate Survival Journal 9, 58–63.Google Scholar
Marmaras, V. J. and Lampropoulou, M. (2009). Regulators and signalling in insect haemocyte immunity. Cellular Signalling 21, 186–195.CrossRefGoogle ScholarPubMed
Mourya, D. T., Yadav, P. and Mishra, A. C. (2004). Effect of temperature stress on immature stages and susceptibility of Aedes Aegypti mosquitoes to Chikungunya virus. American Journal of Tropical Medicine and Hygiene 70, 346–350.CrossRefGoogle ScholarPubMed
Murdock, C. C., Paaijmans, K. P., Bell, A. S., King, J. G., Hillyer, J. F., Read, A. F. and Thomas, M. B. (2012). Complex effects of temperature on mosquito immune function. Proceedings of the Royal Society B. 279, 3357–3366.CrossRefGoogle ScholarPubMed
Rantala, M. J. and Roff, D. A. (2007). Inbreeding and extreme outbreeding causes sex differences in immune defence and life history traits in Epirrita autumnata . Heredity 98, 329–336.CrossRefGoogle ScholarPubMed
Rantala, M. J., Jokinen, I., Kortet, R., Vainikka, A. and Suhonen, J. (2002). Do pheromones reveal male immunocompetence? Proceedings of the Royal Society B 269, 1681–1685.CrossRefGoogle ScholarPubMed
Samuel, W. M., Madslien, K. and Gonynor-McGuire, J. (2012). Review of deer ked (Lipoptena cervi) on moose in Scandinavia with implications for North America. Alces 48, 27–33.Google Scholar
Schmid-Hempel, P. (2005). Evolutionary ecology of insect immune defences. Annual Review of Entomology 50, 529–551.CrossRefGoogle Scholar
Sinclair, B. J., Ferguson, L. V., Salehipour-shirazi, G. and MacMillan, H. A. (2013). Cross-tolerance and cross-talk in the cold: relating low temperatures to desiccation and immune stress in insects. Integrative and Comparative Biology 53, 545–556.CrossRefGoogle ScholarPubMed
Sonenshine, D. E. (1993). Biology of Ticks. Oxford University Press, New York, pp. 447.Google Scholar
Taylor, D. (2006). Innate immunity in ticks: a review. Journal of the Acarological Society of Japan 15, 109–127.CrossRefGoogle Scholar
Tian, C., Gao, B., Fang, Q., Ye, G. and Zhu, S. (2010). Antimicrobial peptide-like genes in Nasonia vitripennis: a genomic perspective. BMC Genomics 11, 187.CrossRefGoogle ScholarPubMed
Vogelweith, F., Dourneau, M., Thiéry, D., Moret, Y. and Moreau, J. (2013). Geographical variation in parasitism shapes larval immune function in a phytophagous insect. Naturwissenschaften 100, 1149–1161.CrossRefGoogle Scholar
Välimäki, P., Madslien, K., Malmsten, J., Härkönen, L., Härkönen, S., Kaitala, A., Kortet, R., Laaksonen, S., Mehl, R., Redford, L., Ylönen, H. and Ytrehus, B. (2010). Fennoscandian distribution of an important parasite of cervids, the deer ked (Lipoptena cervi), revisited. Parasitology Research 107, 117–125.CrossRefGoogle ScholarPubMed
Zhao, L. and Jones, W. A. (2012). Expression of heat shock protein genes in insect stress responses. Invertebrate Survival Journal 9, 93–101.Google Scholar
Yourth, C. P., Forbes, M. R. and Smith, B. P. (2002). Immune expression in a damselfly is related to time of season, not to fluctuating asymmetry or host size. Ecological Entomology 27, 123–128.CrossRefGoogle Scholar