Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-24T09:02:24.842Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite burden and the insect immune response: interpopulation comparison

Published online by Cambridge University Press:  29 August 2012

KARI M. KAUNISTO  and
JUKKA SUHONEN
KARI M. KAUNISTO*
Affiliation:
Section of Ecology, Department of Biology, FI-20014University of Turku, Finland
JUKKA SUHONEN
Affiliation:
Section of Ecology, Department of Biology, FI-20014University of Turku, Finland
*
*Corresponding author: Tel: +358 40 7401653. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The immune response affects host's survival and reproductive success. Insurmountable immune function has not evolved because it is costly and there is a trade-off between other life-history traits. In previous studies several factors such as diet and temperature have been proposed to cause interpopulation differences in immune response. Moreover, the insect immune system may be functionally more protective upon secondary exposure, thus infection history may associate with the immune response. Here we measured how geographical location and parasite burden is related to variation in immune response between populations. We included 13 populations of the Northern Damselfly Coenagrion hastulatum (Odonata: Coenagrionidae) in Finland over a latitudinal range of 880 km to this study. We found that water mites associated strongly with the immune response at interpopulation level: the more the mites, the higher the immune response. Also, in an alternative model based on AIC, latitude and individual size associated with the immune response. In turn, endoparasitic gregarines did not affect the immune response. To conclude, a positive interpopulation association between the immune response and the rate of water mite infection may indicate (i) local adaptation to chronic parasite stress, (ii) effective ‘induced’ immune response against parasites, or (iii) a combined effect of both of these.

Keywords

Odonataencapsulationgregarinewater miteCoenagrion
Type
Research Article
Information
Parasitology , Volume 140 , Issue 1 , January 2013 , pp. 87 - 94
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

Åbro, A. (1974). The gregarine infection in different species of Odonata from the same habitat. Zoologica Scripta. 3, 111–120. (DOI:10.1111/j.1463-6409.1974.tb00809.x)CrossRefGoogle Scholar
Åbro, A. (1976). The mode of gregarine infection in Zygoprera (Odonata). Zoologica Scripta 5, 265–275. (DOI:10.1111/j.1463-6409.1976.tb00708.x)CrossRefGoogle Scholar
Åbro, A. (1986). Gregarine infection of Zygoptera in diverse habitats. Odonatologica 16, 119–128.Google Scholar
Åbro, A. (1990). The impact of parasites in adult populations of Zygoptera. Odonatologica 19, 223–233.Google Scholar
Åbro, A. (1996). Gregarine infection of adult Calopteryx virgo L. (Odonata: Zygoptera). Journal of Natural History 30, 855–859. (DOI:10.1080/00222939600770481)CrossRefGoogle Scholar
Andres, J. A. and Cordero, A. (1998). Effects of water mites on the damselfly Ceriagrion tenellum. Ecological Entomology 23, 103–109. (DOI:10.1046/j.1365-2311.1998.00125.x)CrossRefGoogle Scholar
Anderson, D. R., Burnham, K. P. and Thompson, W. L. (2000). Null hypothesis testing: Problems, prevalence, and an alternative. Journal of Wildlife Management 64, 912–923. (DOI: 10.2307/3803199)CrossRefGoogle Scholar
Angelibert, S. and Giani, N. (2003). Dispersal characteristics of three odonate species in a patchy habitat. Ecography 26, 13–20. (DOI: 10.1034/j.1600-0587.2003.03372.x)CrossRefGoogle Scholar
Arala-Chaves, M. and Sequeira, T. (2000). Is there any kind of adaptive immunity in invertebrates? Aquaculture 191, 247–258. (DOI:10.1016/S0044-8486(00)00430-0)CrossRefGoogle Scholar
Boggs, C. L. and Freeman, K. D. (2005). Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144, 353–361. (DOI: 10.1007/s00442-005-0076-6)CrossRefGoogle ScholarPubMed
Braune, P. and Rolff, J. (2001). Parasitism and survival in a damselfly: does host sex matter? Proceedings of the Royal Society of London, B 268, 1133–1137. (DOI: 10.1098/rspb.2001.1641)CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583. (DOI: 10.2307/3284227)CrossRefGoogle Scholar
Bush, A. O.Fernández, J. C., Esch, G. W. and Seed, J. R. (2001). Parasitism: the diversity and ecology of animal parasites. Cambridge University Press.Google Scholar
Contreras-Garduno, J., Cordoba-Aguilar, A. and Peralta-Vazquez, H. (2008). Differences in immune ability do not correlate with parasitic burden in two Zygoptera species (Calopterygidae, Coenagrionidae). Odonatologica 37, 111–118.Google Scholar
Corbet, P. S. (1999). Dragonflies: Behaviour and Ecology of Odonata. Harley Books, Colchester, UK.Google Scholar
Corbet, P. S. , Suhling, F. and Soendgerath, D. (2005). Voltinism of Odonata: a review. International Journal of Odonatologica 9, 1–44.Google Scholar
Corby-Harris, V. and Promislow, D. E. L. (2008). Host ecology shapes geographical variation for resistance to bacterial infection in Drosophila melanogaster. Journal of Animal Ecology 77, 768–776. (DOI: 10.1111/j.1365-2656.2008.01399.x)CrossRefGoogle ScholarPubMed
Cordoba-Aguilar, A., Conteras-Garduno, J., Peralta-Vazquez, H., Luna-Gonzalez, A., Campa-Cordova, A. I. and Ascencio, F. (2006). Sexual comparisons in immune ability, survival and parasite intensity in two damselfly species. Journal of Insect Physiology 52, 861–869. (DOI: 10.1016/j.jinsphys.2006.05.008)CrossRefGoogle ScholarPubMed
Cordoba-Aguilar, A., Jimenez-Cortes, J. G. and Lanz-Mendoza, H. (2009). Seasonal variation in ornament expression, body size, energetic reserves, immune response, and survival in males of a territorial insect. Ecological Entomology 34, 228–239. (DOI: 10.1111/j.1365-2311.2008.01061.x)CrossRefGoogle Scholar
De Block, M., Mc Peek, M. A. and Stoks, R. (2008 a). Stronger compensatory growth in a permanent-pond Lestes damselfly relative to temporary-pond. Oikos 117, 245–254. (DOI: 10.1111/j.2007.0030-1299.16376.x)CrossRefGoogle Scholar
De Block, M., Slos, S., Johansson, F. and Stoks, R. (2008 b). Integrating life history and physiology to understand latitudinal size variation in a damselfly. Ecography 31, 115–123. (DOI:10.1111/j.2007.0906-7590.05313.x)CrossRefGoogle Scholar
Dijkstra, K. (2006). Field Guide to the Dragonflies of Britain and Europe. British Wildlife Publishing, Dorset, UK.Google Scholar
Forbes, M. R. and Baker, R. L. (1991). Condition and fecundity of the damselfly, Enallagma ebrium (Hagen) – the importance of ectoparasites. Oecologia 86, 335–341. (DOI:10.1007/BF00317598)CrossRefGoogle ScholarPubMed
Forbes, M. R., Muma, K. E. and Smith, B. P. (1999). Parasitism of Sympetrum dragonflies by Arrenurus planus mites: maintenance of resistance particular to one species. International Journal for Parasitology 29, 991–999. (DOI: 10.1016/S0020-7519(99)00061-2)CrossRefGoogle ScholarPubMed
Forbes, M. R., Muma, K. E. and Smith, B. P. (2002). Diffuse coevolution: constraints on a generalist parasite favour of a dead-end host. Ecography 25, 345–351. (DOI: 10.1034/j.1600-0587.2002.250311.x)CrossRefGoogle Scholar
Forbes, M. R., and Robb, T. (2008). Testing hypotheses about parasite-mediated selection using odonate hosts. In Dragonflies and Damselflies. Model Organisms for Ecological and Entomological Research (ed. Córdoba-Aguilar, A.), pp. 175–188. Oxford University Press, Chippenham, UK.CrossRefGoogle Scholar
Frank, S. A. (2000). Specific and non-specific defense against parasitic attack. Journal of Theoretical Biology 202, 283–304. (DOI: 10.1006/jtbi.1999.1054)CrossRefGoogle ScholarPubMed
González-Santoyo, I., Córdoba-Aguilar, A., González- Tokmanand, D. M. and Lanz-Mendoza, H. (2010). Phenoloxidase activity and melanization do not always covary with sexual trait expression in Hetaerina damselflies (Insecta: Calopterygidae). Behaviour 147, 1285–1307. (DOI: 10.1163/000579510X516777)CrossRefGoogle Scholar
Hassall, C., Lowe, C. D., Harvey, J. F., Watts, P. C. and Thompson, D. J. (2010). Phenology determines seasonal variation in ectoparasite loads in a natural insect population. Ecological Entomology 35, 514–522. (DOI:10.1111/j.1365-2311.2010.01210.x)CrossRefGoogle Scholar
Honkavaara, J., Rantala, M. J. and Suhonen, J. (2009). Mating status, immune defence, and multi-parasite burden in the damselfly Coenagrion armatum. Entomologia Experimentalis et Applicata 132, 165–171. (DOI: 10.1111/j.1570-7458.2009.00877.x)CrossRefGoogle Scholar
Ilvonen, S.Ilvonen, J. J., Kaunisto, K. M., Krams, I. and Suhonen, J. (2011). Can infection by eugregarine parasites mediate species coexistence in Calopteryx damselflies? Ecological Entomology 36, 582–587. (DOI: 10.1111/j.1365-2311.2011.01307.x)CrossRefGoogle Scholar
Johansson, F., Sniegula, S. and Brodin, T. (2010). Emergence patterns and latitudinal adaptations in development time of Odonata in north Sweden and Poland. Odonatologica 39, 97–106.Google Scholar
Karjalainen, S. (2010). Suomen sudenkorennot. Tammi, Helsinki, Finland.Google Scholar
Koskimäki, J., Rantala, M. J. and Suhonen, J. (2009). Wandering males are smaller than territorial males in the damselfly Calopteryx virgo L. (Zygoptera:Calopterygidae). Odonatologica 38, 159–165.Google Scholar
Köning, C. and Schmid-Hempel, P. (1995). Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris (L.). Proceedings of the Royal Society of London. B 260, 225–227. (DOI: 10.1098/rspb.1995.0084)Google Scholar
Lawniczak, M. K. and Barnes, A. (2007). Mating and immunity in invertebrates. Trends in Ecology and Evolution 22, 48–55. (DOI:10.1016/j.tree.2006.09.012)CrossRefGoogle ScholarPubMed
Leung, B. and Forbes, M. R. (1997). Modelling fluctuating asymmetry in relation to stress and fitness. Oikos 78, 397–405. (DOI: 10.2307/3546309)CrossRefGoogle Scholar
Marden, J. H. and Cobb, J. R. (2004). Territorial and mating success of dragonflies that vary in muscle power output and presence of gregarine gut parasites. Animal Behaviour 68, 857–865. (DOI:10.1016/j.anbehav.2003.09.019)CrossRefGoogle Scholar
Mesterton-Gibbons, M., Marden, J. H. and Dugatkin, L. A. (1996). On wars of attrition without assessment. Journal of Theoretical Biology 181, 65–83. (DOI: 10.1006/jtbi.1996.0115)CrossRefGoogle Scholar
Nagel, L., Robb, T. and Forbes, M. R. (2010). Inter-annual variation in prevalence and intensity of mite parasitism relates to appearance and expression of damselfly resistance. BMC Ecology 10, 5.CrossRefGoogle ScholarPubMed
Nagel, L., Mlynarek, J. J. and Forbes, M. R. (2011). Immune response to nylon inserts in two damselfly species that differ in their resistance to ectoparasitic mites. Ecological Entomology 36, 736–743.CrossRefGoogle Scholar
Neubauer, K. and Rehfeldt, G. (1995). Roosting site selection in the damselfly species Calopteryx haemorrhoidalis (Odonata, Calopterygidae). Entomologia Generalis 19, 291–302.CrossRefGoogle Scholar
Plaistow, S. and Siva-Jothy, M. T. (1996). Energetic constraints and male mate-securing tactics in the damselfly Calopteryx splendens xanthostoma (Charpentier). Proceedings of the Royal Society of London. B 263, 1233–1239. (DOI:10.1098/rspb.1996.0181)Google Scholar
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. (DOI:10.1038/sj.hdy.6800945)CrossRefGoogle ScholarPubMed
Rantala, M. J., Honkavaara, J. and Suhonen, J. (2010). Immune system activation interacts with territory-holding potential and increases predation of the damselfly Calopteryx splendens by birds. Oecologia 163, 825–832. (DOI: 10.1007/s00442-010-1582-8)CrossRefGoogle ScholarPubMed
Reinhardt, K. (1996). Negative effects of Arrenurus water mites on the flight distances of the damselfly Nehalennia speciosa (Odonata: Coenagrionidae). Aquatic Insects 18, 233–240. (DOI:10.1080/01650429609361626)CrossRefGoogle Scholar
Robinson, J. V. (1983). Effects of water mite parasitism on the demographics of an adult populations of Ischnura posita (Hagen) (Odonata: Coenagrionidae). American Midland Naturalist 109, 169–174. (DOI: 10.2307/2425527)CrossRefGoogle Scholar
Rolff, J. and Siva-Jothy, M. T. (2004). Selection on insect immunity in the wild. Proceedings of the Royal Society of London, B 271, 2157–2160. (DOI:10.1098/rspb.2004.2859)CrossRefGoogle ScholarPubMed
Rouquette, J. R. and Thompson, D. J. (2007). Patterns of movement and dispersal in an endangered damselfly and the consequences for its management. Journal of Applied Ecology 44, 692–701. (DOI:10.1111/j.1365-2664.2007.01284.x)CrossRefGoogle Scholar
Sadd, B. and Schmid-Hempel, P. (2006). Insect immunity shows specificity in protection upon secondary pathogen exposure. Current Biology 16, 1206–1210. (DOI:10.1016/j.cub.2006.04.047)CrossRefGoogle ScholarPubMed
Schilder, R. J. and Marden, J. H. (2006). Metabolic syndrome and obesity in an insect. Proceedings of the National Academy of Sciences, USA 103, 18805–18809. (DOI:10.1073/pnas.0603156103)CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. (2004). Evolutionary ecology of insect immune defenses. Annual Review of Entomology 50, 529–551. (DOI: 10.1146/annurev.ento.50.071803.130420)CrossRefGoogle Scholar
Schmid-Hempel, P. (2005). Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved. Bioessays 27, 1026–1034. (DOI:10.1002/bies.20282)CrossRefGoogle ScholarPubMed
Sheldon, B. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321. (DOI: 10.1016/0169-5347(96)10039-2)CrossRefGoogle ScholarPubMed
Siva-Jothy, M. T. (2000). A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proceedings of the Royal Society of London, B 267, 2523–2527. (DOI:10.1098/rspb.2000.1315)CrossRefGoogle Scholar
Siva-Jothy, M. T. and Plaistow, S. J. (1999). A fitness cost of eugregarine parasitism in a damselfly. Ecological Entomology 24, 465–470. (DOI:10.1046/j.1365-2311.1999.00222.x)CrossRefGoogle Scholar
Söderhäll, K. and Cerenius, L. (1998). Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 23–28. (DOI:10.1016/S0952-7915(98)80026-5)CrossRefGoogle ScholarPubMed
Sokolovska, N., Rowe, L. and Johansson, F. (2000). Fitness and body size in mature odonates. Ecological Entomology 25, 239–248. (DOI:10.1046/j.1365-2311.2000.00251.x)CrossRefGoogle Scholar
Suhonen, J., Honkavaara, J. and Rantala, M. (2010). Activation of the immune system promotes insect dispersal in the wild. Oecologia 162, 541–547. (DOI: 10.1007/s00442-009-1470-2)CrossRefGoogle ScholarPubMed
Thompson, J. N. (1994). The Evolutionary Process. University of Chicago Press, Chicago, IL, USA.Google Scholar
Tynkkynen, K., Rantala, M. J. and Suhonen, J. (2004). Interspecific aggression and character displacement in the damselfly Calopteryx splendens. Journal of Evolutionary Biology 17, 759–767. (DOI: 10.1111/j.1420-9101.2004.00733.x)CrossRefGoogle ScholarPubMed
Zar, J. H. (1999). Biostatistical Analysis. 4th Edn. Prentice Hall, Upper Saddle River, NJ, USA.Google Scholar
Zuk, M. and Stoehr, A. M. (2002). Immune defence and host life history. American Naturalist 160, 9–22. (DOI: 10.1086/342131)CrossRefGoogle ScholarPubMed