Parasitoidism is one of the main causes of insect egg mortality. Parasitoids are often able to detect eggs using semiochemicals released from eggs and disturbed plants. In response, female insects adopt a wide variety of oviposition strategies to reduce the detectability of eggs and subsequent mortality. We evaluated the proportion of parasitized and undeveloped eggs of three common damselfly species from the family Lestidae, the most diverse group of European damselflies, in terms of oviposition strategies, notably clutch patterning and the ability to utilize oviposition substrates with different mechanical properties. We assumed that higher costs associated with some oviposition strategies will be balanced by lower egg mortality. We found that the ability of Chalcolestes viridis to oviposit into very stiff substrates brings benefit in the form of a significantly lower rate of parasitoidism and lower proportion of undeveloped eggs. The fundamentally different phenology of Sympecma fusca and/or their ability to utilize dead plants as oviposition substrate resulted in eggs that were completely free of parasitoids. Our results indicated that ovipositing into substrates that are unsuitable for most damselfly species significantly reduces egg mortality. Notably, none of these oviposition strategies would work unless combined with other adaptations, such as prolonging the duration of the prolarval life stage or the ability to oviposit into stiff tissue.

Department of Biology and Ecology Faculty of Science University of Ostrava Chittussiho 10 CZ 710 00 Slezská Ostrava Czech Republic

Department of Ecology Faculty of Environmental Sciences Czech University of Life Sciences Prague Kamýcká 129 CZ 165 00 Praha⁻Suchdol Czech Republic

Zobrazit více v PubMed

Siva-Jothy M.T., Gibbons D.W., Pain D.D.J. Female oviposition-site preference and egg hatching success in the damselfly Calopteryx splendens xanthostoma. Behav. Ecol. Sociobiol. 1995;37:39–44. doi: 10.1007/BF00173897. DOI

Rantala M.J., Ilmonen J., Koskimäki J., Suhonen J., Tynkkynen K. The macrophyte, Stratiotes aloides, protects larvae of dragonfly Aeshna viridis against fish predation. Aquat. Ecol. 2004;38:77–82. doi: 10.1023/B:AECO.0000021005.22624.16. DOI

Capinera J.L. Encyclopedia of Entomology. Springer; Berlin, Germany: 2008.

Suhling F., Sahlén G., Kalkman V., Gorb S., Dijkstra K.-D.B., Van Tol J. Odonata. In: Thorp J., Rogers C., Tockner K., editors. Thorp and Covich’s Freshwater Invertebrates. Academic Press; New York, NY, USA: 2015. pp. 893–932.

Corbet P.S. Dragonflies: Behaviour and Ecology of Odonata. Harley Books, Colchester. Harley Books; Colchester, UK: 1999.

Moisan P., Labandeira C.C., Matushkina N.A., Wappler T., Voigt S., Kerp H. Lycopsid-arthropod associations and odonatopteran oviposition on Triassic herbaceous Isoetites. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2012;344–345:6–15. doi: 10.1016/j.palaeo.2012.05.016. DOI

Labandeira C.C. Early History of Arthropod and Vascular Plant Associations. Annu. Rev. Early Planet. Sci. 1998;26:329–377. doi: 10.1146/annurev.earth.26.1.329. DOI

Matushkina N.A., Gorb S. Mechanical properties of the endophytic ovipositor in damselflies (Zygoptera, Odonata) and their oviposition substrates. Zoology. 2007;110:167–175. doi: 10.1016/j.zool.2006.11.003. PubMed DOI

Matushkina N.A., Lambret P., Gorb S. Keeping the golden mean: Plant stiffness and anatomy as proximal factors driving endophytic oviposition site selection in a dragonfly. Zoology. 2016;119:474–480. doi: 10.1016/j.zool.2016.03.003. PubMed DOI

Matushkina N.A., Gorb S.N. Stylus of the odonate endophytic ovipositor: a mechanosensory organ controlling egg positioning. J. Insect Physiol. 2002;48:213–219. doi: 10.1016/S0022-1910(01)00166-4. PubMed DOI

Matushkina N.A., Lambret P.H. Ovipositor morphology and egg laying behaviour in the dragonfly Lestes macrostigma (Zygoptera: Lestidae) Int. J. Odonatol. 2011;14:69–82. doi: 10.1080/13887890.2011.568190. DOI

Martens A. Initial preference of oviposition sites: Discrimination between living and dead plant material in Sympecma fusca and Coenagrion caerulescens (Odonata: Lestidae, Coenagrionidae) Eur. J. Entomol. 2001;98:121–123. doi: 10.14411/eje.2001.021. DOI

Matushkina N.A., Gorb S. Patterns of endophytic egg-sets in damselflies (Odonata, Zygoptera) Vestn. Zool. 2000;14:152–159.

Jödicke R. Die Binsenjungfern und Winterlibellen Europas: Lestidae. Westarp Wissenschaften; Magdeburg, Germany: 1997. Die Neue Brehm-Bücherei; Bd. 631, Die Libellen Europas-Band 3)

Matushkina N.A., Buy D., Lambret P. Egg clutch patterning in Lestes virens (Odonata, Lestidae) with evolutionary emphasis on endophytic oviposition in lestid dragonflies. Insect Sci. 2016;23:893–902. doi: 10.1111/1744-7917.12230. PubMed DOI

Parker G.A., Courtney S.P. Models of clutch size in insect oviposition. Theor. Popul. Biol. 1984;26:27–48. doi: 10.1016/0040-5809(84)90022-4. DOI

Lancaster J., Downes B.J. Aquatic Entomology. Volume 285 Oxford University Press; Oxford, UK: 2013.

Chiappini E., Salerno G., Berzolla A., Iacovone A., Cristina Reguzzi M., Conti E. Role of volatile semiochemicals in host location by the egg parasitoid Anagrus breviphragma. Entomol. Exp. Appl. 2012;144:311–316. doi: 10.1111/j.1570-7458.2012.01290.x. DOI

Manrique V., Jones W.A., Williams L.H., Bernal J.S. Olfactory responses of Anaphes iole (Hymenoptera: Mymaridae) to volatile signals derived from host habitats. J. Insect Behav. 2005;18:89–104. doi: 10.1007/s10905-005-9349-5. DOI

Cronin J.T., Strong D.R. Dispersal-Dependent Oviposition and the Aggregation of Parasitism. Am. Nat. 1999;154:23–36. doi: 10.1086/303221. PubMed DOI

Cronin J.T. Habitat edges, within-patch dispersion of hosts, and parasitoid oviposition behavior. Ecology. 2009;90:196–207. doi: 10.1890/08-0208.1. PubMed DOI

Hirayama H., Kasuya E. Oviposition depth in response to egg parasitism in the water strider: High-risk experience promotes deeper oviposition. Anim. Behav. 2009;78:935–941. doi: 10.1016/j.anbehav.2009.07.019. DOI

Amano H., Hayashi K., Kasuya E. Avoidance of egg parasitism through submerged oviposition by tandem pairs in the water strider, Aquarius paludum insularis (Heteroptera: Gerridae) Ecol. Entomol. 2008;33:560–563. doi: 10.1111/j.1365-2311.2008.00988.x. DOI

Harabis F., Dolny A., Helebrandova J., Ruskova T. Do egg parasitoids increase the tendency of Lestes sponsa (Odonata: Lestidae) to oviposit underwater? Eur. J. Entomol. 2015;112:63–68. doi: 10.14411/eje.2015.017. DOI

Lambret P., Besnard A., Matushkina N.A. Plant preference during oviposition in the endangered dragonfly Lestes macrostigma (Odonata: Zygoptera) and consequences for its conservation. J. Insect Conserv. 2015;19:741–752. doi: 10.1007/s10841-015-9796-z. DOI

Dolný A., Harabiš F., Bárta D. Vážky (Insecta: Odonata) České Republiky. Atlasy; Praha, Czech Republic: 2016.

Matushkina N., Gorb S. A Check-list of Substrates for Endophytic Oviposition of Some European Dragonflies (Insecta: Odonata) Kharkov Entomol. Soc. Gaz. 2003;10:108–118.

Dijkstra K.-D.B., Lewington R. Field Guide to the Dragonflies of Britain and Europe including Western Turkey and North-Western Africa. British Wildlife Publishing; Milton on Stour, UK: 2006.

Harabiš F. The value of terrestrial ecotones as refuges for winter damselflies (Odonata: Lestidae) J. Insect Conserv. 2016;20:971–977. doi: 10.1007/s10841-016-9929-z. DOI

Paulson D. World Odonata List. University of Puget Sound; Washington, DC, USA: 2018. [(accessed on 10 December 2018)]. Available online: https://www.pugetsound.edu/academics/academic-resources/slater-museum/biodiversity-resources/dragonflies/world-odonata-list2/

Bates D., Maechler M., Bolker B., Walker S., Christensen R.H.B., Singmann H., Dai B., Grothendieck G. Package ‘lme4’. [(accessed on 10 October 2018)]; Available online: https://cran.r-project.org/web/packages/lme4/index.html.

Hothorn T., Bretz F., Westfall P., Heiberger R.M., Schuetzenmeister A., Scheibe S. Multcomp: Simultaneous Inference in General Parametric Models. Biom. J. 2008;50:346–363. doi: 10.1002/bimj.200810425. PubMed DOI

R Development Core Team . R: A Language and Environment for Statistical Computing. The R Foundation for Statistical Computing; Vienna, Austria: 2015. [(accessed on 10 October 2018)]. Available online: http://www.R-project.org/

Janz N. Evolutionary ecology of oviposition strategies. Evol. Ecol. 2002:349–376. doi: 10.1002/9780470760253. DOI

Harabiš F., Dolný A., Šipoš J. Enigmatic adult overwintering in damselflies: Coexistence as weaker intraguild competitors due to niche separation in time. Popul. Ecol. 2012;54:549–556. doi: 10.1007/s10144-012-0331-8. DOI

Umbanhowar J., Hastings A. The Impact of Resource Limitation and the Phenology of Parasitoid Attack on the Duration of Insect Herbivore Outbreaks. Theor. Popul. Biol. 2002;62:259–269. doi: 10.1006/tpbi.2002.1617. PubMed DOI

Borisov S.N. Adaptations of dragonflies (Odonata) under desert conditions. Entomol. Rev. 2006;86:534–543. doi: 10.1134/S0013873806050058. DOI

Schiel F.J., Buchwald R. Contrasting life-history patterns between vernal pond specialists and hydroperiod generalists in Lestes damselflies (Odonata: Lestidae) Odonatologica. 2015;44:349–374.

Behavioural Phenotypic Plasticity of Submerged Oviposition in Damselflies (Insecta: Odonata)