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Do Egg Parasitoids Increase the Tendency of Lestes Sponsa (Odonata: Lestidae) to Oviposit Underwater?

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Do Egg Parasitoids Increase the Tendency of Lestes Sponsa (Odonata: Lestidae) to Oviposit Underwater? Eur. J. Entomol. 112(1): 63–68, 2015 doi: 10.14411/eje.2015.017 ISSN 1210-5759 (print), 1802-8829 (online) Do egg parasitoids increase the tendency of Lestes sponsa (Odonata: Lestidae) to oviposit underwater? FILIP HARABIŠ 1, *, Aleš DOLNÝ 2, *, **, JANA HELEBRANDOVÁ2 and TEREZA RUSKOVÁ2 1 Department of Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129, CZ-165 21 Prague 6, Czech Republic; e-mail: [email protected] 2 Department of Biology and Ecology / Institute of Environmental Technologies, Faculty of Sciences, University of Ostrava, Chittussiho 10, CZ-710 00 Slezská Ostrava, Czech Republic; e-mails: [email protected]; [email protected]; [email protected] Key words. Odonata, Lestidae, Lestes sponsa, submerged oviposition, egg parasitism, parasitoids, selection of oviposition site, dragonflies Abstract. The selection of oviposition sites by insects can significantly affect egg mortality. Spreadwing damselflies (Odonata: Lesti- dae) predominantly lay their eggs in parts of plants growing above the surface of water and only occasionally also those parts growing underwater. Factors affecting the choice of oviposition site and decision to lay underwater are still poorly understood. We examined whether localities with different risk of egg parasitism, different oviposition strategies (above or below the water surface) and the depth at which the eggs were laid, affected the total number of eggs laid, the proportion parasitized and egg mortality. In general, a signifi- cantly higher proportion of the eggs laid above the surface of water were parasitized but spreadwing damselflies showed significant preference for laying eggs underwater at both of the sites studied. This preference, however, had a different effect on the overall mortal- ity of eggs at the two sites studied. Hence underwater oviposition by damselflies may be seen as a conditional anti-predator strategy, occurring only if the benefits exceed potential risks. Underwater oviposition may provide additional benefits other than protection against egg parasitism. INTRODUCTION several dozen minutes (Waage, 1984; Fincke, 1986; Tsub- As eggs are an immobile stage in the life cycle of insects, aki et al., 2006; Santolamazza et al., 2011). This leaves the they are very vulnerable to predation and parasitism. Dam- main question unanswered: Why do some species of dam- selflies lay eggs in several different ways, which may pro- selflies prefer this high-cost oviposition strategy, especially tect the eggs and significantly reduce egg mortality. Each when eggs laid in plant tissues are well protected (Corbet, strategy, however, incurs certain risks and energy costs 1999; Martens, 2001). Several hypotheses have been pro- (summarized by Corbet, 1999). The most general classi- posed to account for submerged oviposition in damselflies. fication of the modes of oviposition distinguishes between Fincke (1986) describes the evolution of underwater ovi- endophytic and exophytic oviposition, but there is sig- position as a consequence of sexual harassment and male nificant variation within these two groups (Corbet, 1999). guarding behaviour. Another hypothesis (Fincke, 1986; Several species of dragonflies, of the family Aeshnidae and Miller, 1994) stresses the importance of interspecific in- nearly all damselflies oviposit endophytically, which sig- teractions, with endophytic oviposition a means of protect- nificantly mitigate the likelihood of their eggs desiccating ing eggs from abiotic stresses such as drying out and high or freezing and reduces risk of their being eaten by preda- temperatures and incidental predators but not attack by egg tors (Corbet, 1999). Endophytic oviposition, however, is parasitoids (Spence, 1986; Corbet, 1999). time-consuming, involves additional energy costs and The majority of aquatic parasitoids (about 150 species investment in specific morphological structures, because of Hymenoptera) are generalists, utilizing a wide range egg-laying females must insert their eggs into plant tissues of eggs of different host taxa (Fursov, 1995; Bennett, (Matushkina & Gorb, 2007). 2008) and idiobionts, parasitoids that prevent further de- Even more time consuming and risky is the strategy of velopment of their hosts after initially immobilizing them endophytic oviposition in which the adult damselflies lay (Askew & Shaw, 1986; Strand, 1986). Parasitoids may kill eggs underwater (Corbet, 1999). Underwater (submerged) a significant percentage of their hosts and so induce many oviposition by damselflies is often considered to be an inci- behavioural adaptations in aquatic insects (Spence, 1986; dental phenomenon as adult damselflies are not adapted to Gibbons & Pain, 1992; Henriquez & Spence, 1993; Amano stay submerged in water. However, several studies indicate et al., 2008). Several studies on the interactions between that some damselflies (the families Calopterygidae and the egg parasitoid Tiphodytes gerriphagus (Hymenoptera: Coenagrionidae) are able to lay eggs after submergence for Scelionidae) and several species of water striders indicate * The first two authors contributed equally to this work. ** Corresponding author. 63 that these Hemiptera are able to detect parasitoids (Hen- Species studied riquez & Spence, 1993; Hirayama & Kasuya, 2009). In Lestes sponsa is a common species in almost all parts of Eu- addition, there is evidence that submerged oviposition by rope and Asia (Dijkstra & Lewington, 2006). Oviposition is water striders could be a behavioural response to a high predominantly by tandem pairs. The female damselfly lays eggs density of egg parasitoids (Hirayama & Kasuya, 2009). Al- endophytically. Eggs can complete their development in about 8 though these parasitoids can attack eggs underwater, such weeks (Jödicke, 1997), but those laid in August, undergo winter diapause. Larvae begin to hatch only when the water temperature attacks are significantly less frequent than of eggs laid rises above 13°C (Jödicke, 1997). The rate of development inside above the surface of water (Amano et al., 2008; Hirayama the egg and survival greatly depend upon ambient temperature & Kasuya, 2009). The tendency to lay eggs as deeply as (Jödicke, 1997; Corbet, 1999). possible is however limited by increasing mortality of eggs Prior to this study, more than 250 submerged ovipositions by at greater depths, their inability to move underwater and tandem pairs were observed. We only scored instances of sub- so avoid predation and their risk of drowning while lay- merged oviposition when the female was completely submerged ing eggs (Amano et al., 2008; Hirayama & Kasuya, 2008, (including wings). The majority of L. sponsa oviposited underwa- 2009). ter. The situation when a female oviposited partially submerged As noted above, all previous laboratory studies on the was very rare. This occurred only in situations when the pair was distracted, such as by other males (Dolný et al., 2014). effect of parasitoids on the selection by their host of an ovi- position site and the occurrence of submerged oviposition Submerged oviposition and egg mortality were done using water striders. The effects of egg para- Ten days after the last recorded oviposition event (22th August sitoids on the behaviour of damselflies and other aquatic in 2010), random samples of plants were collected at each local- insects are rarely investigated. This may be important be- ity, with five samples at least 2 m apart collected at each locality. cause damselflies have a markedly different oviposition We only sampled Juncus spp. and Equisetum spp., which bear noticeable scars after endophytic oviposition by Lestes. We were behaviour to that of the taxa previously studied. The aim not able to distinguish eggs of different species of Lestes, but L. of the present study is to determine whether L. sponsa has sponsa was the most abundant species at both sites. Earlier in a defensive strategy against egg parasitoids. In addition, the season, when observing the behaviour of L. sponsa, the posi- we wanted to reveal other potential benefits of underwater tion of the water level was marked on the stems of plants using oviposition. Two localities with a high and low population a Centropen Paint Marker, which indicated that the water level density of parasitoids, respectively, were used in this study. did not change during the experiment. A random sample of 204 Specifically, we addressed: (i) is there a difference in the of the collected plants was kept at a temperature of about 10°C overall number of eggs laid, the proportion of parasitized and processed within ten days of collection. Stems were cut into eggs or the number of dead eggs (undeveloped or damaged 5 cm long segments and their position relative to the surface of the water recorded. All eggs were excised from plant tissues in eggs) when L. sponsa lays eggs under or above the surface each segment. Developing, parasitized and dead eggs were visu- of the water, (ii) does the depth in the water or height above ally determined using a dissecting microscope at a magnification the water affect the proportion of the above mentioned egg of 40×. The development of damselfly and egg parasitoids was categories. Our study hypotheses were: (1) parasitoids in- relatively fast and therefore also clearly visible. It was possible fluence damselfly behaviour, therefore in the locality with to distinguish between “developing eggs” and “eggs containing a low risk of parasitism few eggs should be laid under the parasitoids” as parasitoid
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