Multiparasitism enables a specialist endoparasitoid to complete parasitism in an unsuitable host caterpillar

Abstract

Parasitoid wasps serve as natural enemies of numerous insect species; therefore, knowledge of host-parasitoid interactions is fundamental for understanding ecosystems. Each endoparasitoid wasp taxon exhibits a specific host range. Female parasitoids, however, occasionally oviposit into non-host species. Since the survival probability of eggs in non-host species is virtually zero, these behaviors have long been considered maladaptive. However, in the present study, we found that eggs of a specialist parasitoid, Cotesia kariyai (Hymenoptera: Braconidae), oviposited in unsuitable host caterpillars, Mythimna loreyi (Lepidoptera: Noctuidae), successfully complete larval development in the non-host when these caterpillars are simultaneously oviposited by another naturally sympatric parasitoid wasp, Meteorus pulchricornis (Hymenoptera: Braconidae), for which My. loreyi is the usual host. This observation suggests that the seemingly maladaptive behavior of ovipositing in unsuitable host insects can be adaptive, allowing them to maintain reproductive potential in environments where their ordinary hosts are absent. We propose a new term, "pirate parasitism", for this type of obligatory multiparasitism. Understanding detailed mechanisms of this phenomenon may provide deeper insights into parasitoid-host dynamics and evolution of host use strategies by parasitoids.

Keywords: Cotesia kariyai; Meteorus pulchricornis; Mythimna loreyi; Kleptoparasitism; Multiparasitism; Pirate parasitism.

Fig. 1

Outcome of multiparasitism by Cotesia kariyai (Ck) and Meteorus pulchricornis (Mp) in Mythimna loreyi (Myl) caterpillars. The successful parasitism rate of each parasitoid in 3rd, 4th or 5th instar Myl caterpillars (a), and number of emerged wasps per caterpillar when Ck emerged from the caterpillars (b). Mys = My. separata. (∗P < 0.05; ∗∗P < 0.01 and ∗∗∗P < 0.001 by binomial test; N.S.: no significant differences by Chi-square test, Bars labeled with the same letter are not significantly different on the basis of Tukey’s HSD test after ANOVA)

Fig. 2

Effects of order and interval of oviposition by two parasitoids on outcomes of multiparasitism. The successful parasitism rate of each parasitoid in 4th instar Myl caterpillars (a), and numbers of wasps per caterpillar when Ck emerged from the caterpillars in different orders and intervals of oviposition by two parasitoids (b). Myl = Mythimna loreyi, Mys = My. separata, Ck = Cotesia kariyai, and Mp = Meteorus pulchricornis. (∗P < 0.05; ∗∗P < 0.01 and ∗∗∗P < 0.001 by binomial test; bars labeled with the same letter are not significantly different on the basis of (a) Tukey’s WSD teat after Chi-square test and (b) Tukey’s HSD test after ANOVA.)

Fig. 3

Observation of parasitoid larvae in Mythmna loreyi caterpillars. Preparation and dissection timing of parasitized caterpillars used for observation (a) and observed larvae of two parasitoids in multiparasitized Myl caterpillar (b). Proportion of observed parasitoid larvae is shown in (c). Myl = Mythimna loreyi, Ck = Cotesia kariyai, and Mp = Meteorus pulchricornis.

Fig. 4

Outcome of simultaneous free-oviposition rearing experiments in cages. Results of each 10 replications and their total are shown.

Fig. 5

Pirate parasitism: Introducing a new term. Obligatory multiparasitism refers to kleptoparasitic parasitism by a parasitoid that requires oviposition by another parasitoid species either to (a) reach the host, or (b) complete its development in the host after oviposition. In the latter case, termed “pirate multiparasitism”, parasitism is defined as occurring when a parasitoid necessitates prior or subsequent parasitism by another parasitoid species and can complete its development through multiparasitism.