Development of the Hyperparasitoid Eurytoma Goidanichi Boucek (Hymenoptera: Eurytomidae) and the Primary Role of the Mother Wasp

Animal Biology 58 (2008) 113–121 www.brill.nl/ab

Development of the hyperparasitoid Eurytoma goidanichi Boucek (Hymenoptera: Eurytomidae) and the primary role of the mother wasp

Jun Tagawa*, Keiji Komatsubara, Naohiro Oka, and Yasuko Satoh Department of Biosphere-Geosphere System Science, Faculty of Informatics, Okayama University of Science, Okayama 700-0005, Japan

Abstract Development of the solitary hyperparasitoid Eurytoma goidanichi Boucek (Hymenoptera: Eurytomidae), which attacks cocoons of the gregarious parasitoid Cotesia glomerata L. (Hymenoptera: Braconidae), was investigated. Within one day after being laid in cocoons of C. glomerata, eggs of E. goidanichi were transplanted into healthy host cocoons of various ages. In the laboratory, hyperparasitoid and host development within cocoons was observed through slits in the cocoons. The survival rate of eggs transplanted into young (0–1-day-old or 2–3-day-old) cocoons reached 80% or more; that of eggs transplanted into 4–5-day-old cocoons was 70%. However, eggs transplanted into old (6–7-day-old) cocoons failed to develop, and all the hosts of this age emerged as adults. At 20°C, the mean egg duration of E. goidanichi was 2.8 days. Larvae moulted four times and pupated 8.7 days after hatching, a few days after reaching their maximum size. Mean adult ecdysis occurred 8.9 days after pupation. The pupae of those E. goidanichi which had developed in 2–3-day-old or 4–5-day-old cocoons were smaller than pupae of wasps that had developed in 0–1-day-old cocoons. Hosts continued development while being devoured by E. goidanichi larvae, but no developmental progress was observed after removal of hyperparasitoid eggs from naturally parasitized hosts. Apparently, E. goidanichi females halt host development at the time of parasitization and are thereby able to improve their utilization of host cocoons.

Keywords Hyperparasitoid; Eurytoma goidanichi; Cotesia glomerata; developmental arrest; paralysis; survival rate

Introduction Cotesia glomerata L. (Braconidae) is a common gregarious endoparasitoid wasp which, in Japan, attacks mainly the larvae of the small white butterfly, Pieris rapae crucivora Boisduval (Pieridae). After egression from their hosts, the parasitoid larvae pupate in

*) Corresponding author; e-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2008 DOI: 10.1163/157075608X303672 114 Jun Tagawa et al. / Animal Biology 58 (2008) 113–121 cocoons, which are typically clustered on or near food plants. The cocoons of this parasitoid are, as in other primary parasitoids (Askew, 1971), in turn parasitized by hyperparasitoids (Matsuzawa, 1958). One such hyperparasitoid, Eurytoma goidanichi Boucek (Eurytomidae), attacks the cocoons of C. glomerata, irrespective of their developmental stadium. However, the high mortality of eggs laid in old cocoons (Tagawa and Fukushima, 1993; Tagawa et al., 2000) suggests that old pupae are less suitable resources for this solitary ectoparasitoid. Because females laid more male eggs in old cocoons than in young ones, they were considered to be able to discriminate between young and old hosts qualitatively. Nevertheless, E. goidanichi females showed no host- age preference, even when young hosts were available (Tagawa et al., 2000). In this regard, several factors, such as host-searching efficiency, longevity and egg load, were considered to affect the decision of E. goidanichi females (Tagawa et al., 2000), as in many other parasitoids (Iwasa et al., 1984; Parker and Courtney, 1984; Skinner, 1985; Waage, 1986; Charnov and Skinner, 1988; Minkenberg et al., 1992; Heimpel et al., 1996; Mackauer et al., 1996). However, these factors alone cannot account for the behaviour of females when they encounter old host cocoons. Tagawa and Fukushima (1993) reported that some E. goidanichi eggs laid in cocoons a day prior to host emergence developed into adults. In cases where host development is not arrested by the hyperparasitoid, eggs must hatch within a day after deposition. For another hyperparasitoid, Eurytoma appendigaster, attacking cocoons of the gypsy moth parasitoid, Cotesia melanoscela, the egg period was estimated as ca. 2 days (Muesebeck and Dohanian, 1927). The arrest of host development by an immature wasp or its mother is necessary if E. goidanichi eggs require a similar period to hatch. In general, ectoparasitoids paralyze hosts before laying eggs (Askew, 1971); the effects of that paralysis differ among parasitoid species and hosts (Beard, 1952; Vinson and Iwantsch, 1980; Coudron et al., 1990; Deyrup et al., 2006). Therefore, to understand the oviposition strategy of E. goidanichi more fully, a study of the development of the hyperparasitoid and the host within a cocoon would seem potentially informative. The objective of this study was to investigate the larval development ofE. goidanichi in cocoons of C. glomerata of different age classes, and to demonstrate whether or not E. goidanichi halted host development.

Materials and methods Cocoon clusters of Cotesia glomerata L. were collected from cabbage fields in Okayama during the spring of 1998 and 2000, and maintained at 20°C under a L16:D8 photo- period regime (standard experimental conditions). A few days before adult emergence of the hyperparasitoid, the cocoons were separated and placed individually into 5-ml glass vials to obtain virgin wasps. Individuals of Eurytoma goidanichi Boucek that emerged from the collected cocoons of C. glomerata were sexed. One male and five females were kept together in a 30-ml glass vial for one week under standard conditions to ensure mating. During this period, adult parasitoids were fed honey and water. These females were used for the following oviposition experiments.