The effect of direct interspecific competition on patch exploitation strategies in parasitoid wasps.

The presence of competitors may affect the pay-off of individuals' foraging strategies. They should therefore modify their resource exploitation decisions accordingly. In such a direct competition situation, theory predicts that individuals should stay longer on a resource patch than when foraging alone. However, models predicting patch residence time focus on intraspecific competition without agonistic interactions. Here, we investigate the patch use strategies of females of two parasitoid species, Eupelmus vuilleti and Dinarmus basalis, attacking the same host, Callosobruchus maculatus, knowing that D. basalis is more aggressive and can exclude E. vuilleti during pairwise contests for single hosts. Our results showed that time allocation and oviposition strategies differed in relation to the species and type of competition (i.e., presence/absence of competitor, simultaneous/sequential female introduction or resident/intruder female). Eupelmus vuilleti females tended to wait in the patch surroundings for D. basalis females' departure to return and exploit hosts parasitized by the opponent (after destruction of her eggs). In contrast, D. basalis females tended to self-superparasitize and stay motionless near the hosts. After detecting an E. vuilleti female entering the patch, they attacked and chased her permanently from the patch. Females of both species spent less time in the patch when faced with a competitor than when alone. This study is the first to test the influence of direct interspecific competition and arrival order on patch exploitation strategies in parasitoid species, and highlights the necessity to include agonistic behaviors in theoretical models predicting optimal patch residence time in competitive situations.

Reproduction in a variable environment: How does Eupelmus vuilleti, a parasitoid wasp, adjust oogenesis to host availability?

Oogenesis of the parasitoid wasp Eupelmus vuilleti is known to be dependent on host availability. However, examination of ovarian dynamics by microscopy showed that oogenesis and vitellogenesis are initiated before female eclosion and proceed 1-2 days after, independent of host presence. Oogenesis continued beyond the 2nd day only in the presence of hosts, otherwise it was replaced by egg resorption. It is thus possible to distinguish between host-independent and host-dependent periods of oogenesis. In the presence of host, each ovariole (three per ovary) contained generally three oocytes: a fully mature oocyte, a nearly mature one and an immature one. However, host deprived-females resorbed their most mature and their smallest oocytes, but kept one almost mature oocyte per ovariole. Comparison of zero, short and long host deprivation periods showed that females always had the ability to quickly lay eggs to exploit any new host. However, increased deprivation led to a reduction in the number and the viability of eggs. Enzymo-immunological measurements of ecdysteroids were made in whole females, in dissected ovaries and in newly laid eggs. Our results indicated that ecdysteroids play a major role as circulating hormones involved in the regulation of oogenesis.

Mitigation of egg limitation in parasitoids: immediate hormonal response and enhanced oogenesis after host use.

Synovigenic insects (i.e., insects emerging with few ripe eggs and maturing more eggs during the course of their lifetime) may suffer from transient egg limitation due to the stochastic nature of encounters with patchy hosts and the low availability of ripe eggs at any given time point. Egg limitation also affects the stability of host-parasitoid models. Thus, quantification of the behavioral decisions influencing egg maturation, identification of the underlying physiological mechanisms, and determination of the rate of egg maturation are highly relevant to both parasitoid behavioral ecology and host-parasitoid population dynamics. The aim of this study was to identify, in a highly controlled setting, the physiological processes responsible for egg manufacture after varying host use by a synovigenic parasitoid. We quantified the time course of the reproductive hormonal response and subsequent egg production in the host feeding bruchid parasitoid, Eupelmus vuilleti (Hymenoptera: Eupelmidae) for three treatments: (1) host examination without further host use, (2) host feeding, and (3) host feeding followed by oviposition. We carried out continuous behavioral observations with single hosts, enzyme immunoassays for quantifying ecdysteroids, and ovary dissection. Ecdysone levels increased within two minutes of contact with a host, the fastest hormonal response reported for any insect. Even simple contact with a host, without further host use, triggered an increase in hormone levels, leading to the maturation of a single egg, using body reserves only. Feeding on the host caused a much larger increase in ecdysone levels and was followed by a marked increase in oogenesis. Oviposition had a weak effect on hormone levels, but increased oogenesis. We discuss the mechanisms responsible for these rapid responses, the source of ecdysteroids, and the implications of our results for the population dynamics of host-parasitoid systems and the behavioral ecology of synovigenic species.

Host-induced ecdysteroids in the stop-and-go oogenesis in a synovigenic parasitoid wasp.

Eupelmus vuilleti (Hymenoptera; Eupelmidae) is a solitary ectoparasitoid producing yolk-rich eggs. The female oviposits mainly on the fourth larval instar of Callosobruchus maculatus (Coleoptera; Bruchidae), which develop within pods and seeds of Vigna unguiculata (Fabacae). Parasitoid females are synovigenic, i.e., they are born with immature eggs and need to feed from the host to sustain egg production during their entire lifetime. However, eggs are rapidly resorbed in unfavourable conditions and an efficient stop-and-go mechanism controls oogenesis in such animals. In this study, the possible involvement of ecdysteroids in the regulation of parasitoid oogenesis is examined. In a first step, the identity and titre of ecdysteroids in reproductively active and inactive female parasitoids were investigated by high performance liquid chromatography followed by enzyme immuno-assay (EIA/HPLC). A larger secretion of ecdysone was found in female during their reproductive period compared with inactive females. In a second step, both the secretion of ecdysteroids into the medium of in vitro incubated ovaries and the ecdysteroid content of females reared with or without host were measured (EIA). The presence of the host, which represents both the oviposition site and the nutritional source, induced an active biosynthesis of ecdysone. This synthesis started at a slow rate after host introduction and reached a maximum after 48 h. When hosts were available, this synthesis was cyclic and continuous during the entire female lifetime. These results showed that host presence triggered ovarian synthesis of ecdysteroids, which are involved in a stop-and-go regulation of egg production linked to host availability.

Importance of sterols acquired through host feeding in synovigenic parasitoid oogenesis.

Eupelmus vuilleti (Hymenoptera; Eupelmidae) is a host feeding ectoparasitoid of fourth-instar larvae or pupae of Callosobruchus maculatus (Coleoptera; Bruchidae) infecting Vigna unguiculata seed and pods (Fabacae). Parasitoid females are synovigenic, i.e. they are born with immature eggs and need to feed from the host in order to sustain egg production. In this study, the role of sterols obtained through host feeding in parasitoid oogenesis are examined. Quantitative and qualitative analyses of the sterol contents in each partner of the tritrophic interaction show that a parasitoid female's larval sterol contents is sufficient to produce only 30% of the total number of eggs laid throughout a female's life cycle. In a second step, by manipulating the composition of the sterols hemolymph in the host, it is shown that cholesterol obtained through adult nutrition plays a crucial role in the eggs viability but does not affect the egg production quantitatively. This result has important implications for understanding both the nutrient allocation strategy in this species and the impact of cholesterol in parasitoid reproduction.

Sources of chemical signals which enhance multiparasitism preference by a cleptoparasitoid.

The cleptoparasitoid Eupelmus vuilleti recognizes and prefers laying on hosts parasitized by Dinarmus basalis to unparasitized hosts. This recognition is based on the perception of a chemical substance deposited on the surface of the seed. Dufour's gland secretion and cuticular hydrocarbons of D. basalis are attractive and may mediate the host discrimination. This activity is linked to a mixture of linear and methyl alkanes whose source is apparently the Dufour's gland.

Analysis of multiparasitism by Eupelmus vuilleti (Craw) (Eupelmidae) and Dinarmus basalis (Rond) (Pteromalidae) in the presence of one of their common hosts, Bruchidius atrolineatus (Pic) (Coleoptera Bruchidae).

Bruchidius atrolineatus (Pic) is a tropical beetle (Coleoptera Bruchidae) that develops during the larval and pupal stages in the seeds of a legume Vigna unguiculata (Walp). Two species of Hymenoptera, Dinarmus basalis (Rond) and Eupelmus vuilleti (Craw), solitary ectoparasitoids of the larvae and pupae of B. atrolineatus, were introduced successively in the presence of their hosts, varying the interval between the two introductions. When D. basalis females were introduced 24 h, 3 days or 7 days after E. vuilleti, multiparasitism was low. The females had low fecundity, and their eggs were not distributed randomly over the different available hosts. When E. vuilleti females were introduced second, they oviposited on the different hosts availabe and did not avoid multiparasitism. The presence of hosts already parasitised by D. basalis increased the reproduction of E. vuilleti, and the fecundity of the females was higher than in control batches with E. vuilleti alone. E. vuilleti seems capable of detecting the ovipositor shafts drilled by the D. basalis females, and by introducing its own ovipositors killing the D. basalis eggs or larvae. When interspecific competition was occurring the number of E. vuilleti adults emerging from the seeds was no different from that observed in control batches with E. vuilleti alone, and there were always fewer D. basalis adults than in control batches (D. basalis alone). This interspecific competition reduces the influence of the two parasitoids in the biological control of bruchid populations.