Behavioral And Developmental Strategies For Adapting The Heterogeneous Environmental Conditions Of The Generalist Ectoparasitoid Sclerodermus Pupariae (Hymenoptera: Bethylidae)

The native idiobiont ectoparasitoid, Sclerodermus pupariae Yang et Yao(Hymenoptera:Bethylidae), is originally discovered from parasitizing the larvae and pupae of the emerald ash borer(EAB), Agrilus planipennis Fairmaire(Coleoptera: Buprestidae). As a generalist, it also parasitizes some cerambycid and buprestid larvae, and has the abilities of excellent host location behavior, relatively short developmental duration, high reproductive ability, and extremely female biased population. This parasitoid usually locates their hosts by walking on or flying to the bark of host plant. Once detected, female parasitoid kills or paralyzes hosts before oviposition external of the host body. To clarify the adaptive ability of this bethylid parasitoid to varied environmental conditions, this study investigated the viability and adaptive mechanisms of this wasp in heterogeneous environmental conditions. The results of our researches were shown as follows:1. Different fitness of parasitoid was demonstrated when they rearing on different hosts.The selective parasitism ability of wasps to novel host, Massicus raddei, increased strongly over six targeted rearing generations, but the different scenario was observed on the natural host, Agrilus planipennis. Shorter time of handing, higher fertility and longevity, and subsequently low mortality of parasitoid on novel host were found as they were reared successively on the oak long-horned beetles(OLB, M. raddei). Results from the no-choice experiments indicated that parasitoids from the targeted strain showed better performance on OLB larvae than those on the emerald ash borer(EAB, A. planipennis); while parasitoids from the natural strain would gain more fitness on EAB than those on OLB. Further, searching ability of parasitoid to M. raddei from the targeted strain was significantly higher than that of parasitoid from the natural strain.2. Both early adult and adult learning of parasitoid would cause extremely biased in host preference and parasitism ability. Both the volatiles from EAB and OLB showed no significant difference in attraction the na?ve parasitoids whether they developed from the EAB or OLBlarvae. However, parasitoids were significantly attracted by the volatiles of EAB since they were reared from EAB larvae and subsequently emerged without interference. Even if the parasitoids developed from the OLB larvae and emerged without interference, they also showed no preference to both components of the volatiles. These results suggested that learning experience in early adult stage would influence the host seeking behavior of adult parasitoids; but food resources of immature parasitoids might have no significant impact on their behaviors in adult stage. Learning experience in adult stage had more important influence on parasitoid’s host seeking behavior. Associative learning experience with one host would promote the parasitoids more sensitive to the particular resources. Additionally, greater paralysis efficiency and higher OLB larvae parasitism were revealed when the parasitoids were exposed to the OLB conditions, although the parasitoids originally used the EAB larvae as host resources.3. A trade-off between grow larger and develop faster in parasitoid was observed when they encountering with different-sized host. Maternal parasitoids obtained lower rates of parasitism when inoculating small or large hosts due to early host death and parasitoid injury,respectively, indicating significant fitness costs associated with paralyzing those sizes of hosts.Host size was shown to have highly variable effects on selected fitness parameters. For maternal females, increasing initial host size led to increasing host-handling time, and fertility exhibited a parabolic relationship with host size. The highest fertility was exhibited when parasitoids oviposited on medium-sized hosts. Host-size effects were very apparent for parasitoid offspring, with the largest hosts producing later-emerging but larger females.Parasitoid offspring sex ratios in all host size classes were significantly female-biased, and exhibited a quadratic function with increasing host size. Assessment of host profitability revealed that medium-sized OLB larvae(middle 3rd instar) presented the best fitness return for the parasitoids. These findings suggest that this bethylid parasitoid can achieve a compromise in optimization of the two most important fitness functions when encountering an abundance of different-sized hosts.4. Successful parasitism and reproduction would be promoted by the higher foundress densities. Handling time and developmental duration of parasitoids decreased with increasing foundress densities. The early death of parasitoids that induced by host self-defending would be eliminated by the higher numbers of maternal wasp. Brood size of the parasitoids increased significantly when the number of maternal wasps ranged from one to four. However, further increases in foundress number did not affect the parasitoid brood size. The sex ratios of S.pupariae were always female-biased. The proportions of male in the progeny colonies were less than 10% throughout all experimental treatments. Under a restricted condition of food resource, body sizes of parasitoids significantly declined with increasing maternal parasitoid densities. Although the parasitoid body size reduced when maternal wasp number was higher, it could be compromised by the relatively higher number of female offspring produced.5. The increasing densities of consumers on a host larva would triggered more parasitoids to be winged ones. Higher densities of consumers on a host may encourage more individuals to be the migrated ones. These findings highlighted the phenotypic partitioning of wing morphology in parasitoid S. pupariae under varied environmental cues. Parasitism ability of winged or wingless female parasitoid showed no significant difference. Wingless female parasitoid was more fertile than winged individual. The reduction of parasitoids’ fecundity indicated that the energy used to construct wings and flight muscles would simply not available for reproductive investment. Moreover, winged or wingless progeny did not vary significantly in time to development. The Mendel’s law may not be a suitable explanation for the wing differentiation of this bethylid parasitoid, and wingless maternal parasitoids produced more winged progeny under laboratory conditions.6. Sclerodermus pupariae and Dastarcus helophoroides could coexist in the same habitat,and introducing multiple species of parasitic natural enemies could be feasible for management of the Asian long-horned beetle(ALB, Anoplophora glabripennis). Host parasitism rate by S.pupariae was not significantly different when either S. pupariae was exposed alone or together with adult of D. helophoroides, whereas this result would be changed as the parasitoid wasp was exposed together with the eggs of parasitic beetle, D. helophoroides. In the secondscenario, parasitism rate to ALB by S. pupariae were sharply declined. It seemed like that the bethylid wasp had advantage in ecological competition for host resources when comparing with adult of D. helophoroides; while parasitoid wasp became to a vulnerable one since the competitors were directly changed to the eggs of D. helophoroides. Total parasitism rate to ALB of both parasitoids(released together) were significantly higher than that of parasitoid was released alone. The multiparasitism was not observed in the experiments, indicating that intrinsic competition between the two species of parasitoids might seldom occur in the field.The two species of parasitoids could therefore coexist in the same habitat, and any adverse effects on the suppression of ALB populations caused by competitive behavior between the two species of parasitoids would likely be negligible.7. Sugar-rich foods exhibited the same function as the host hemolymph for parasitoid’s reproduction and longevity. The pre-oviposition duration was decreased significantly in parasitoid that with the experience of previous nutrition feeding. Fecundity of parasitoids which fed on honey had nonsignificant difference compare to the others. Survival analysis on this bethylid parasitoid showed that the longevity of newly emerged female parasitoid would be prolonged by the short process of nutritional supplements. The lifespan of parasitoid which fed on host hemolymph or honey were two times as long as that of the parasitoid only fed on distilled water. These findings suggested that the process of nutritional supplements of parasitoid before encountering the hosts is vital. The effects of feeding on host hemolymph or honey on the enhancement of parasitoid activity and longevity are equivalent. Thus, we proposed that it could achieve higher efficiency for using and protecting the natural enemy resources by furnishing some flowering plants around the parasitoid release sites in pest biological control programs.8. Maternal care of parasitoid would influence the survival of offspring. Guarding behavior is an important behavior in quasisocial insects, and this behavior is believed to improve the survival of offspring. A relatively higher mortality of offspring was observed once the absence of females in the case of more parasitoids developing on a host. During the developmental stages, only offspring in the late larval stage was sensitive to maternal guardingbehavior. In multiple foundresses experiment, both multiparous and nulliparous stepmothers showed guarding behavior and that this behavior improved the survival of the immature offspring. These results indicated that S. pupariae females display maternal care, whereas this behavior was conditionally- specific. Guarding behavior may not be triggered when the local condition was much suitable.In the present study, we investigated the intrinsic plasticity of behavioral and physiological of S. pupariae as they encountering the variable environmental conditions. We found that parasitoids would adapt one host species once they rearing on a host for several generations. Learning behavior in adult stage prompted the parasitoids obtained the ability to adapt the changing hosts and host habitats. Further, multiple parasitoid adults parasitized on a host ensured the success in host exploitation, and the increasing densities of consumers on a host would triggered more parasitoids to be winged ones that could guarantee the adult can more easily disperse to colonize habitats. Additionally, we also suggested that maternal care of adult parasitoids is essential for the successful development of immature parasitoids. Our results demonstrated that S. pupariae can more rapidly adapt to the heterogeneous conditions by their behavioral and physiological plasticities. These abilities guarantee the S. pupariae to be an excellent parasitic natural enemy in a wide range of fields.