Optimal Conditions for Diapause Survival of Aprostocetus fukutai, an Egg Parasitoid for Biological Control of Anoplophora chinensis.

Aprostocetus fukutai is a specialist egg parasitoid of the citrus longhorned beetle Anoplophora chinensis, a high-risk invasive pest of hardwood trees. The parasitoid overwinters as diapausing mature larvae within the host egg and emerges in early summer in synchrony with the egg-laying peak of A. chinensis. This study investigated the parasitoid's diapause survival in parasitized host eggs that either remained in potted trees under semi-natural conditions in southern France or were removed from the wood and held at four different humidities (44, 75, 85-93 and 100% RH) at 11 °C or four different temperature regimes (2, 5, 10 and 12.5 °C) at 100% RH in the laboratory. The temperature regimes reflect overwintering temperatures across the parasitoid's geographical distribution in its native range. Results show that the parasitoid resumed its development to the adult stage at normal rearing conditions (22 °C, 100% RH, 14L:10D) after 6- or 7-months cold chilling at both the semi-natural and laboratory conditions. It had a low survival rate (36.7%) on potted plants due to desiccation or tree wound defense response. No parasitoids survived at 44% RH, but survival rate increased with humidity, reaching the highest (93.7%) at 100% RH. Survival rate also increased from 21.0% at 2 °C to 82.8% at 12.5 °C. Post-diapause developmental time decreased with increased humidity or temperature. There was no difference in the lifetime fecundity of emerged females from 2 and 12.5 °C. These results suggest that 100% RH and 12.5 °C are the most suitable diapause conditions for laboratory rearing of this parasitoid.

Optimizing Parasitoid and Host Densities for Efficient Rearing of Ontsira mellipes (Hymenoptera: Braconidae) on Asian Longhorned Beetle (Coleoptera: Cerambycidae).

Ontsira mellipes Ashmead is a gregarious larval ectoparasitoid of woodboring cerambycids. It is native to North America but can readily attack the exotic Asian longhorned beetle, Anoplophora glabripennis (Motschulsky). This study aimed to develop an efficient rearing system for this parasitoid, as a potential novel association biocontrol agent for the beetle, by investigating the effects of different densities of host (two, three, or four larvae) and parasitoid (one, two, three, four, five, six, seven, and eight female wasps) on Ontsira's parasitization efficiency and reproductive outcomes. Results showed that overall parasitism and total numbers of parasitized hosts or progeny produced increased with host and/or parasitoid densities, but the number of parasitized hosts or progeny produced per female parasitoid decreased with parasitoid density at each given host density. Nonlinear regression indicated a consistent pattern of mutual interference as parasitoid density increased. Additional experiments showed that superparasitism (indirect interference) did not occur probably because the parasitoid detects hosts through vibration cues from host feeding and attacked (thus paralyzed) hosts are no longer detectable. Thus, the interference probably results from direct or exploitative competition. Interestingly, female parasitoids responded to increased parasitoid density with a significant increase in clutch size. Overall, per capita parasitization efficiency or reproductive outcomes were optimized at a low parasitoid-host ratio but with large group size of hosts and parasitoids. Therefore, an optimal combination of exposing three or four parasitoids to four hosts is proposed for efficient mass-rearing of this parasitoid.

Reproductive Traits of Ontsira mellipes (Hymenoptera: Braconidae), a North American Parasitoid, as a Novel Biological Control Agent for Exotic Anoplophora glabripennis (Coleoptera: Cerambycidae).

Ontsira mellipes Ashmead is a gregarious larval ectoparasitoid of woodboring cerambycids that is native to North America but can readily attack the exotic Asian longhorned beetle, Anoplophora glabripennis (Motschulsky). To evaluate the potential of the parasitoid as a novel association control agent for the pest beetle, this study investigated some key reproductive traits of the parasitoid, including egg maturation dynamics, and host size preference and suitability in association with the beetle. Results showed that female wasps emerged with a substantial portion (38%) of their lifetime complement of mature eggs and matured eggs rapidly, reaching a peak 4-6 d post-eclosion. The number of mature eggs was positively related to the female wasp's body size. Oviposition prompted production of more mature eggs by young female wasps. The parasitoid did not show a significant preference for large over small hosts in a choice test. Host size did not affect the parasitoid's offspring survival, developmental time, or sex ratio. However, clutch size increased with increasing host size. Female wasps that developed from large hosts had larger body size and consequently a higher mature egg load than those reared from small hosts. Neither longevity nor the total number of parasitized hosts over a female's lifetime was affected by the female's size, but the total number of offspring produced per female increased with the female's size. These results have important implications for improving rearing and field-release strategies as well as understanding the ecological mechanisms underlying host size selection in gregarious parasitoids.

Cerambycid Communities and Their Associated Hymenopteran Parasitoids From Major Hardwood Trees in Delaware: Implications for Biocontrol of Invasive Longhorned Beetles.

Cerambycidae provide important ecological services in forests yet cause economic damage when they infest living trees. Parasitoids can regulate woodborer populations, providing considerable control of pest cerambycids. Identifying parasitoids of native cerambycids may be useful in managing cerambycid outbreaks and aid in new-association biocontrol of exotic invasive cerambycids. We investigated Cerambycidae and associated hymenopteran parasitoid communities infesting Acer rubrum, Pinus virginiana, and Carya tomentosa from a forest in Delaware from 2005 to 2012. Cerambycid abundance, diversity, and richness, as well as parasitoid abundance, were measured by collecting trees in different conditions: felled, girdled, and naturally infested. Effect of edge or interior red maple on cerambycid abundance, diversity, and richness was examined. Over 14,500 cerambycids of 56 species and 38 genera were collected during the 7-yr period. Eleven species represented 95% of all cerambycids collected. Treatment only affected red maple, showing increased cerambycid richness and diversity from naturally infested trees. Cerambycid richness and diversity were two times greater on hickory than other species when combining girdled and felled treatments. Over 19,000 parasitic Hymenoptera of 12 families emerged from woodborer-infested wood with >70% of individuals belonging to Braconidae. Thirteen known species, and two unknown species, of Braconidae were identified from a subsample of 495 specimens; Ontsira mellipes (Ashmead) (Hymenoptera: Braconidae) and Rhoptrocentrus piceus Marshall (Hymenoptera: Braconidae) were the most abundant. This study provides fundamental information on native parasitoids associated with Cerambycidae, including cerambycid larval host associations. Parasitoids identified herein should be investigated for potential adaptation to invasive Cerambycidae to benefit invasive woodborer management.

Life History, Reproductive Biology, and Larval Development of Ontsira mellipes (Hymenoptera: Braconidae), a Newly Associated Parasitoid of the Invasive Asian Longhorned Beetle (Coleoptera: Cerambycidae).

The invasive Asian longhorned beetle, Anoplophora glabripennis (Motschulsky), is a destructive xylophagous forest pest species originating from Asia. Several endemic North American hymenopteran (Braconidae) species in the mid-Atlantic region were capable of attacking and reproducing on A. glabripennis larvae in laboratory bioassays. Ontsira mellipes Ashmead (Hymenoptera: Braconidae) has been continually reared on A. glabripennis larvae at USDA-ARS BIIRU since 2010, and has been identified as a potential new-association biocontrol agent. Two experiments were conducted to investigate parasitism, paralysis, reproductive biology, larval development, and longevity of adult O. mellipes In the first experiment, pairs of adult parasitoids were given single A. glabripennis larvae every 2 d (along with honey and water) over their lifetimes, while in the second experiment individual parasitoids were observed daily from egg to adult, and adults were subsequently starved. Adults in the first experiment parasitized ∼21% of beetle larvae presented to them throughout their life, and paralysis of larvae occurred 1-2 d after oviposition. More than half of the individual pairs parasitized A. glabripennis larvae, with each female producing around 26 offspring throughout her life. In the second experiment, median development time of O. mellipes from egg to adult was about 3 wk, with five larval instars. Adult O. mellipes that were provided with host larvae, honey, and water lived 9 d longer than host-deprived and starved adults. These findings indicate that mass-rearing procedures for O. mellipes may be developed using the new association host for development of effective biocontrol programs against A. glabripennis.

Potential New Associations of North American Parasitoids With the Invasive Asian Longhorned Beetle (Coleoptera: Cerambycidae) for Biological Control.

The Asian longhorned beetle, Anoplophora glabripennis (Motschulsky), is a polyphagous wood-boring insect native to Asia. Since it invaded North America in the 1990s, the beetle has been continuously targeted by quarantines and eradication programs in the United States and Canada. We examined the potential for development of new species-associations between A. glabripennis and hymenopteran parasitoids collected from cerambycids and other wood-boring insects infesting red maple (Acer rubrum L.) trees in the mid-Atlantic region of the United States. Results of our study showed that five groups of braconid parasitoids (Ontsira mellipes Ashmead, Rhoptrocentrus piceus Marsh, Spathius laflammei Provancher, Heterospilus spp., and Atanycolus spp.) successfully attacked early instars of A. glabripennis larvae infesting red maple logs and produced both male and female progenies. One species, O. mellipes, was continuously reared on A. glabripennis larvae inserted inside small red maple sticks for over 50 generations, and produced female-biased progeny (∼6:1 female to male ratio) at each generation. Continuous rearing of O. mellipes on A. glabripennis larvae did not significantly increase the parasitism and mean number of progeny produced per parasitized host. Together, these findings demonstrate that some North American parasitoids may be able to develop new associations with A. glabripennis and thus should be further studied under semifield or field conditions for possible use in biocontrol.