Assessing the host range of Anastatus orientalis, an egg parasitoid of spotted lanternfly (Lycorma delicatula) using Eastern U.S. non-target species.

The spotted lanternfly, Lycorma delicatula (Hemiptera: Fulgoridae), an invasive planthopper discovered in Pennsylvania, U.S. in 2014, has spread to many surrounding states despite quarantines and control efforts, and further spread is anticipated. A classical (importation) biological control program would contribute to the long-term management of L. delicatula in the eastern U.S. In its native range of China, Anastatus orientalis (Hymenoptera: Eupelmidae), an egg parasitoid, causes significant mortality. Anastatus orientalis consists of multiple haplotypes that differ in important biological parameters. To delineate the physiological host range of A. orientalis Haplotype C, we completed no-choice and choice testing. No-choice testing of non-target eggs from 36 insect species spanning six orders and 18 families showed that physiologically this haplotype of A. orientalis can develop in a variety of host species eggs from the families Coreidae, Fulgoridae, Pentatomidae, and Saturniidae. Ten of the 16 species that were attacked in the no-choice tests were also attacked in the choice tests. The production of progeny on non-target egg masses was significantly lower than on the controls (L. delicatula egg masses run simultaneously) in the no-choice and choice tests. For the non-target species that were attacked and resulted in female wasp progeny, these females were able to produce their own progeny at the same rate as control females that were reared from the L. delicatula eggs. Larger host eggs corresponded to an increased female-biased sex ratio of the progeny, suggesting that gravid females select them for fertilized eggs. Results from these studies suggest that A. orientalis Haplotype C prefers to parasitize L. delicatula egg masses but is capable of developing in some non-target species.

Footprints and Ootheca of Lycorma delicatula Influence Host-Searching and -Acceptance of the Egg-Parasitoid Anastatus orientalis.

The spotted lanternfly, Lycorma delicatula White (1845) (Hemiptera: Fulgoridae), is an invasive insect that was first reported in North America in Berks County, Pennsylvania, in 2014. It is a polyphagous phloem feeder that attacks over 70 plant species, threatening the agricultural, lumber, and ornamental industries of North America. Infestations of the pest have been reported in several U.S. counties, and a lack of endemic predators and parasitoids feeding on L. delicatula suggests a release from natural enemies in the invaded range. An egg-parasitoid Anastatus orientalis (Hymenoptera: Eupelmidae) was reported attacking L. delicatula at high rates in its native range and may play a key role in reducing its populations there. To better understand the foraging behavior of A. orientalis, a series of behavioral experiments were conducted to determine successful parasitism and behavioral responses to traces left by adult L. delicatula and to the oothecae which cover their eggs. Our results suggest that wasps detected chemical traces left by L. delicatula adults while walking on surfaces and exhibited a strong arrestment response. Moreover, wasps preferred to oviposit in egg masses with intact oothecae. The implications of these findings are herein discussed with regard to the exploitation of host kairomones by foraging wasps, as well as to its ability to overcome host structural defenses.

Halyomorpha halys (Hemiptera: Pentatomidae) Responses to Traps Baited With Pheromones in Peach and Apple Orchards.

Monitoring insect populations is a fundamental component of integrated pest management programs. In many cropping systems, monitoring is accomplished through captures in baited traps. The aggregation pheromone and pheromone synergist for the invasive Halyomorpha halys (Hemiptera: Pentatomidae) are known. We compared the response of H. halys to commercial lures in peach and apple orchards. Two commercial pheromone formulations, PHEROCON Trécé BMSB ('Trécé') and AgBio Inc. Stink Bug Xtra Combo ('Xtra Combo'), were compared with unbaited traps in peach orchards in 2015 and 2016 and in an apple orchard in 2016. In both crops and years, more H. halys responded to the Trécé lure, and fruit from trees near baited traps had correspondingly higher injury. In both years, peach fruit near Trécé baited traps had significantly higher feeding injury (52.2 ± 5.0%) than fruit near Xtra Combo baited and unbaited traps (35.2 ± 4.5% and 22.2 ± 3.4%, respectively). Injury to apple fruit near baited traps in 2016 was significantly different from fruit near unbaited traps (Trécé: 93.0 ± 3.8%, Xtra Combo: 74.1 ± 5.1%, and unbaited: 19.0 ± 2.7%). A field response index, which quantifies attraction of H. halys to each lure, demonstrated an equal response to both lures in 2015 peach and a higher response to Trécé lure in 2016 in both crops, which suggests the lure is pulling bugs from a larger area. We conclude that formulation differences, population pressure, and host plant species influence H. halys populations' response and resulting injury, and should be considered for trap-based decision management.

Biological control effects of non-reproductive host mortality caused by insect parasitoids.

As the rate of spread of invasive species increases, consumer-resource communities are often populated by a combination of exotic and native species at all trophic levels. In parasitoid-host communities, these novel associations may lead to disconnects between parasitoid preference and performance, and parasitoid oviposition may result in death of the parasitoid offspring, death of the host, or death of both. Despite their relevance for biological control risk and efficacy assessments, the direct and indirect population-level consequences of parasitoids attacking and killing their hosts without successfully reproducing (non-reproductive mortality) are poorly understood. Non-reproductive mortality induced by egg parasitoids (parasitoid-induced host egg abortion) may be particularly important for understanding the population dynamics of the invasive agricultural pest Halyomorpha halys (Hemiptera: Pentatomidae) and endemic stink bugs in North America, which are attacked by a suite of both native and introduced egg parasitoids. It is unclear, however, how various factors controlling parasitoid foraging and developmental success manifest at the population level. We constructed two related versions of a two-host-one-parasitoid model to evaluate the population-level consequences of non-reproductive host mortality. Egg abortion can result in strong negative or positive enemy-mediated indirect effects, taking the form of apparent competition, apparent parasitism, apparent amensalism, or apparent commensalism. For parasitoids limited in their reproductive output by the number of eggs they can produce, higher non-reproductive host mortality can reduce the strength of the positive indirect effect in cases of apparent parasitism, and it can reduce the negative indirect effect on the more suitable host in cases of apparent competition. For time-limited parasitoids, unsuitable hosts with high levels of non-reproductive parasitoid-induced mortality can be strongly suppressed in the presence of a suitable host, while the suitable host is only negligibly impacted (i.e., apparent amensalism). We evaluate these model-derived hypotheses within the context of H. halys and its native and nonnative parasitoids in North America, and discuss their application to risk assessment in biological control programs.

Hidden risks and benefits of natural enemy-mediated indirect effects.

Polyphagous natural enemies can mediate a variety of indirect interactions between resource populations. Such indirect interactions are often reciprocally negative (i.e. apparent competition), but the sign of effects between resource populations can be any combination of positive (+), negative (-), or neutral (0). In this article we focus on parasitoids to illustrate the importance of natural enemy-mediated indirect interactions in predicting risk and efficacy in biological control. We review recent findings to illustrate how an improved understanding of parasitoid behavioral ecology may increase model accuracy.

Perennial Grain and Oilseed Crops.

Historically, agroecosystems have been designed to produce food. Modern societies now demand more from food systems-not only food, fuel, and fiber, but also a variety of ecosystem services. And although today's farming practices are producing unprecedented yields, they are also contributing to ecosystem problems such as soil erosion, greenhouse gas emissions, and water pollution. This review highlights the potential benefits of perennial grains and oilseeds and discusses recent progress in their development. Because of perennials' extended growing season and deep root systems, they may require less fertilizer, help prevent runoff, and be more drought tolerant than annuals. Their production is expected to reduce tillage, which could positively affect biodiversity. End-use possibilities involve food, feed, fuel, and nonfood bioproducts. Fostering multidisciplinary collaborations will be essential for the successful integration of perennials into commercial cropping and food-processing systems.

Release of genetically engineered insects: a framework to identify potential ecological effects.

Genetically engineered (GE) insects have the potential to radically change pest management worldwide. With recent approvals of GE insect releases, there is a need for a synthesized framework to evaluate their potential ecological and evolutionary effects. The effects may occur in two phases: a transitory phase when the focal population changes in density, and a steady state phase when it reaches a new, constant density. We review potential effects of a rapid change in insect density related to population outbreaks, biological control, invasive species, and other GE organisms to identify a comprehensive list of potential ecological and evolutionary effects of GE insect releases. We apply this framework to the Anopheles gambiae mosquito - a malaria vector being engineered to suppress the wild mosquito population - to identify effects that may occur during the transitory and steady state phases after release. Our methodology reveals many potential effects in each phase, perhaps most notably those dealing with immunity in the transitory phase, and with pathogen and vector evolution in the steady state phase. Importantly, this framework identifies knowledge gaps in mosquito ecology. Identifying effects in the transitory and steady state phases allows more rigorous identification of the potential ecological effects of GE insect release.

Do trade-offs have explanatory power for the evolution of organismal interactions?

The concept of a trade-off has long played a prominent role in understanding the evolution of organismal interactions such as mutualism, parasitism, and competition. Given the complexity inherent to interactions between different evolutionary entities, ecological factors may especially limit the power of trade-off models to predict evolutionary change. Here, we use four case studies to examine the importance of ecological context for the study of trade-offs in organismal interactions: (1) resource-based mutualisms, (2) parasite transmission and virulence, (3) plant biological invasions, and (4) host range evolution in parasites and parasitoids. In the first two case studies, mechanistic trade-off models have long provided a strong theoretical framework but face the challenge of testing assumptions under ecologically realistic conditions. Work under the second two case studies often has a strong ecological grounding, but faces challenges in identifying or quantifying the underlying genetic mechanism of the trade-off. Attention is given to recent studies that have bridged the gap between evolutionary mechanism and ecological realism. Finally, we explore the distinction between ecological factors that mask the underlying evolutionary trade-offs, and factors that actually change the trade-off relationship between fitness-related traits important to organismal interactions.