George E. Heimpel

Landscape diversity enhances biological control of an introduced crop pest in the north-central USA

Arthropod predators and parasitoids provide valuable ecosystem services in agricultural crops by suppressing populations of insect herbivores. Many natural enemies are influenced by non-crop habitat surrounding agricultural fields, and understanding if, and at what scales, land use patterns influence natural enemies is essential to predicting how landscape alters biological control services. Here we focus on biological control of soybean aphid, Aphis glycines Matumura, a specialist crop pest recently introduced to the north-central United States. We measured the amount of biological control service supplied to soybean in 26 replicate fields across Michigan, Wisconsin, Iowa, and Minnesota across two years (2005-2006). We measured the impact of natural enemies by experimentally excluding or allowing access to soybean aphid infested plants and comparing aphid population growth over 14 days. We also monitored aphid and natural enemy populations at large in each field. Predators, principally coccinellid beetles, dominated the natural enemy community of soybean in both years. In the absence of aphid predators, A. glycines increased significantly, with 5.3-fold higher aphid populations on plants in exclusion cages vs. the open field after 14 days. We calculated a biological control services index (BSI) based on relative suppression of aphid populations and related it to landscape diversity and composition at multiple spatial scales surrounding each site. We found that BSI values increased with landscape diversity, measured as Simpsons D. Landscapes dominated by corn and soybean fields provided less biocontrol service to soybean compared with landscapes with an abundance of crop and non-crop habitats. The abundance of Coccinellidae was related to landscape composition, with beetles being more abundant in landscapes with an abundance of forest and grassland compared with landscapes dominated by agricultural crops. Landscape diversity and composition at a scale of 1.5 km surrounding the focal field explained the greatest proportion of the variation in BSI and Coccinellidae abundance. This study indicates that natural enemies provide a regionally important ecosystem service by suppressing a key soybean pest, reducing the need for insecticide applications. Furthermore, it suggests that management to maintain or enhance landscape diversity has the potential to stabilize or increase biocontrol services.

Ecology and Management of the Soybean Aphid in North America

The soybean aphid, Aphis glycines Matsumura, has become the single most important arthropod pest of soybeans in North America. Native to Asia, this invasive species was first discovered in North America in July 2000 and has rapidly spread throughout the northcentral United States, much of southeastern Canada, and the northeastern United States. In response, important elements of the ecology of the soybean aphid in North America have been elucidated, with economic thresholds, sampling plans, and chemical control recommendations widely adopted. Aphid-resistant soybean varieties were available to growers in 2010. The preexisting community of aphid natural enemies has been highly effective in suppressing aphid populations in many situations, and classical biological control efforts have focused on the addition of parasitoids of Asian origin. The keys to sustainable management of this pest include understanding linkages between the soybean aphid and other introduced and native species in a landscape context along with continued development of aphid-resistant varieties.

PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency.

We used polymerase chain reaction to determine whether Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae) DNA was present in the guts of larvae and adult males and females of the generalist predator Coleomegilla maculata De Geer (Coleoptera: Coccinellidae). The predators were fed Ostrinia nubilalis egg masses and allowed to digest at either 20 °C or 27 °C for time spans ranging from 0 to 12 h. Four primer pairs, specific for O. nubilalis were developed, using a nuclear ribosomal RNA sequence including part of the 18S gene, the complete internal transcribed spacer (ITS‐1) region and part of the 5.8S gene. These primers amplified four sequences that were 492, 369, 256 and 150 base pairs long. We found a significant negative effect of time since feeding on the number of bands that could be detected. The shortest fragment was detected for the longest time after feeding (up to 12 h). We found no effect of predator weight, sex, developmental stage, or meal size on the time course over which bands of varying lengths could be detected.

Comparing floral nectar and aphid honeydew diets on the longevity and nutrient levels of a parasitoid wasp

We compared the effects of floral nectar from buckwheat, Fagopyrum esculentum Moench, and honeydew produced by the soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae), on longevity, nutrient levels, and egg loads of the parasitoid Diadegma insulare Cresson (Hymenoptera: Ichneumonidae). Diadegma insulare lived for 2 days in control treatments of water or clean soybean leaves, for 6–7 days with honeydew, and in excess of 2 weeks with buckwheat nectar. Potential reasons for the superiority of buckwheat nectar over soybean aphid honeydew for extending the longevity of parasitoids include: (i) parasitoids ingest more sugars from floral sources, (ii) oligosaccharides in honeydew have a lower nutritional value than nectar sugars, and (iii) honeydew has antagonistic compounds. Overall sugar levels were lower in honeydew‐ vs. nectar‐fed female wasps, suggesting a lower feeding rate, but other explanations cannot be excluded. Diadegma insulare eclosed with high levels of lipids and glycogen, and low levels of gut and storage sugars. All carbohydrates increased over the life of both nectar‐ and honeydew‐fed wasps, but remained low or decreased in starved wasps. Lipid levels declined over the lifespan of female wasps, but females fed floral nectar showed the slowest rate of lipid decline. Diet did not affect egg load, probably because the females were not given hosts in the experiment.

Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp

Lifetime patterns of carbohydrate and lipid metabolism were compared in starved and sucrose‐fed adults of the parasitoid Macrocentrus grandii (Goidanich) (Hymenoptera: Braconidae). As expected, sucrose‐fed individuals lived longer than did starved individuals. Macrocentrus grandii males and females eclosed with levels of simple storage sugars (presumably primarily trehalose) and glycogen that were below maximum levels recorded from sucrose‐fed parasitoids. Both of these nutrients dropped to very low levels in starved individuals within 4 days post‐emergence and were maintained at high levels in sucrose‐fed individuals throughout their lives. Lipid reserves at emergence represented the highest lipid levels for both sexes in the two diet treatments, with levels declining over the lifetimes of males and females from both diet treatments. Our results therefore suggest that dietary sucrose is used to synthesize trehalose and glycogen, but not lipids in M. grandii. Also, in contrast to the patterns observed for the simple sugars and glycogen, lipid levels in starved individuals did not drop below levels observed in sugar‐fed individuals. The average number of mature eggs carried by females at emergence was 33 and increased to approximately 85 in sucrose‐fed and 130 in starved females by the age of 5 d in the absence of hosts. The egg maturation rate was therefore higher in starved than in sugar‐fed females. Potential explanations for this unexpected result are discussed.

Plant-Provided Food for Carnivorous Insects: Does floral nectar improve biological control by parasitoids?

Introduction The incorporation of plant diversity within agricultural systems has led to decreased insect pest densities in approximately 50% of studies in which monocultures and polycultures were directly compared (Risch et al . 1983; Andow 1991; Coll 1998; Gurr et al . 2000). One of the leading hypotheses explaining the observation of decreased pest densities under polycultures is that increased plant diversity can enhance the action of natural enemies of pests (the “enemies hypothesis” of Root 1973). Increased plant diversity can provide natural enemies with resources such as a favorable microclimate, alternative hosts or prey, or plant-based foods such as pollen, nectar, or honeydew (Landis et al . 2000). In this chapter, we focus on one of the more intuitively clear predictions encompassed within Roots enemies hypothesis – the idea that the presence of nectar-producing plants can improve biological control of pests by supplying parasitoids with sugar. Note that this idea includes two components: an outcome (improved biological control) and an underlying mechanism (nectar-feeding), both of which need to be demonstrated. We refer to the combined outcome and mechanism as the “parasitoid nectar provision hypothesis”. The hypothesis that plant diversification can decrease pest pressure by providing sugar to parasitoids that would otherwise be sugar-limited has its origins in anecdotal or semi-quantitative observations of increased parasitism rates and biological control in the vicinity of flowering plants.

The Soybean Aphid in China: A Historical Review

Abstract Since the discovery of the soybean aphid, Aphis glycines Matsumura, in North America in the summer of 2000, a great deal of interest has developed in the biology, ecology, and control of this insect in its native range of eastern Asia. Although there is a wealth of literature on A. glycines that could help guide the efforts of North American entomologists, much of it is written in Chinese. Here, we review the Chinese-language literature on the biology, ecology, natural enemies, and control of the soybean aphid in China.

European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America

We consider the possibility of an extensive invasional meltdown occurring in central North America involving eleven Eurasian species. The scenario begins with the potential co-facilitation between the European earthworm Lumbricus terrestris and European buckthorn, Rhamnus cathartica. Once introduced, European buckthorn has served as the overwintering host for two important invasive crop pests, oat crown rust, Puccinea coronata and the soybean aphid, Aphis glycines. The spread of R. cathartica itself may have been aided by seed dispersal by the European starling, Sturnus vulgaris, and the presence of L. terrestris has likely facilitated the invasion of Bipalium adventitium, an Asian predatory flatworm that specializes on earthworms. Beyond this, the soybean aphid is consumed by a number of introduced species, including the lady beetle Harmonia axyridis, the ground beetle Agonum muelleri and the parasitoid Aphelinus certus. We hypothesize that the presence of soybean aphid increases regional abundances of these species. We discuss both the evidence for this multi-species invasional meltdown scenario and potential implications of meltdown dynamics for invasive species management. The particular management issues that we discuss are: (1) opportunities for managing multiple invasive species simultaneously by targeting facilitator species, and (2) implications of meltdown dynamics for biological control introductions against the soybean aphid.

Multifaceted determinants of host specificity in an aphid parasitoid

The host specificity of insect parasitoids and herbivores is thought to be shaped by a suite of traits that mediate host acceptance and host suitability. We conducted laboratory experiments to identify mechanisms shaping the host specificity of the aphid parasitoid Binodoxys communis. Twenty species of aphids were exposed to B. communis females in microcosms, and detailed observations and rearing studies of 15 of these species were done to determine whether patterns of host use resulted from variation in factors such as host acceptance or variation in host suitability. Six species of aphids exposed to B. communis showed no signs of parasitism. Four of these species were not recognized as hosts and two effectively defended themselves from attack by B. communis. Other aphid species into which parasitoids laid eggs had low suitability as hosts. Parasitoid mortality occurred in the egg or early larval stages for some of these hosts but for others it occurred in late larval stages. Two hypotheses explaining low suitability were investigated in separate experiments: the presence of endosymbiotic bacteria conferring resistance to parasitoids, and aphids feeding on toxic plants. An association between resistance and endosymbiont infection was found in one species (Aphis craccivora), and evidence for the toxic plant hypothesis was found for the milkweed aphids Aphis asclepiadis and Aphis nerii. This research highlights the multifaceted nature of factors determining host specificity in parasitoids.

Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field

We used field observations of freely foraging Aphytis aonidiae parasitoids in conjunction with results of laboratory studies of A. aonidiae and other Aphytis species to simulate lifetime patterns of behavior and reproduction. Field observations provided estimates of encounter rates with three classes of hosts, the mortality rate from predation on adult parasitoids, and host‐handling times for oviposition and host feeding by adult wasps. A series of physiological parameters, including the egg maturation rate and the value of host‐feeding meals, were estimated from previously published studies. Plasticity in parasitoid behavior was incorporated in two ways. For one set of simulations we used a behavioral rule derived empirically from observations of parasitoids made in the field, and for another we used a dynamic state‐variable model to generate a set of behavioral rules that maximize lifetime reproductive success. As was expected, the empirically derived rule led to better matches with field observations than did simulations using the output of the dynamic model. Projections of lifetime reproductive success in the field ranged between three and 37 eggs within the 95% confidence intervals of the mortality rate and host encounter rate and depending on which behavioral rule was used. Lifetime reproductive success from the simulation with central estimates of the mortality and host encounter rates that incorporated the empirical rule was 6.25 eggs. Using the empirical versus the theoretical rule in the simulations led to a 10%–30% decline in projections of lifetime reproductive success, depending on mortality and host encounter rates. Regardless of the behavioral rule, the simulations underscored the observation that the host encounter rate was greater than the egg maturation rate. The overall oviposition rate was sufficiently high to lead to daily episodes of temporary egg limitation during which parasitoids must mature an egg before being able to oviposit.