Mark K. Asplen

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.

Almost There: Transmission Routes of Bacterial Symbionts between Trophic Levels

Many intracellular microbial symbionts of arthropods are strictly vertically transmitted and manipulate their hosts reproduction in ways that enhance their own transmission. Rare horizontal transmission events are nonetheless necessary for symbiont spread to novel host lineages. Horizontal transmission has been mostly inferred from phylogenetic studies but the mechanisms of spread are still largely a mystery. Here, we investigated transmission of two distantly related bacterial symbionts – Rickettsia and Hamiltonella – from their host, the sweet potato whitefly, Bemisia tabaci, to three species of whitefly parasitoids: Eretmocerus emiratus, Eretmocerus eremicus and Encarsia pergandiella. We also examined the potential for vertical transmission of these whitefly symbionts between parasitoid generations. Using florescence in situ hybridization (FISH) and transmission electron microscopy we found that Rickettsia invades Eretmocerus larvae during development in a Rickettsia-infected host, persists in adults and in females, reaches the ovaries. However, Rickettsia does not appear to penetrate the oocytes, but instead is localized in the follicular epithelial cells only. Consequently, Rickettsia is not vertically transmitted in Eretmocerus wasps, a result supported by diagnostic polymerase chain reaction (PCR). In contrast, Rickettsia proved to be merely transient in the digestive tract of Encarsia and was excreted with the meconia before wasp pupation. Adults of all three parasitoid species frequently acquired Rickettsia via contact with infected whiteflies, most likely by feeding on the host hemolymph (host feeding), but the rate of infection declined sharply within a few days of wasps being removed from infected whiteflies. In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding. This study demonstrates potential routes and barriers to horizontal transmission of symbionts across trophic levels. The possible mechanisms that lead to the differences in transmission of species of symbionts among species of hosts are discussed.

A 'Goldilocks' hypothesis for dispersal of biological control agents

The rate at which biological control agents disperse from release sites has important implications for their establishment and spread. Low rates of dispersal can yield spread that is too slow and may necessitate redistribution efforts for importation biological control and a high density of release sites for augmentation. Low dispersal rates may also lead to inbreeding at the site of release. On the other hand, high rates of dispersal can lead to Allee effects at the leading edge of the invasion front, potentially reducing the likelihood of establishment. Given these disadvantages associated with both low and high dispersal rates, we argue that intermediate rates of dispersal are likely to maximize the probability of establishment and appropriate spread for biological control agents released in the context of either importation or augmentative biological control. We consider this putative relationship a ‘Goldilocks hypothesis’ since it posits an optimum at intermediate values. In this review paper we begin by discussing the rationale for the Goldilocks hypothesis and then provide a case study from our work on importation biological control of the soybean aphid, Aphis glycines. Work on the soybean aphid parasitoid Binodoxys communis has shown that long-distance dispersal of immature parasitoids within winged migrating aphids is unlikely. This is likely good news for importation biological control because parasitoids dispersed in this manner would likely encounter crippling Allee effects. On the other hand, results from a field release study also suggest that female B. communis females (but not males) disperse actively from release sites. This female-biased dispersal may lead to strong mate-finding Allee effects and therefore may make establishment less likely.

Multistate Comparison of Attractants for Monitoring Drosophila suzukii (Diptera: Drosophilidae) in Blueberries and Caneberries

ABSTRACT Drosophila suzukii Matsumara, also referred to as the spotted wing drosophila, has recently expanded its global range with significant consequences for its primary host crops: blueberries, blackberries, raspberries, cherries, and strawberries. D. suzukii populations can increase quickly, and their infestation is difficult to predict and prevent. The development of effective tools to detect D. suzukii presence in new areas, to time the beginning of activity within a crop, to track seasonal activity patterns, and to gauge the effectiveness of management efforts has been a key research goal. We compared the efficiency, selectivity, and relationship to fruit infestation of a range of commonly used homemade baits and a synthetic formulated lure across a wide range of environments in 10 locations throughout the United States. Several homemade baits were more efficient than apple cider vinegar, a commonly used standard, and a commercially formulated lure was, in some configurations and environments, comparable with the most effective homemade attractant as well as potentially more selective. All alternative attractants also captured flies between 1 and 2 wk earlier than apple cider vinegar, and detected the presence of D. suzukii prior to the development of fruit infestation. Over half the Drosophila spp. flies captured in traps baited with any of the attractants were not D. suzukii, which may complicate their adoption by nonexpert users. The alternative D. suzukii attractants tested are improvement on apple cider vinegar and may be useful in the development of future synthetic lures.

Specialisation of bacterial endosymbionts that protect aphids from parasitoids

1. Infection by the bacterial endosymbiont Hamiltonella defensa is capable of protecting the pea aphid from parasitism by Aphidius ervi and the black bean aphid from parasitism by Lysiphlebus fabarum. Here we investigate protection of a third aphid species, the cowpea aphid, Aphis craccivora, from four parasitoid species: Binodoxys communis, B. koreanus, Lysiphlebus orientalis, and Aphidius colemani.

Cold Hardiness of Winter-Acclimated Drosophila suzukii (Diptera: Drosophilidae) Adults

ABSTRACT Drosophila suzukii Matsumura, often called spotted wing drosophila, is an exotic vinegar fly that is native to Southeast Asia and was first detected in the continental United States in 2008. Previous modeling studies have suggested that D. suzukii might not survive in portions of the northern United States or southern Canada due to the effects of cold. As a result, we measured two aspects of insect cold tolerance, the supercooling point and lower lethal temperature, for D. suzukii summer-morph pupae and adults and winter-morph adults. Supercooling points were compared to adults of Drosophila melanogaster Meigen. The lower lethal temperature of D. suzukii winter-morph adults was significantly colder than that for D. suzukii summer-morph adults, while supercooling points of D. suzukii winter-morph adults were actually warmer than that for D. suzukii summer-morph adults and pupae. D. suzukii summer-morph adult supercooling points were not significantly different than those for D. melanogaster adults. These measures indicate that D. suzukii is a chill intolerant insect, and winter-morph adults are the most cold-tolerant life stage. These results can be used to improve predictions of where D. suzukii might be able to establish overwintering populations and cause extensive damage to spring fruit crops.

Factors limiting the spread of the protective symbiont Hamiltonella defensa in Aphis craccivora aphids

ABSTRACT Many insects are associated with heritable symbionts that mediate ecological interactions, including host protection against natural enemies. The cowpea aphid, Aphis craccivora, is a polyphagous pest that harbors Hamiltonella defensa, which defends against parasitic wasps. Despite this protective benefit, this symbiont occurs only at intermediate frequencies in field populations. To identify factors constraining H. defensa invasion in Ap. craccivora, we estimated symbiont transmission rates, performed fitness assays, and measured infection dynamics in population cages to evaluate effects of infection. Similar to results with the pea aphid, Acyrthosiphon pisum, we found no consistent costs to infection using component fitness assays, but we did identify clear costs to infection in population cages when no enemies were present. Maternal transmission rates of H. defensa in Ap. craccivora were high (ca. 99%) but not perfect. Transmission failures and infection costs likely limit the spread of protective H. defensa in Ap. craccivora. We also characterized several parameters of H. defensa infection potentially relevant to the protective phenotype. We confirmed the presence of H. defensa in aphid hemolymph, where it potentially interacts with endoparasites, and performed real-time quantitative PCR (qPCR) to estimate symbiont and phage abundance during aphid development. We also examined strain variation of H. defensa and its bacteriophage at multiple loci, and despite our lines being collected in different regions of North America, they were infected with a nearly identical strains of H. defensa and APSE4 phage. The limited strain diversity observed for these defensive elements may result in relatively static protection profile for this defensive symbiosis.

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.

Parasitism of Autumnal Morphs of the Soybean Aphid (Hemiptera: Aphididae) by Binodoxys communis (Hymenoptera: Braconidae) on Buckthorn

ABSTRACT The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is both heteroecious and holocyclic, seasonally alternating between buckthorn (Rhamnus spp.), (the primary, overwintering host) and soybean, Glycine max (L.) Merr. (the secondary host). Recently, a classical biological control program for this invasive pest has been implemented in North America using the Asian aphidiine braconid wasp Binodoxys communis Gahan. Two critical, related questions regarding the overwintering biology of B. communis are 1) does the parasitoid maintain fidelity to A. glycines throughout the aphid life cycle and follow it to its primary host; and, if it does, 2) is parasitoid migration facilitated by phoretic movement within buckthorn-specific winged aphids? In the laboratory, we compared B. communis parasitism on several different autumnal morphs of A. glycines: winged gynoparae (fall migrants) and their oviparous offspring on buckthorn, fourth-instar alatoid nymphs that would form either gynoparae or summer migrants on soybean, and third-instar gynoparous alatoid nymphs on soybean. We also introduced gynoparae and B. communis onto caged buckthorn plants in southeastern Minnesota to examine autumnal parasitism under natural conditions. In both the laboratory and field, parasitism rates of oviparae were much higher than those of gynoparae. In addition, B. communis rarely completed development on fourth-instar alatoid nymphs. Although wasps successfully developed on third-instar gynoparous nymphs, these hosts mummified before forming wings. These results suggest that although at least one buckthorn-specific morph of A. glycines seems suitable for B. communis parasitism, it is unlikely that alate-mediated dispersal of immature parasitoids is an adaptive strategy to locate Rhamnus in this species.

Sex-specific dispersal by a parasitoid wasp in the field

Although parasitoid wasps are important regulators of herbivorous insect populations, very little is known regarding their movement under field conditions. Here, we examined the vertical and cardinal directionality of dispersal by Binodoxys communis (Gahan) (Hymenoptera: Braconidae: Aphidiinae), an exotic Asian parasitoid released as a biological control agent of the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae: Aphidinae), in North American soybeans, Glycine max (L.) Merr. (Fabaceae). The patterns are consistent with time‐dependent, sex‐specific dispersal strategies; whereas males show flight that is devoid of vertical or cardinal directionality, females consistently move at or above soybean canopy height toward the east and north. Male capture rates also appear to be more correlated with local conditions than those of females. These results suggest that females actively cross the flight boundary layer (the space above which insect flight is largely wind‐driven as opposed to self‐directed) and follow air currents away from soybean fields, whereas males engage in more localized movement. The data also suggest differing response potentials of the sexes to changing local resource conditions (host availability, female availability, host plant cultivar). We discuss the implications for sex‐specific movement on the basic biology of introduced parasitoid species, and their applied role as potential agents in importation biological control programs.