Keith R. Hopper

Mate finding, dispersal, number released, and the success of biological control introductions

Abstract. 1 An analysis of published data and a mathematical model of the population dynamics of introduced parasitoids were used to explore the possibility that biological control introductions fail because an Allee effect drives small, introduced populations extinct. Such an Allee effect would arise because low densities, resulting from dispersal into a new environment, lead to failure to mate, which leads to a male‐biased sex ratio, which, if extreme enough, could cause population extinction. 2 For chalcidoids, ichneumonoids and tachinids, the proportion of parasitoid populations that established when introduced for control of lepidopteran pests increased with the number of parasitoids per release, the total number released, and the number collected when each variable was analysed separately. For chalcidoids alone, establishment increased with the number of releases for this variable analysed separately. However, stepwise logistic regression of establishment on these variables included only the total number released for chalcidoids and the number per release for ichneumonoids and tachinids. This suggests that an Allee effect may limit the establishment of introduced parasitoids more than stochastic environmental variation or lack of genetic variation. 3 A reaction‐diffusion model of parasitoid introductions was developed, which included mate finding, dispersal, reproduction and survival. Sensitivity analysis showed that the critical number of females needed to establish a population decreased hyperbolically as mate detection distance and net reproductive rate were increased, but the critical number increased linearly as mean‐square displacement was increased. The critical number of females did not change when the gross distance traversed per generation was varied. This was because increased area searched by males compensated for increased displacement. Changing from virgin females producing all males (arrhenotoky) to virgin females producing no progeny increased the critical number of females by over 30%. 4 The analysis of past introductions and the sensitivity analysis of the reaction‐diffusion model both suggested a threshold of about 1000 insects per release to ensure establishment of introduced parasitoids. The implications of our results for the design of biological control introductions are discussed. Limitations in retrospective analyses and current knowledge indicate the need for an experimental approach to introductions.

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.

Prospects for Importation Biological Control of the Soybean Aphid: Anticipating Potential Costs and Benefits

Abstract We discuss the potential pros and cons of using importation biological control against the soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae). Importation of exotic organisms for biological control is never completely risk-free, but the potential negative impacts of not achieving biological control of invasive pests may exceed the risks associated with a biological control introduction. The potential benefits of biological control include reduced insecticide use and a reduced ability of the invasive pest to impact native flora and fauna, and we outline what the scope of these benefits may be for the soybean aphid. The benefits are only accrued, however, if biological control is successful, so the likelihood of successful biological must also be assessed. Accordingly, we outline some issues relevant to predicting the success of importation biological control of the soybean aphid. We also outline the potential risks to nontarget organisms that would be associated with importation biological control of the soybean aphid. Currently, two parasitoid species, Aphelinus albipodus Hayat and Fatima (Hymenoptera: Aphelinidae) and Lipolexis gracilis Förster (Hymenoptera: Braconidae) have been imported from Asia and have passed through quarantine. We briefly review the biology and host range of these two species. A different strain of A. albipodus that was released against the Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), in the early 1990s was also found to attack the soybean aphid in the laboratory and has been redistributed from Wyoming to Minnesota and Wisconsin in field releases against the soybean aphid. We discuss our rationale for going forward with this redistribution.

Population Dynamics of Aphis glycines (Homoptera: Aphididae) and Its Natural Enemies in Soybean in Northern China

Abstract A field survey of soybean aphid, Aphis glycines Matsumura, and its natural enemies was conducted during summer 2002 in Langfang, northern China (116.4° E, 39.3° N). Aphids colonized soybean when plants were still small in early July. After a lag of 2 wk, aphid density increased rapidly in late July, reaching a peak of 114 ± 46 aphids per five soybean plants on 1 August. The population declined to a plateau immediately after this peak and then declined again starting in mid-August, although a second small peak occurred in late August. The finite rate of increase varied from zero- to five-fold, and the aphid seemed to be limited by natural enemies. The main species of natural enemy were the aphid parasitoid Lysiphlebus sp., the aphid predators Propylaea japonica (Thunberg), Scymnus (Neopullus) babai Sasaji, and Paragus tibialis (Fallén). In a field exclosure experiment, A. glycines density in small-mesh cages peaked three-fold higher than in large-mesh cages and 12-fold higher than on uncaged plants, indicating that natural enemies did indeed limit aphid density.

Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance.

The Asian parasitoid, Binodoxys communis (Gahan) (Hymenoptera: Braconidae), is a candidate for release against the exotic soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in North America. In this study, we examined preferences by B. communis for the different developmental stages of A. glycines and investigated consequences of these preferences for parasitoid fitness. We also determined to what extent aphid defensive behaviours mediate such preferences. We found that B. communis readily attacks and successfully develops in the different A. glycines developmental stages. Binodoxys communis development time gradually increased with aphid developmental stage, and wasps took longest to develop in alates. An average (+/-SE) of 54.01+/-0.08% of parasitized A. glycines alatoid nymphs transformed into winged adult aphids prior to mummification. No-choice assays showed a higher proportion of successful attacks for immature apterous A. glycines nymphs compared to adults and alatoid nymphs. Also, choice trials indicated avoidance and lower attack and oviposition of adults and alatoid nymphs. The different aphid stages exhibited a range of defensive behaviours, including body raising, kicking and body rotation. These defenses were employed most effectively by larger aphids. We discuss implications for the potential establishment, spread and biological control efficacy of A. glycines by B. communis in the event that it is released in North America.

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.

French wasps in the New World: experimental biological control introductions reveal a demographic Allee effect

Many populations introduced into a novel environment fail to establish. One underlying process is the Allee effect, i.e., the difficulty of individuals to survive and reproduce when rare, and the consequently low or negative population growth. Although observations showing a positive relation between initial population size and establishment probability suggest that the Allee effect could be widespread in biological invasions, experimental tests are scarce. Here, we used a biological control program against Diuraphis noxia (Mordvilko) (Hemiptera: Aphididae) in the United States to manipulate initial population size of the introduced parasitoid Aphelinus asychis Walker (Hymenoptera: Aphelinidae) originating from France. For eight populations and three generations after introduction, we studied spatial distribution and spread, density, mate-finding, and population growth. Dispersal was lower in small populations during the first generation. Smaller initial population size nonetheless resulted in lower density during the three generations studied. The proportion of mated females and the population sex ratio were not affected by initial population size or population density. Net reproductive rate decreased with density within each generation, suggesting negative density-dependence. But for a given density, net reproductive rate was smaller in populations initiated with few individuals than in populations initiated with many individuals. Hence, our results demonstrate a demographic Allee effect. Mate-finding is excluded as an underlying mechanism, and other component Allee effects may have been overwhelmed by negative density-dependence in reproduction. Impact of generalist predators could provide one potential explanation for the relationship between initial population size and net reproductive rate. However, the continuing effect of initial population size on population growth suggests genetic processes may have been involved in the observed demographic Allee effect.

Population Dynamics of Aphis glycines (Homoptera: Aphididae) and Impact of Natural Enemies in Northern China

Abstract Field surveys of soybean aphid, Aphis glycines Matsumura, and its natural enemies, as well as natural enemy exclosure experiments, were conducted during 2003 and 2004 in soybean fields near Langfang, China. In 2003, aphid density increased six-fold during 12 d in July from 66 ± 12 per 10 plants to a seasonal peak of 401 ± 79 per 10 plants. Aphid density remained high for another 10 d and declined during late July and early August. In 2004, aphid density increased 29-fold during 13 d in July from 14 ± 2 per 10 plants to a seasonal peak of 375 ± 30 per 10 plants. Unlike 2003, aphid density remained relatively high during late July and August, peaking again at 296 ± 31 per 10 plants on 24 August. In both years, aphid density remained below economic injury level and seemed to be limited by natural enemies. Exclosure of natural enemies led to increases in A. glycines density in 2003 and 2004. In 2003, peak aphid densities in large- and medium-mesh cages were three- and seven-fold higher, respectively, than densities on uncaged plants. In 2004, peak aphid densities in large- and medium-mesh cages were 2-fold and 30-fold higher, respectively, than densities on uncaged plants in one experiment. In another experiment, peak aphid densities in large-, medium-, and small-mesh cages were 8-fold, 28-fold, and 68-fold higher, respectively, than densities on uncaged plants. Both predators and parasitoids were important in limiting aphid density. We compare our results with those from North America and discuss implications for biological control.

Oviposition vs. offspring fitness in Aphidius colemani parasitizing different aphid species

We measured the acceptance and suitability of four aphid species [Aphis gossypii Glover, Myzus persicae (Sulzer), Rhopalosiphum padi (L.), and Schizaphis graminum (Rondani)] (Homoptera: Aphididae) for the parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Female parasitoids parasitized fewer R. padi than the other three aphid species, and fewer offspring successfully completed development in R. padi than in the other three host species. Sex ratios of emerging adults were more male‐biased from R. padi than from the other three aphid species, suggesting that R. padi is a poor quality host for this population of A. colemani. Ovipositing A. colemani encountered R. padi at a slower rate, spent more time handling R. padi, and parasitoid offspring died at a higher rate in R. padi compared to A. gossypii. Our results show that oviposition behavior and offspring performance are correlated. In each experiment, we tested the effect of the host species in which the parasitoids developed (parental host) on the number of hosts attacked, the proportion of each host species accepted for oviposition and the survival of progeny. Parental host affected maternal body size and, through its effect on body size, the rate of encounter with hosts. Other than this, parental host species did not affect parasitism.