Roy G. Van Driesche

Field-cage methodology for evaluating climatic suitability for introduced wood-borer parasitoids: Preliminary results from the emerald ash borer system

Abstract Field-cage methods were developed to evaluate the abilities of Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius agrili Yang (Hymenoptera: Braconidae), biocontrol agents of Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), to parasitize, develop and overwinter following three late-season releases at both a northern (Michigan) and a southern (Maryland) location within the current North American range of A. planipennis. In August, September and October of 2009, five young green ash trees were selected at each location. Tetrastichus planipennisi and S. agrili were each randomly assigned to one of two cages attached to each tree, surrounding separate sections of trunk in which late-instar A. planipennis had been inserted. The following April, the caged trunk sections were dissected to determine the fate of each A. planipennis larva and the developmental stages of all recovered parasitoid progeny. At both locations, T. planipennisi and S. agrili were able to parasitize hosts and successfully overwinter (i.e., reach adulthood the following spring). For T. planipennisi, successful parasitism (i.e., parasitoid progeny reached adulthood) occurred for all caged releases in Maryland, but only for the August and September releases in Michigan. At both locations, percent parasitism by T. planipennisi was higher in August and September than in October. For S. agrili, successful parasitism occurred for all caged releases in Maryland, but only for the August release in Michigan. In Maryland, percent parasitism by S. agrili in August and September was higher than in October. The caging method described here should be useful in determining the climatic suitability of other regions before proceeding with large-scale releases of either species and may have utility in other wood-borer parasitoid systems as well.

Should arthropod parasitoids and predators be subject to host range testing when used as biological control agents

Testing of candidate biological control agents to estimate their likely field host ranges in the area of release has been part of weed biological control for several decades, with evolving techniques and goals. Similar efforts have been made less often for parasitoids and predators being introduced for arthropod biological control. Here, we review both techniques of host range testing and social objectives of such screening. We ask whether agents introduced for arthropod biological control should be subjected to host range testing before release, and if so, are methods used for estimating host ranges of herbivorous arthropods appropriate, or are different approaches needed. Current examples in which host range testing has been employed for arthropod biological control are reviewed. We conclude with recommendations concerning guiding principles about use of host range testing. We recommend modest expansion of host range testing for arthropod biological control for projects on continents. We recommend more extensive testing for projects of introduction onto islands. We note that introductions to islands could provide opportunities to gain experience in use of host range estimation for this class of organisms and to conduct post release evaluations of host ranges. We urge caution in efforts to mandate host range testing but simultaneously recommend consultation between biological control workers and insect conservationists.

Threats posed to rare or endangered insects by invasions of nonnative species.

Endangerment factors are reviewed for 57 U.S. federally listed insects and 116 rare eastern North American lepidopterans to determine the importance of invasive species relative to 15 other recognized endangerment factors. Invasive plants, social insects (especially ants), and vertebrate grazers and predators repeatedly were identified as groups directly or indirectly threatening native insect biodiversity. Among rare eastern North American lepidopterans, the (mostly indirect) consequences of the establishment of the gypsy moth (Lymantria dispar) surfaced as a general threat. Remote islands, especially those with high human visitation, stand out as being highly threatened by invasives. In the worst cases, impacts from invasive species cascade through a community and destabilize existing trophic interconnections and alter basic ecosystem properties, changing hydrology, nutrient cycles, soil chemistry, fire susceptibility, and light availability, and precipitate myriad other changes in biotic and abiotic parameters. Invasive ants and herbivorous insects provide some of the most dramatic examples of such insect-induced invasional cascades.

Establishment and Abundance of Tetrastichus planipennisi (Hymenoptera: Eulophidae) in Michigan: Potential for Success in Classical Biocontrol of the Invasive Emerald Ash Borer (Coleoptera: Buprestidae)

ABSTRACT Tetrastichus planipennisi Yang is a gregarious larval endoparasitoid native to China and has been introduced to the United States since 2007 for classical biological control of the invasive emerald ash borer, Agrilus planipennis Fairmaire, an exotic beetle responsible for widespread ash mortality. Between 2007–2010, T. planipennisi adults (3,311–4,597 females and ≈1,500 males per site) were released into each of six forest sites in three counties (Ingham, Gratiot, and Shiawassee) of southern Michigan. By the fall of 2012, the proportion of sampled trees with one or more broods of T. planipennisi increased to 92 and 83% in the parasitoid-release and control plots, respectively, from 33 and 4% in the first year after parasitoid releases (2009 fall for Ingham county sites and 2010 for other sites). Similarly, the mean number of T. planipennisi broods observed from sampled trees increased from less than one brood per tree in the first year after parasitoid releases to 2.46 (at control plots) to 3.08 (at release plots) broods by the fall of 2012. The rates of emerald ash borer larval parasitism by T. planipennisi also increased from 1.2% in the first year after parasitoid releases to 21.2% in the parasitoid-release plots, and from 0.2 to 12.8% for the control plots by the fall of 2012. These results demonstrate that T. planipennisi is established in southern Michigan and that its populations are increasing and expanding. This suggests that T. planipennisi will likely play a critical role in suppressing emerald ash borer populations in Michigan.

Population dynamics of an invasive forest insect and associated natural enemies in the aftermath of invasion: implications for biological control

Summary 1. Understanding the population dynamics of exotic pests and associated natural enemies is important in developing sound management strategies in invaded forest ecosystems. The emerald ash borer (EAB) Agrilus planipennis Fairmaire is an invasive phloem-feeding beetle that has killed tens of millions of ash Fraxinus trees in North America since first detected in 2002. 2. We evaluated populations of immature EAB life stages and associated natural enemies over a 7-year period (2008–2014) in six stands of eastern deciduous forest in southern Michigan, where Tetrastichus planipennisi Yang and two other Asian-origin EAB parasitoids were released for biological control between 2007 and 2010. 3. We observed 90% decline in densities of live EAB larvae in infested ash trees at both parasitoid-release and control plots from 2009 to 2014 and found no significant differences in EAB density or mortality rates by parasitoids, avian predators or other undetermined factors between parasitoid-release and control plots. The decline in EAB larval density in our study sites was correlated with significant increases in EAB larval parasitism, first by native parasitoids, then by T. planipennisi. 4. Life table analyses further indicated that parasitism by the introduced biocontrol agent and the North American native parasitoids contributed significantly to the reduction of net EAB population growth rates in our study sites from 2010 to 2014. 5. Synthesis and applications. Our findings indicate that successful biocontrol of emerald ash borer (EAB) may involve suppression of EAB abundance both by local, generalist natural enemies (such as Atanycolus spp.) and by introduced specialist parasitoids (such as T. planipennisi). Biological control programmes against EAB in the aftermath of invasion should focus on establishing stable populations of T. planipennisi and other introduced specialist parasitoids for sustained suppression of low-density EAB populations. Moreover, we recommend releasing the introduced specialist biocontrol agents as soon as possible to prevent the outbreak of EAB populations in both newly infested and aftermath forests when EAB densities are still low.

Natural enemies implicated in the regulation of an invasive pest: a life table analysis of the population dynamics of the emerald ash borer

The emerald ash borer Agrilus planipennis Fairmaire is a serious invasive forest pest of ash (Fraxinus) trees in North America. Life tables were constructed for both experimentally established cohorts and wild populations of A. planipennis on healthy host trees from 2008 to 2011 in six forests in central Michigan. Life table analysis showed that the net population growth rates (R0) for the experimental cohorts (16.0 ± 2.9) and associated wild A. planipennis (19.4 ± 1.9) were the highest for the first study period (2008–2009) at three Ingham Co. sites but decreased to 4.7 ± 0.9 and 4.6 ± 0.4, respectively, for the second (2009–2010) study period at the same sites. By contrast, R0 values of both experimental cohorts (5.7 ± 2.2) and associated wild A. planipennis populations (11.3 ± 2.5) were intermediate in the third (2010–2011) study period at different sites in the Gratiot and Shiawassee Cos. The sudden decrease in R0 of both experimental and wild A. planipennis cohorts in the Ingham Co. sites corresponded with increases in parasitism by hymenopteran parasitoids Atanycolus spp. (native) and Tetrastichus planipennisi Yang (introduced), as well as an increase in woodpecker predation, indicating the role of these natural enemies in regulation of the pests population dynamics.

Insect-Resistant Transgenic Crops and Biological Control

Natural enemies such as predators and parasitoids fulfil an important ecological and economic function by helping to keep herbivore populations below the economic injury level. Thus, they contribute to sustainable integrated pest management (IPM) systems. It is well established that plant resistance factors that affect herbivores also interact with natural enemies and consequently with the biological control function they provide. Similarly, host plant resistance derived from genetic engineering will have an impact on biological control. There is evidence today that the currently available transgenic crops that express Cry proteins derived from Bacillus thuringiensis (Bt) have no direct effects on natural enemies due to their narrow spectrum of activity. However, the fact that the target pests are efficiently controlled by the deployed Bt crops has inevitable consequences for natural enemies that specialize on these species as hosts or prey. On the other hand, it has become clear that in crop systems where the deployment of Bt varieties has lead to a decline in insecticide use, biological control organisms have benefited significantly. Consequently, this technology can contribute to natural enemy conservation and thus be a useful tool in IPM.

Discovery and utilization of Bemisia argentifolii patches by Eretmocerus eremicus and Encarsia formosa (Beltsville strain) in greenhouses

The ability of two species of aphelinid parasitoids to find and attack Bemisia argentifolii was determined. Experiments were conducted with whitefly patches on single leaf poinsettia plants randomly distributed in canopies of four commercially grown poinsettia crops at an early and late stage of plant growth. Eretmocerus eremicus found experimental patches in canopies of small and large plants more quickly and frequently, and killed more nymphs following patch discovery than Encarsia formosa (Beltsville strain). E. eremicus exhibited a Type I functional response in small and large canopies while E. formosa (Beltsville strain) showed a Type II functional response in small canopies and a weak linear response in large canopies. In greenhouses treated with E. eremicus, canopy size increased 4.6× and nymphs per plant increased 14.2× between small and large canopy experiments. Consequently, area of search for this parasitoid increased 83%, number of wasps counted on patches decreased 74%, and proportion of nymphs killed in artificial patches decreased 47% between small and large canopies. In greenhouses treated with E. formosa Beltsville strain, canopy size increased 7.3× and nymphs per plant increased 25.4× between small and large canopy experiments. Consequently for E. formosa Beltsville strain, area of search increased 11%, number of wasps counted on patches decreased 86%, and proportion of nymphs killed in artificial patches decreased 47% between small and large canopies.

Evaluation of Encarsia formosa (Hymenoptera: Aphelinidae) to Control Bemisia argentifolii (Homoptera: Aleyrodidae) on Poinsettia (Euphorbia Pulcherrima):a Lifetable Analysis

Weekly releases of the parasitoid Encarsia formosa Gahan failed to control a low density population (initially, 0.51 nymphs and pupae per plant) of the whitefly Bemisia argentifolii Bellows & Perring on greenhouse grown poinsettia plants in Massachusetts when released at the rate of 4-7 adult females per plant. A lifetable constructed for uncaged B. argentifolii in the presence of E. formosa indicated that survivorship from the first/second instar to adult emergence was 14%. In contrast, in a lifetable constructed for B. argentifolii on caged poinsettia from which E. formosa was excluded, survivorship was 67%. Release of E. formosa reduced the number of insecticide applications on poinsettia by 75%, but the cost of using E. formosa (on a per m2 basis) was 9.5 times that of insecticides alone.

Assessment of risk posed by introduced braconid wasps to Pieris virginiensis, a native woodland butterfly in New England

Abstract The range of the native butterfly Pieris virginiensis Edwards has decreased in New York and Ontario since the 1940s. Loss of habitat and harm from Cotesia glomerata (L.), a braconid parasitoid introduced to North America in the late nineteenth century for biological control of the invasive pest butterfly Pieris rapae (L.), have been suggested as the causes of this decline. In western Massachusetts, extensive habitat suitable for P. virginiensis remains and its principal host plant, Cardamine diphylla, is common. We found P. virginiensis to be widely present, occurring at 39% of host plant patches. In laboratory tests, we found that both C. glomerata and Cotesia rubecula (Marshall) are able to parasitize and successfully develop in P. virginiensis larvae when these are presented on detached leaves of C. diphylla. However, when we exposed laboratory-reared first or second instars of either P. rapae or P. napi (both suitable hosts for these Cotesia spp.) as sentinel larvae on leaves of either Brassica oleracea or C. diphylla at sites where P. virginiensis was present, no parasitism by either Cotesia sp. was detected. Some sentinel larvae were parasitized by an unidentified ichneumonid in the genus Hyposoter. We conclude that in western Massachusetts, P. virginiensis is widely distributed at low densities and that while it is physiologically an acceptable and suitable host for both C. glomerata and C. rubecula, larvae of field populations of this butterfly are not attacked because these parasitoids do not forage in forested habitats, even when they are locally present in adjacent meadows. Consequently, we report that this butterfly is not threatened by these parasitoids contrary to early suggestions in the literature.