BioControl (2012) 57:199–209 DOI 10.1007/s10526-011-9408-0 Population responses of hymenopteran parasitoids to the emerald ash borer (Coleoptera: Buprestidae) in recently invaded areas in north central United States Jian J. Duan • Leah S. Bauer • Kristopher J. Abell • Roy van Driesche Received: 1 July 2011 / Accepted: 17 September 2011 / Published online: 11 October 2011 Ó International Organization for Biological Control (outside the USA) 2011 Abstract Populations of hymenopteran parasitoids and 58% in 2010 (a year later after field releases). associated with larval stages of the invasive emerald ash Low levels (1–5%) of parasitism of EAB larvae by borer (EAB) Agrilus planipennis Fairmaire (Coleop- T. planipennisi were consistently detected at surveysites tera: Buprestidae) were surveyed in 2009 and 2010 in in both years. Separately, the abundance of the native the recently invaded areas in north central United States parasitoid, Atanycolus spp., increased sharply, resulting (Michigan), where two introduced EAB larval parasit- in an average parasitism rate of EAB larvae from\0.5% oids, Tetrastichus planipennisi Yang and Spathius agrili in 2009 to 19% in 2010. Other parasitoids such as Yang were released for classical biological control. Phasgonophora sulcata Westwood, Spathius spp., Bal- Results from two years of field surveys showed that cha indica Mani & Kaul, Eupelmus sp., and Eurytomus several hymenopteran parasitoids have become associ- sp. were much less abundant than T. planipennisi and ated with EAB in Michigan. Among these parasitoids, Atanycolus spp., and each caused \1% parasitism. the gregarious species T. planipennisi was the most Besides hymenopteran parasitoids, woodpeckers con- abundant, accounting for 93% of all parasitoid individ- sumed 32–42% of the immature EAB stages present uals collected in 2009 (immediately after field release) at our study sites, while undetermined biotic factors (such as microbial disease and host tree resistance) caused 10–22% mortality of observed EAB larvae. Relevance of these findings to the potential for biolog- Handling Editor: Mark Hoddle ical control of EAB in the invaded areas of North J. J. Duan (&) America is discussed. USDA ARS, Beneficial Insects Introduction Research Unit, Newark, DE 19713, USA Keywords Indigenous Á Exotics and invasive e-mail: [email protected] species Á Parasitoids Á Wood borers Á Biological control L. S. Bauer USDA Forest Service, Northern Research Station, East Lansing, MI 48823, USA Introduction K. J. Abell Department of Plant, Insect and Soil Sciences, The emerald ash borer, Agrilus planipennis Fairmaire University of Massachusetts, Amherst, MA, USA (Coleoptera: Buprestidae), native to northeast Asia, was first discovered in southeast Michigan (USA) in R. van Driesche Department of Plant, Insect and Soil Sciences, 2002 (Haack et al. 2002), and has since spread to 15 University of Massachusetts, Amherst, MA, USA U.S. states (Emerald Ash Borer Information 2011) and 123 200 J. J. Duan et al. two Canadian provinces (Canadian Food Inspection species or self-introduced exotic species of Hyme- Agency 2011). Much has been learned in the past noptera, including Atanycolus spp., Spathius florid- several years about the biology and life history of this anus Ashmead (=S. simillimus Ashmead), Spathius pest and various biotic factors that could potentially laflammei Provancher, and Leluthia astigma (Ash- affect its population dynamics in North America. In mead) (Braconidae), Phasgonophora sulcata West- most of the infested areas, EAB adults emerge in late wood (Chalcididae), Balcha indica Mani & Kaul and spring and early summer (May–June), and feed on ash Eupelmus spp. (Eupelmidae) (Bauer et al. 2004, 2005; foliage for at least two weeks before mating and Lyons 2008; Cappaert and McCullough 2009; Duan laying eggs in crevices and under bark flakes on limbs et al. 2009; Kula et al. 2010). The highest known level and trunks of ash trees in early summer (June–July). of mortality, however, is caused by woodpeckers, After eclosion, first instar larvae chew through the which attack the larger, immature stages of EAB in bark to reach the phloem, where they feed and develop North America (Cappaert et al. 2005; Lindell et al. throughout the growing season (Cappaert et al. 2005). 2008; Duan et al. 2010). Host-tree resistance and After larvae go through three molts, the mature fourth pathogenic microorganisms also influence the survival instar larvae chew pupation chambers in the outer and reproduction of EAB in both North America sapwood or bark. The mature larvae then develop a (Bauer et al. 2004; Rebek et al. 2008; Duan et al. 2010) folded appearance, which we termed J-larvae. Usually and Asia (Liu and Bauer 2006; Liu et al. 2007; Duan following a winter chill period, J-larvae develop into et al. 2011). Although the combined rate of attack prepupae, which are visibly shorter and more cylin- by these various mortality agents is inadequate to drical. Pupation generally occurs in early spring, with suppress EAB spread and ash mortality in North adults emerging from late spring through early sum- America, their potential role in regulating population mer. Adults live for several weeks feeding on mature dynamics may increase over time and needs to be ash leaves, and rarely cause any significant damage to investigated for the purpose of managing this invasive the host tree (Bauer et al. 2004). Larvae, in contrast, pest. feed for several months on ash tree phloem, creating Besides these endemic biotic factors, the recent extensive galleries under the bark. When EAB pop- classical biological control efforts against EAB in ulations are high, larval consumption of tree phloem is North America have also led to the release of one egg substantial, resulting in tree girdling and death in three parasitoid, Oobius agrili Zhang and Huang (Encyrti- to five years. dae), and two larval parasitoids, Tetrastichus plani- EAB populations in the northern United States pennisi Yang (Eulophidae) and Spathius agrili Yang (e.g., Michigan and Pennsylvania) may require (Braconidae), all of which were collected from two years to complete development, especially in northern China (Liu et al. 2003; Yang et al. 2005, newly infested, healthy ash trees (Cappaert et al. 2005; 2006; Zhang et al. 2005; Liu et al. 2007). Releases of Siegert et al. 2007; Duan et al. 2010). Similar the Chinese parasitoids started in Michigan in 2007, developmental plasticity is known for Agrilus anxius followed by Ohio and Indiana in 2008, and Maryland Gory, a native buprestid that feeds on birch trees and Illinois in 2009 and 2010 (USDA APHIS 2007; (Barter 1957). The most recent observations in Bauer et al. 2008, 2010). Although these parasitoids Michigan indicate that EAB populations have over- have apparently become established at several loca- lapping two-year generations in the field, with a mixed tions, levels of parasitism by these introduced para- population of first-season (1st to 3rd instar larvae) and sitoids at the release sites are considerably lower second-season (4th instar larvae to prepupae or pupae) (&1.5% in Duan et al. 2010) than levels (12–73%) immature stages being present in both spring and fall reported from China (Liu et al. 2003, 2007). However, (Duan et al. 2010). One implication of this condition is it is expected that prevalence of these introduced that larval stages suitable for parasitism are likely to be biological control agents and other factors will change present for nearly the entire growing season, favoring over time. Successional changes in the endemic the impact of biological control agents. Field surveys parasitoid complex attacking EAB larvae in the United in Michigan, Pennsylvania, Ohio, USA and Ontario, States and their interactions with the newly introduced Canada show that EAB larvae in newly infested areas EAB larval parasitoids from China can now be studied are parasitized by several native North American in the field. 123 Population response of parasitoids to emerald ash borer 201 For the last two years, we conducted field surveys (made frequently in small batches) of approximately to characterize the hymenopteran parasitoids associ- 3200 females (plus 1000–2000 males) of T. plani- ated with EAB larvae infesting North American ash pennisi and a single release of 200 females (plus 100 trees (primarily Fraxinus pennsylvanica Marshall) in males) of S. agrili were also made during the summer recently invaded areas of Michigan. The surveys were 2009 in the release plot at each study site. Both sexes conducted in 2009 and 2010 in three forested areas of of T. planipennisi or S. agrili were held together central Michigan, where the two newly introduced inside rearing cages for at least three days before field larval parasitoids, T. planipennisi and S. agrili, were releases, and presumably mated as both species released in 2008 and 2009. normally mate immediately upon adult wasp emer- gence (Ulyshen et al. 2010; Gould et al. 2011). Detailed procedures, timing, and number of the parasitoids Materials and methods released for each species at the three study sites are described in Duan et al. (2010). Survey sites Sampling methods Surveys were conducted in ash stands in naturally forested areas located at three sites in Ingham County, Surveys of parasitoid populations associated with near Lansing, MI, USA. The characteristics of the three EAB larvae started in the spring (25 April–12 May) of sites were described in detail in Duan et al. (2010). Site 2009 and continued into the summer (20–24 July) and 1 (42° 430N/84° 250W) was located in two contiguous fall (29 September–7 October) of 2009. In 2010, Meridian Township parks (Central Park and Nancy surveys continued in the spring (20–25 April), sum- Moore Park). Site 2 (42° 410N/84° 220W), ca. 8-km mer (July 21–25), and fall (October 19–22). At each away, spanned two additional Meridian Township survey time, we destructively sampled three to five parks (Harris Nature Center and Legg Park).