J Pest Sci (2017) 90:1169–1179 DOI 10.1007/s10340-017-0892-6 ORIGINAL PAPER Pentatomid host suitability and the discovery of introduced populations of Trissolcus japonicus in Oregon 1 2 3 Christopher Hedstrom • David Lowenstein • Heather Andrews • 1 2 Barry Bai • Nik Wiman Received: 31 January 2017 / Revised: 30 May 2017 / Accepted: 1 June 2017 / Published online: 17 June 2017 Ó Springer-Verlag GmbH Germany 2017 Abstract Trissolcus japonicus is an egg parasitoid of acceptance patterns were similar between stink bug spe- Halyomorpha halys, brown marmorated stink bug, a severe cies, our results suggest a greater potential for parasitoid agricultural pest in the USA. T. japonicus is being evalu- development in H. halys eggs compared to the native ated in quarantine as a classical biological control agent to pentatomids. During host-range testing, we detected field manage H. halys populations in the USA. To determine T. populations of T. japonicus at 11 sites in Portland, OR, japonicus’ potential for successful management of the pest, indicating an unintentional introduction and establishment. we performed a series of no-choice and paired-host-range Further work is needed to characterize its nontarget activity tests, evaluating parasitism and host recognition in ten and dispersal patterns in areas where H. halys causes nontarget insects. In laboratory no-choice tests, T. japoni- economic damage in Oregon. cus successfully parasitized egg masses of seven Pentato- midae native to Oregon in addition to H. halys. Mean Keywords Biological control Á Stink bug Á Parasitoid Á parasitism proportions of egg masses were greater than Halyomorpha halys Á Trissolcus japonicus 40% in two species, B. dimidiata and H. abbreviatus, and were statistically similar to parasitism of H. halys. How- ever, paired-host tests identified higher proportions of Key message parasitized H. halys egg masses compared to four other pentatomids. T. japonicus was equally attracted to volatiles • The host range of Trissolcus japonicus, a potential produced by H. halys and other pentatomids but demon- classical biological control agent for Halyomorpha strated significantly longer arrestment response time on halys, was evaluated. surfaces with H. halys contact kairomones. Although host • Trissolcus japonicus, parasitizes the eggs of multiple pentatomid species, but more frequently parasitizes H. halys compared to other stink bug hosts and is attracted Communicated by T. Haye. to volatiles produced by H. halys. • These findings aid in prediction of the wasp’s success Special Issue: The brown marmorated stink bug Halyomorpha halys an emerging pest of global concern. as a biocontrol agent. • Trissolcus japonicus was detected in Portland, OR in & Christopher Hedstrom 2016, indicating an adventive introduction and estab- [email protected] lishment in Oregon. 1 Oregon Department of Agriculture, 635 Capitol St. NE, Salem, OR 97301, USA Introduction 2 Department of Horticulture, Oregon State University, 4017 Agriculture and Life Sciences, Corvallis, OR 97331, USA Halyomorpha halys (Sta˚l), brown marmorated stink bug 3 Oregon State University North Willamette Research and Experiment Center, 15210 NE Miley Road, Aurora, (Hemiptera: Pentatomidae), is an invasive insect pest in the OR 97002, USA USA. Polyphagous feeding by H. halys has made it an 123 1170 J Pest Sci (2017) 90:1169–1179 economically important pest in vegetable, fruit, and nurs- exotic organisms for biological control (Howarth 1991; ery crops (Leskey et al. 2012a, b; Wiman et al. 2014) Fruit Louda et al. 2003). Host-range testing in quarantine is the crops in the Mid-Atlantic states closest to the initial out- first step for evaluation prior to the intentional release of a break have experienced severe economic damage (Leskey potential biological control agent to predict nontarget hosts et al. 2012a, b). Since its initial detection, H. halys has been (Bellows and Fisher 1999; Babendreier et al. 2005). detected in 43 states and is an agricultural pest in 19 of Penatomidae, which includes H. halys, is represented by them (NEIPM 2017). In the Pacific Northwest, H. halys has more than 50 species in the Oregon State Arthropod Col- become a pest of hazelnuts, peaches, and other specialty lection (Oregon State University, Corvallis, OR) (Hed- crops (Wiman et al. 2014). H. halys poses unique man- strom 2016). None of the species are known to be rare or agement challenges due to its presence throughout the endangered, although many are poorly understood in terms growing season and feeding patterns on ornamental and of phenology, host plant preferences, and other aspects of agricultural plants (Leskey et al. 2012a, b). Several insec- their biology. Most species are phytophagous, and several ticides that are effective at reducing H. halys populations species such as Euschistus conspersus Uhler, Chlorocroa may provide short-term control (Nielsen et al. 2008). ligata (Say), and Thyanta custator Fabricius are occasional However, insecticides registered for H. halys have broad- pests in agriculture. Several Oregon pentatomids, including spectrum activity and adversely affect beneficial insects Zicrona caerulea (L.), Podisus brevispinus Phillips,P. (Roubos et al. 2014), antagonizing integrated pest man- maculiventris (Say), and Perillus bioculatus (Fabricius), agement (IPM) programs. are predatory. Clearly, these predators are the most con- Alternative management strategies for H. halys that are cerning for possible nontarget effects of T. japonicus. less disruptive to IPM programs are being investigated. For egg parasitoids such as T. japonicus, the potential for Targeted pesticide applications that incorporate H. halys nontarget effects can be evaluated through semiochemical behavior, such as those limited to field perimeters in peach recognition and parasitism of host material. Parasitoid-host cropping systems, have reduced crop injury (Blaauw et al. selection involves several steps that include identifying 2015). In addition to insecticides, cultural controls, such as suitable habitat, as well as locating and recognizing hosts physical exclusion (Dobson et al. 2016) and trap crops prior to oviposition (Vinson 1984). In the searching phase (Nielsen et al. 2016), can manage H. halys but could be before oviposition, parasitoids rely on volatile and contact impractical in many crop systems. Several generalist semiochemical cues to locate hosts, as well as physical predators attack H. halys eggs and nymphs (Cornelius et al. examination of the host egg upon location of the potential 2016; Morrison et al. 2016), but they typically do not cause host (Bin et al. 1993). Trissolcus spp. typically recognize enough mortality to limit population growth. Classical hosts through kairomones involved in host reproduction biological control may provide the greatest potential for (Conti et al. 2003) including volatile chemicals associated management of H. halys across urban, natural, and agri- with adults and eggs, (Sales et al. 1980; Colazza et al. cultural habitats where populations of the pest thrive. 1999), and short-range physical cues including visual Surveys in H. halys’s native range of China for natural recognition (Conti et al. 2003). Recognition of contact cues enemies identified the egg-parasitoid wasp Trissolcus can trigger behavioral response such as arrestment, when japonicus (Ashmead), samurai wasp, (Hymenoptera: Sce- parasitoids remain motionless with their antennae together lionidae), [=Trissolcus halyomorphae (Talamas et al. pointed toward the ground. Evaluating T. japonicus 2013)] as a key candidate classical biological control agent responses to pentatomid hosts in a controlled environment (Yang et al. 2009). Since 2010, the Beneficial Insects and can isolate the effects of host-induced plant volatiles asso- Introduction Unit of the USDA-ARS in Newark, Delaware, ciated with leaf surfaces that may counteract or enhance and several other institutions have evaluated T. japonicus stink bug semiochemicals. In studies restricting contact to in quarantine for potential introduction into the USA. filter paper walked on by stink bugs, Trissolcus basalis While host-specificity research on T. japonicus in quaran- exhibited acceptance behaviors, including arrestment, in tine facilities was ongoing, two detections of adventive T. response to semiochemicals (Peri et al. 2006; Salerno et al. japonicus populations were observed in Maryland (Tala- 2006). Identifying the behavioral responses of T. japonicus mas et al. 2015) and Washington State (Milnes et al. 2016). to multiple stink bug species will detect potential para- Host-specificity testing is critical to ensure that a bio- sitoid-host associations. This will help to predict the success logical control agent will parasitize its target host in the of a biological control agent and risk of nontarget effects field and to reduce risk of unintended ecological conse- prior to augmentative releases for managing H. halys. quences that could result from parasitism of native fauna The recent adventive populations T. japonicus in the by the agent (Ehler 1991; McEvoy 1996; Van Driesche USA may contribute to improved management of H. halys et al. 2000). There are documented examples of unintended (Talamas et al. 2015; Milnes et al. 2016). Since T. japon- consequences on ecological food webs after the release of icus has been recovered in multiple areas in the USA where 123 J Pest Sci (2017) 90:1169–1179 1171 H. halys is established, it is inevitable that T. japonicus will recently emerged (\36 h) females