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Assessing the Host Range of the North American Parasitoid Ontsira Mellipes: T Potential for Biological Control of Asian Longhorned Beetle ⁎ Xingeng Wanga, , Ellen M

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Assessing the Host Range of the North American Parasitoid Ontsira Mellipes: T Potential for Biological Control of Asian Longhorned Beetle ⁎ Xingeng Wanga, , Ellen M Biological Control 137 (2019) 104028 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Assessing the host range of the North American parasitoid Ontsira mellipes: T Potential for biological control of Asian longhorned beetle ⁎ Xingeng Wanga, , Ellen M. Aparicioa, Theresa C. Murphyb, Jian J. Duana, Joseph S. Elkintonc, Juli R. Gouldb a United States Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit, Newark, DE 19713, USA b United States Department of Agriculture, Animal and Plant Health Inspection Service, Otis ANGB Lab, MA 02542, USA c Department of Environmental Conservation, University of Massachusetts, Amherst, MA 01003, USA GRAPHICAL ABSTRACT Ontsira mellipes attacked A. glabripennis and did not show a preference between A. glabripennis and other attacked cerambycids (* = significant, ns = not significant, P = 0.05). #Parasitoids used in this trial were reared from M. carolinensis while all other trials used parasitoids reared from A. glabripennis. ARTICLE INFO ABSTRACT Keywords: The Asian longhorned beetle (ALB), Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae) is a high-risk, Anoplophora chinensis invasive pest of hardwood trees that has been targeted for eradication in the US since the 1990s. Ontsira mellipes Anoplophora glabripennis Ashmead (Hymenoptera: Braconidae) is a native North American parasitoid that has been found to be capable of Biotic resistance attacking ALB larvae under laboratory conditions. To investigate the potential host range of O. mellipes we exposed six Exotic insect pest common North American cerambycid species (Elaphidion mucronatum (Say), Monochamus carolinensis Olivier, Indigenous parasitoid Monochamus notatus (Drury), Neoclytus scutellaris Olivier, Xylotrechus colonus (Fabricius), and Xylotrechus sagittatus Germar) and the citrus longhorned beetle (Anoplophora chinensis Forster) to adult O. mellipes for possible oviposition. Results showed that O. mellipes successfully attacked A. glabripennis, A. chinensis, E. mucronatum, M. carolinensis and M. notatus, but did not attack N. scutellaris, X. colonus and X. sagittatus in both choice and no-choice tests. Ontsira mellipes did not show a preference between A. glabripennis and other attacked host species, regardless of the host species on which the tested parasitoids were reared. The number of progeny emerging per parasitized host larva was influenced by the attacked host species and by the interaction between the attacked host species and the size of parasitized larvae. Neither host species nor the size of parasitized larvae influenced the sex ratio (≈ 80% females) of the parasitoid’s offspring. In terms of progeny fitness, the parasitoid preformed equally well on A. glabripennis as on native hosts such as M. car- olinensis. The use of O. mellipes as a biological control agent for A. glabripennis is discussed. ⁎ Corresponding author. E-mail address: [email protected] (X. Wang). https://doi.org/10.1016/j.biocontrol.2019.104028 Received 29 March 2019; Received in revised form 9 July 2019; Accepted 13 July 2019 Available online 15 July 2019 1049-9644/ Published by Elsevier Inc. X. Wang, et al. Biological Control 137 (2019) 104028 1. Introduction and Korea (Carter et al., 2009; Meng et al., 2015). In North America, the beetle was first detected in New York City, NY in 1996; and thenin In general, biological control programs for invasive exotic pests can Chicago, IL (1998); Toronto, Canada (2001); Jersey City (2002), Car- focus on utilizing natural enemies native to the countries of origin of teret (2004), and Linden (2006), NJ; Worcester (2008) and Boston the pests and/or utilizing natural enemies native to the introduced re- (2010), MA; and Clermont, OH (2011) (Cavey et al., 1998; Haack, gions. Although introduction of specialist natural enemies from a pest’s 2006; Dodds and Orwig, 2011). Populations were found in urban and/ native range has been historically preferable for the control of an exotic or suburban areas in these cities. Anoplophora glabripennis has been pest (Bellows, 2001; Hoddle, 2004; Stiling and Cornelissen, 2005; declared eradicated from Illinois, New Jersey and Ontario, but is still Heimpel and Mills, 2017), there is increasing interest in promoting the present in the other locations (Haack, 2006, Haack et al., 2010; Meng use of indigenous natural enemies in introduced regions (Cornell and et al., 2015; APHIS, 2019). In Europe, the beetle was initially reported Hawkins, 1993; Chang and Kareiva, 1999; Symondson et al., 2002). in Austria in 2001, with additional infestations found in France (2003), Parasitoids, rather than predators and pathogens, have typically been Germany (2004), Italy (2007), Belgium (2008), the Netherlands (2010), the preferred agents for biological control of invasive insect pests (van Switzerland (2011), the United Kingdom (2012), Finland (2015) and Driesche et al., 2010; Daane et al., 2015; Duan et al. 2015b). Specialist Montenegro (2015) (Javal et al. 2017). Populations were eradicated in parasitoids are normally considered more effective in targeting hosts Belgium and the Netherlands but are still present in other countries due to their long-shared history of co-adaption (e.g., Kimberling, 2004) (Hérard et al., 2013; Javal et al. 2017). Anoplophora glabripennis is but can be more vulnerable to modified ecological conditions such as highly polyphagous; attacking various hardwood trees including maple tri-trophic interactions in the introduced range (e.g., Wang et al., (Acer spp.), poplar (Populus spp.), willow (Salix spp.), and elm (Ulmus 2009). When an exotic pest colonizes a new habitat, resident para- spp.) (Haack et al., 2010). In North America, it has been found at- sitoids may require time to adapt to the exotic host, but these naturally tacking 25 deciduous tree species, most notably various maple species occurring biological controls could play an important role in regulating (Haack et al., 2010; Meng et al., 2015). If the populations become exotic pests or hindering the establishment and spread of exotic pests permanently established, it is capable of destroying over 30% of the (i.e., biotic resistance) (Heimpel and Mills, 2017). For example, the urban trees in the US at an estimated economic loss of $669 billion to introduced light brown apple moth Epiphyas postvittana (Walker) (Le- urban areas in the US alone (Nowak et al., 2001). Anoplophora glabri- pidoptera: Tortricidae) suffers from heavy attack by indigenous para- pennis is largely cryptic and remains hidden within the tree during the sitoids in California; both the parasitoid species richness and parasitism immature stages. Even with ongoing extensive quarantine and eradi- rates in California are comparable to, or possibly even higher than, cation efforts, these beetles can be difficult to detect especially inlarge those in the moth’s native range in Australia (Wang et al., 2012). The forested areas, and new introductions are possible. Considering the recent decline of E. postvittana in California may be partly due to the continuous threat of re-establishment in North America, sustainable many resident enemies that readily attack it (Hopper and Mills, 2016). management strategies need to be developed. Biological control is a Therefore, it is prudent to evaluate the potential role of indigenous valuable option for reducing established and incipient populations, natural enemies on invasive exotic pests and investigate their possible especially in large and more natural forests, where more intensive use in addition to other management practices. management methods such as chemical control or removal of infested Assessing a parasitoid’s host range is often the first step in the de- trees may be prohibitively expensive and/or environmentally undesir- velopment of biological control programs (van Driesche and Reardon, able. 2004; Heimpel and Mills, 2017). In the native ecosystems of herbi- Several native natural enemies of A. glabripennis have been reported vorous insect parasitoids, host and parasitoid interactions develop from in China and/or South Korea, but none of these parasitoids tested thus the co-adaptation among the host plant, host, and its specialized far have demonstrated specificity on A. glabripennis (Smith et al., 2007; parasitoids (Price et al., 1980; Godfray, 1994). Parasitoids rely on a Gould et al., 2018; Kim et al., 2018; Rim et al., 2018). Of the tested variety of stimuli (e.g. visual and olfactory cues, physical contact with parasitoids, Dastarcus helophoroides (Fairmaire) (Coleoptera: Bo- the host and its associated products) to locate hosts and employ mul- thrideridae) and Sclerodermus guani Hope (Hymenoptera: Bethylidae) tiple mechanisms to overcome host defenses (Vinson, 1976; Vet and are the two major parasitoids of A. glabripennis reported in China, but Dicke, 1992; Godfray, 1994). Phenological, behavioral, or physiological both species have a broad host range and would be unsuitable candi- constraints may prevent the use of certain hosts, with behavioral dates for classical biological control due to the potential risks to non- adaptations often preceding physiological adaptations in the evolution target native woodborers in North America (Gould et al., 2018; Rim of host specificity (Futuyma and Moreno, 1988; Godfray, 1994; Strand et al., 2018). While efforts are underway to discover more specialized and Obrycki, 1996; Desneux et al., 2012). When many different po- A. glabripennis
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