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

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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. 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. carolinensis. 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 parasitoids in its native range, the use of indigenous tential host species are present in a given habitat the selection of a parasitoids in North America may supplement the current management particular host by a parasitoid could be determined by the availability strategy against this invasive pest. Ontsira mellipes was one of the most of the host, the detectability and behavioral defenses of the host, or the frequently collected parasitoids found during recent surveys of North suitability of the host for the development of the parasitoid’s offspring American native cerambycids and their associated parasitoid commu- (Godfray, 1994). Learning of cues during natal and/or adult develop- nities in red maple (Acer rubrum L.), hickory (Carya tomentosa (Poir.) ment can also affect host selection by parasitoids (Turlings et al., 1993; Nutt) and Virginia pine (Pinus virginiana Mill.) in Mid-Atlantic forests Morris and Fellowes, 2002; Gandolfi et al., 2003; Giunti et al., 2015). (Duan et al., 2015a). Most known members of Ontsira are parasitoids of Overall, it is important to determine the host range or host specificity of Cerambycidae and distributed mainly in the Holarctic (Belokobylskij parasitoids, not only for the selection of efficient agents for biological et al., 2013). Like other members of its genus, O. mellipes is gregarious, control of targeted pests, but also to better understand novel host- an idiobiont, and an ectoparasitoid. Female wasps paralyze the host parasitoid interactions that result from invasions of exotic herbivores larva before laying a clutch of eggs, and hatched larvae feed externally that may indirectly impact native herbivores through shared parasitoids and pupate next to the consumed host (Duan et al., 2015a). Recent (i.e., apparent competition) (Holt and Lawton, 1994; Bonsall and evaluations conducted in a quarantine laboratory show that this para- Hassell, 1999; Heimpel and Mills, 2017). sitoid readily attacks A. glabripennis and has some positive attributes as This study was designed to assess the host range of the North a biological control agent: short generation time (≈25 days for one American parasitoid Ontsira mellipes Ashmead (Hymenoptera: generation) when compared to its target host A. glabripennis (1–2 years Braconidae) as a potential biological control agent for the invasive or even longer in some colder regions) and a female-based sex ratio Asian longhorned beetle, Anoplophora glabripennis (Motschulsky) (85.7% females) (Golec et al., 2016). Female O. mellipes produce (Coleoptera: Cerambycidae). Anoplophora glabripennis is native to China 1.3–6.8 female progeny per parasitized A. glabripennis larva and

2 X. Wang, et al. Biological Control 137 (2019) 104028 parasitization efficiency on this novel host increases with continuous so that it could be placed back over the cut. Underneath the bark flap in rearing on A. glabripennis (Golec et al., 2019). This parasitoid has been the exposed phloem a narrow groove (6.5 × 0.5 × 0.3 cm) was created recorded from larval cerambycids in North America, but little is known using a #11 palm-handled wood veiner (Woodcraft Supply LLC, Par- about its host range (Kula and Marsh, 2011; Duan et al., 2015a). kersburg, WV). The groove extended into the xylem and provided a In this study, we assessed (1) if O. mellipes can attack some common space for the inserted larvae. The bark flap was secured by a thin layer North American cerambycids (Coleoptera: Cerambycidae); (2) whether of Parafilm (Bemis Co., Inc., Neenah, WI). Five red maple sticks, each it prefers to attack A. glabripennis over native species; and (3) if the containing a beetle larva, were then exposed to 5 mated, 1–3 days old natal host of the parasitoid affects its host species preference. In addi- female wasps for one week in a polystyrene container tion, we tested parasitism by O. mellipes on the citrus longhorned beetle, (9.5 × 9.5 × 20.9 cm, Pioneer Plastics Inc., Dixon, KY) with four cir- Anoplophora chinensis Forster (Coleoptera: Cerambycidae), another cular fine mesh ventilation holes (3 cm diameter). Small drops ofhoney high-risk invasive pest (Haack et al., 2010). Native to eastern Asia, A. were streaked on the container lid and a vial with water and cotton chinensis had been detected in eleven European countries since 1980. were placed inside the container. After the parasitoids pupated Populations have been eradicated from nine of these countries but are (≈3 weeks), each exposed stick was dissected using a chisel and a still present in Italy and Croatia (Hérard and Maspero, 2018). Although mallet and all cocoons were transferred to gelatin capsules (Size 1, Herb A. chinensis has not been detected yet in North America, it has been Affair, Palatine, IL) for emergence of parasitoids. frequently intercepted at the US ports of entry as larvae in solid wood packaging material, and invasion into North America is a threat (Haack, 2.2. Selection of native cerambycids 2006). Anoplophora chinensis is also highly polyphagous, attacking citrus and many of the same hardwood trees that A. glabripennis attacks To assess the potential host range of O. mellipes, we focused on (Haack et al., 2010). This additional test adds insights into the potential testing common North American cerambycid beetles infesting major use of O. mellipes for the biological control of A. chinensis should this forest trees such as maples, birches, oaks, and pines. Adult beetles were species become established in the US. collected using cerambycid lure-baited multi-funnel traps and light traps from May through August 2018 from mixed hardwood/pine for- 2. Materials and methods ests in the mid-Atlantic and northeast United States (for details of the collection methods see Gould et al., 2018). Adult beetles were fed a 2.1. Insects and host trees 10% sugar water solution or twigs (Lamiinae) and different species were provided with sticks of their preferred host plants and/or coffee All bioassays were conducted at the quarantine facility of the USDA filters for oviposition at the USDA APHIS Otis Laboratory, MA orBIIRU. ARS Beneficial Insects Introduction Research Unit (BIIRU) in Newark, Of the live-captured adults, six species (Elaphidion mucronatum (Say), DE, where laboratory colonies of the two exotic longhorned beetles (A. Monochamus carolinensis Olivier, Monochamus notatus (Drury), Neoclytus glabripennis and A. chinensis) and the parasitoid (O. mellipes) were scutellaris Olivier, Xylotrechus colonus (Fabricius), and Xylotrechus sa- maintained in separate rooms under controlled conditions gittatus Germar) produced a large number (> 150) of eggs. These spe- (23 ± 1.5 °C, 45–60% RH, 16L:8D). The A. glabripennis colony was cies yielded enough larvae of a suitable stage for host range tests. established from beetles collected in New York, New Jersey, Illinois, These six native cerambycids are among the most common cer- Massachusetts, USA, and China since 1999. The A. chinensis colony was ambycids infesting conifers and hardwoods in the Northeastern United established from larvae provided by the USDA ARS European Biological States (Yanega, 1996; MacRae and Rice, 2007; Handley et al, 2015; Control Laboratory in Montpellier, France, where the original colony Gould et al., 2018). They belong to two subfamilies and three tribes was established using adult beetles collected in Italy. The parasitoid (Handley et al., 2015; Monné et al., 2017). Monochamus carolinensis and colony was established from adults reared from naturally infested red M. notatus are in the same tribe (Monochamini) as the two Asian species maple (Acer rubrum L.) logs collected in Blackbird State Forest in (A. glabripennis and A. chinensis) of the subfamily Laminnae. Neoclytus Townsend, DE during 2010 (Duan et al., 2015a). However, the original scutellaris, X. colonus and X. sagittatus are the members of the Clytini host species of this parasitoid are unclear. tribe and E. mucronatum is a member of the Elaphidiini tribe; both tribes Rearing methods were similar for both beetle species. Branches of belong to the subfamily Cerambycinae. Like A. glabripennis, all of these maple trees (Acer spp.) were collected weekly from the Blackbird State species deposit eggs beneath the bark, and larvae start feeding in the Forest. Large sticks (2–5 cm diameter, 15–20 cm long) were used as an phloem-cambial region when they are young and later bore into the oviposition medium for the beetles, while various small twigs were used xylem. Elaphidion mucronatum and X. colonus are among the most as a food source. Female beetles chew oviposition pits and insert their polyphagous cerambycids; attacking almost all eastern hardwoods. eggs between the inner bark and the sapwood of large sticks and adults Monochamus carolinensis and M. notatus are both common wood-boring will feed on the bark of the twigs. Early larval instars feed under the beetles of pines. Neoclytus scutellarus prefers to attack species of oak but bark, whereas later instars enter the wood. Each pair of adult beetles can also feed on pines. Both M. carolinensis and X. sagitiatus are also was reared in a plastic container (3.47 L) and provided 8–10 small twigs economically important pests as they are vectors of the pinewood ne- as food and one large stick as oviposition medium each week. Exposed matode Bursaphelenchus xylophilus (Steiner & Buhrer) Nickle (Aphe- sticks were held until eggs had hatched (≈one month). Young larvae lenchida: Parasitaphelenchidae) (Linit, 1988). For each species, newly were retrieved from the sticks and transferred to 28.3 ml plastic cups hatched larvae were transferred to 28.3 ml plastic cups to rear in- (SOLO Cup Co., Urbana, IL) for rearing individually on a cellulose- dividually on artificial diets as described above for A. glabripennis, until based artificial diet as described by Dubois et al. (2002). they reached the appropriate size (at least 2nd instar) for testing. The O. mellipes population had been reared on A. glabripennis larvae in medium size maple sticks (1–2 cm diameter, 16 cm long) for 70–75 2.3. Host range test generations since 2010 in the quarantine facility. Additional wild populations of O. mellipes were collected from maple trees naturally in- The test for each beetle species consisted of three treatments: (1) a fested with native cerambycids in 2011–2018 and added to the colony. no-choice test with the beetle species (referred to as the ‘alternative After the host larvae had developed into at least 2nd or 3rd instars (in host’); (2) a no-choice test with A. glabripennis (referred to as the target 1–2 months), they were individually inserted into freshly cut maple host and served as a positive control); and (3) a choice test between A. sticks under a flap of bark (Golec et al., 2018). The outer bark of a stick glabripennis and an alternative species. Test methods and procedures was separated from the inner bark longitudinally by shaving it off with were similar for each beetle species, and all tests were carried out in a sharp box cutter blade leaving the outer bark attached only at one end ventilated polystyrene containers (described above in Section 2.1) in a

3 X. Wang, et al. Biological Control 137 (2019) 104028 growth chamber under the conditions (23 °C, 45–65% RH, and 16L:8D). recognized. Therefore, at the time of dissection each exposed host larva Female wasps used for all tests were reared from A. glabripennis. Newly was categorized as parasitized, alive (not parasitized) or dead (not emerged wasps (1 male: 4 females) were placed in a vial (6 × 2 cm) and parasitized). observed for mating (occurred within 1 h). Naïve (no prior foraging or A subset of parasitoids that emerged from one of the readily at- oviposition experience), 1–3 days old, mated females were used for the tacked hosts (M. carolinensis as a representative native host) in the tests. Tested sticks each containing one beetle larva were prepared as above experiment were tested to determine if emerging parasitoid described above for the rearing of the parasitoid one day prior to the adults preferred to oviposit on members of the species from which they tests to allow for larvae feeding and production of frass. Each tested emerged. Test methods were similar to the above experiment, except larva was taken from the rearing cup, weighed on a Sartorius analytical that in the choice test a single female was exposed to one M. carolinensis electrobalance (Model 1801, ± 0.1 mg) and then inserted into one stick larva in a pine stick and one A. glabripennis larva in a maple stick. Both (≈2 cm diameter, 16 cm long) of its respective (preferred) host tree larvae were weighed to match their comparable sizes ( ± 5 mg) for (red maple A. rubrum for A. glabripennis, A. chinensis, E. mucronatum, X. each replicate. Each stick was carefully checked every 2 days under a colonus or X. sagittatus and pine P. strobus L. for M. carolinensis, M. no- microscope to determine which host was attacked first, the time taken tatus or N. scutellaris). In the no-choice test, a single host larva (i.e., one to first parasitize the host, and the number of eggs laid on eachpara- stick) was exposed to a single mated female wasp, while in the choice sitized host. When both hosts were found parasitized, the order of at- test one larva of each host (i.e., two sticks) were exposed simulta- tack could be easily determined based on the developmental stages of neously to two mated female wasps. This design holds the ratio of host: the immature parasitoid eggs or young larvae (parasitoid eggs started parasitoid constant across different levels of host density. Because hatching 2 days post-oviposition). As described above, all parasitized preliminary observations based on daily monitoring of exposed hosts hosts were reared in the sticks until cocoons had formed. The cocoons revealed that the parasitoid took a mean ( ± SE) of 4.2 ± 0.3 days were transferred to capsules for the emergence of the parasitoids. All (range 1–7 days, n = 20) to parasitize a host, the exposure time in both tested female wasps were immediately killed in the freezer after the 7- no choice and choice tests was set-up for 7 days to maximize the day exposure and dissected to determine how many mature eggs re- probability of attack. In the no-choice test, the larval size was not mained and to measure their ovipositor lengths at the maximum ex- strictly controlled among replicates to purposefully create variation to trusion. This would confirm if the tested female parasitoids had suffered examine the effect of host size. In the choice test, however, similar sizes from egg limitation. The experiment had 30 replicates for each no- ( ± 5 mg) of both beetle species were selected for each replicate. Small choice test and 42 replicates for the choice test. drops of honey were streaked on the container lid and a vial with water and cotton was placed inside the container as nourishment for the 2.4. Data analyses parasitoids. Tests had 18–30 replicates (dependent on the availability of beetle larvae) for each beetle species, except for N. scutellaris (eight The sizes (weight) of tested host larvae were compared among all replicates) and X. sagittatus (ten replicates) due to the difficulty of tested species in the no-choice tests and between the two different host rearing enough larvae of suitable size for the tests. There were only four species in each choice test using a one-way Analysis of Variance replicates of the choice test of N. scutellaris, and the data were excluded (ANOVA). In the no-choice tests, the probability of a host larva being from the analyses due to the small sample size. Exposed sticks were held parasitized (coded as 1) or unparasitized (alive or dead without signs of for three weeks (to allow the parasitoids time to pupate) and then each parasitism, coded as 0) was analyzed using a generalized linear model stick was dissected. All cocoons were transferred to capsules and (GLM) with binomial distribution and a logit link function, considering monitored daily until the emergence of parasitoids. The emergence and the effects of both host species and host larval size. In the choice tests, sex of the parasitoids were recorded daily. All dead hosts were ex- the numbers of parasitized larvae of the two different host species were amined under a microscope to determine the presence or absence of compared using a Chi-square test, with a null hypothesis of equal choice recognizable parasitoid cadavers. The dead parasitoid eggs and larvae of attack of both host species by the parasitoid. were normally attached to the outer surface of the host and were easily In the additional choice test between A. glabripennis and M.

Table 1 Experimental treatments and host larval size (weight) in both no-choice tests with each host species and choice tests between A. glabripennis and each of the other host species for O. mellipes reared from A. glabripennis or M. carolinensis.

Test Natal host of the parasitoid No-choice test Choice test

n Host species Host size (mg)1 n Host species Host size (mg)1

1 A. glabripennis 30 A. chinensis 727 ± 37a 30 A. chinensis 739 ± 52a 30 A. glabripennis 726 ± 37a A. glabripennis 743 ± 52a 2 A. glabripennis 18 E. mucronatum 87 ± 15c 18 E. mucronatum 123 ± 15a 18 A. glabripennis 87 ± 14c A. glabripennis 112 ± 12a 3 A. glabripennis 30 M. carolinensis 470 ± 21b 30 M. carolinensis 465 ± 22a 30 A. glabripennis 468 ± 21b A. glabripennis 461 ± 22a 4 A. glabripennis 30 M. notatus 444 ± 59b 30 M. notatus 414 ± 59a 30 A. glabripennis 442 ± 59b A. glabripennis 414 ± 58a 5 A. glabripennis 8 N. scutellaris 111 ± 37c →2 8 A. glabripennis 116 ± 38c →2 6 A. glabripennis 30 X. colonus 179 ± 21c 30 X. colonus 188 ± 22a 30 A. glabripennis 179 ± 21c A. glabripennis 188 ± 21a 7 A. glabripennis 10 X. sagittatus 72 ± 9c 10 X. sagittatus 110 ± 34a 10 A. glabripennis 74 ± 8c A. glabripennis 112 ± 34a 8 M. carolinensis 30 A. glabripennis 511 ± 18b 42 A. glabripennis 500 ± 11a 30 M. carolinensis 513 ± 19b M. carolinensis 500 ± 11a

1 Values are mean ± SE and compared among different host species for all no-choice tests or between the two different host species for each choicetest separately. Different letters within the column indicate significant difference (P < 0.05, one-way ANOVA, Tukey HSD). 2 No-choice test data were excluded due to small samples (n = 4).

4 X. Wang, et al. Biological Control 137 (2019) 104028 carolinensis using the parasitoids reared from the latter host, the fre- parasitized A. chinensis, E. mucronatum, M. carolinensis and M. notatus, quencies of first attack on the two different host species were compared but did not parasitize N. scutellaris, X. colonus or X. sagittatus (Fig. 2). using a Chi-squared test. The differences in the mean duration to The parasitoid did not show a preference for A. glabripennis over other parasitize M. carolinensis and A. glabripennis were subject to survival host species when the parasitoids were reared from A. glabripennis or a analyses. The number of eggs laid on each parasitized host (i.e., clutch preference for M. carolinensis over A. glabripennis when the parasitoids size) and the percentage of the eggs developed into adults (i.e., off- were reared from M. carolinensis (Fig. 2). spring survival) were compared between the two different host species In the additional choice tests with the parasitoids reared from M. using a one-way ANOVA. carolinensis, there was no significant difference in the frequency that O. Finally, data were pooled from all parasitized larvae for each at- mellipes selected M. carolinensis before A. glabripennis (18) or A. glabri- tacked host species to determine the effects of host species and host size pennis before M. carolinensis (14) (χ2 = 0.67, df = 1, P = 0.412). There (given the variation in larval size within treatments and among species) was no difference in the mean ( ± SE) time that it took for thepara- on realized reproductive success in terms of the number of offspring sitoid to parasitize A. glabripennis (4.18 ± 0.31 days) vs. M. carolinensis emerging from each parasitized host larva and offspring sex ratio. The (3.12 ± 0.43 days) (Log-rank test; χ2 = 1.26, df = 1, P = 0.261). effects of host species, host size and a host species × host size inter- Dissections of female wasps after their oviposition period revealed that action on the number of emerged offspring and offspring sex ratio were female wasps that had laid eggs had a mean ( ± SE) of 20.7 ± 1.6 analyzed using a GLM with Poisson distribution and a log link function. mature eggs (n = 29) remaining in their ovaries, which was fewer than

The relationship between the number of parasitoid offspring emerged those that did not lay eggs (34.5 ± 3.0 mature eggs, n = 11) (F1, and host larval size was also fitted to a linear model for each species 38 = 18.84, P < 0.001). Both the number of eggs laid on each para- separately. Prior to all ANOVA analyses, proportion data were logit sitized host (F1, 50 = 0.81, P = 0.373) and offspring survival (F1, transformed. For all one-way ANOVA analyses, multiple comparisons 50 = 0.74, P = 0.394) were not significantly different between M. car- were subsequently performed using Tukey’s honestly significance dif- olinensis and A. glabripennis (Fig. 3). ference (HSD). All analyses were performed using JMP Pro ver13 (SAS Of all parasitized host larvae, A. chinensis were the largest, followed

2013, Cary, NC). by A. glabripennis, M. carolinensis or M. notatus, and E. mucronatum (F4, 403 = 22.13, P < 0.001) (Table 2). The number of surviving parasitoid 3. Results offspring was affected by host species (F4, 403 = 111.38, P < 0.001) and the interaction between the host species and host size (F4, In the no-choice tests, larval sizes were different among different 403 = 35.08, P < 0.001), but not by host size itself (F1, 403 = 2.91, tests but were similar within each test (F15, 356 = 37.6, P < 0.001) P = 0.088). Further analyses of each host species separately showed a (Table 1). The largest larvae were A. chinensis, followed in descending positive increase of the number of surviving offspring (y) with host size order by A. glabripennis, M. carolinensis, M. notatus, X. colonus, N. scu- (x) in A. glabripennis (y = 7.058 + 0.005x, n = 235, r2 = 0.100, tellaris, E. mucronatum and X. sagittatus. In all choice tests, the sizes of P < 0.001) and M. notatus (y = 6.174 + 0.008x, n = 31, r2 = 0.146, the two different species were not significantly different (all P va- P = 0.019). However, this relationship was not significant in A. chi- lues > 0.05) (Table 1). nensis (n = 40, F = 3.21, r2 = 0.078, P = 0.081), E. mucronatum In the no-choice tests, O. mellipes parasitized A. chinensis, E. mu- (n = 13, F = 0.33, r2 = 0.029, P = 0.578) or M. carolinensis (n = 88, cronatum, M. carolinensis, and M. notatus but did not parasitize N. scu- F = 2.71, r2 = 0.031, P = 0.104). The realized reproductive efficiency tellaris, X. colonus and X. sagittatus. In all tests, A. glabripennis, which in terms of the number of offspring produced per unit host mass (mg) served as a positive control, was parasitized (Fig. 1). The probability of was higher on E. mucronatum, lower on A. chinensis, and similar among a host larva being parasitized was influenced by host species other three parasitized host species (F4, 403 = 20.22, P < 0.001) (χ2 = 70.03, df = 1, P < 0.001), but not by host larval size (Table 2). Offspring sex ratio was not affected by host species (χ2 = 0.07, df = 1, P = 0.796). In the choice test, O. mellipes also (χ2 = 0.88, df = 4, P = 0.966), host larval size (χ2 = 0.11, df = 1,

Fig. 1. Percentages of hosts parasitized, alive (not parasitized) and dead (with no sign of parasitism) in no-choice tests of O. mellipes with different host species. Tested wasps were reared from either A. glabripennis (Tests 1–7) or M. carolinensis (Test 8) and the rearing hosts of the parasitoid severed as a positive control for the test of each host species.

5 X. Wang, et al. Biological Control 137 (2019) 104028

Fig. 2. A choice test showing the percentages of the target host of Asian longhonred beetle (ALB), A. glabripennis and the alternative host species parasitized by O. mellipes. Tested wasps were reared from M. carolinensis (# only for this test) or A. glabripenni (for all other tests). Asterisks indicate significant difference (Chi-square test; ns = not significant).

P = 0.743) or the interaction of both factors (χ2 = 0.16, df = 4, P = 0.997) (Table 2).

4. Discussion

This study demonstrated the ability of the North American parasitoid (O. mellipes) to attack and develop on three North American (E. mucronatum, M. carolinensis and M. notatus) and two Asian (A. glabripennis and A. chinensis) cerambycids. However, O. mellipes did not parasitize three other tested native cerambycids (N. scutellaris, X. colonus and X. sagittatus), which exhibit similar feeding behavior. For successful parasitism, a female O. mellipes must first locate sticks containing live host larvae, then detect, sting, and paralyze the hosts underneath the bark and eventually develop on the hosts. Many wood- boring parasitoids locate the host habitat using attractant semi- ochemical cues from the host plant, host feeding and/or defecating and detect the concealed host using vibrations caused by the host feeding (Hanks et al., 2001; Wang et al., 2010; Paine, 2017). Although the exact mechanisms of host location by this parasitoid have not yet been in- vestigated, O. mellipes females were observed to search on infested sticks, drill their ovipositor through the bark, and sting and paralyze the hosts prior to laying a clutch of eggs on each attacked host species. In contrast, host detection behaviors were not observed on the three unparasitized host species and dissections of exposed sticks confirmed that the host larvae of these species were either alive or dead and showed no Fig. 3. (A) Numbers of eggs laid per parasitized host (clutch size) and (B) signs of parasitism. As was the case for species that were attacked, the percentages of eggs developed into adults (offspring survival) when O. mellipes larvae of N. scutellaris, X. colonus and X. sagittatus were actively feeding parasitized A. glabripennis and M. carolinensis in a choice test. Tested wasps were on maple or pine sticks (their mean galley widths were 4.98 ± 0.97, reared from M. carolinensis. Bars refer to mean ± SE and same letters above the 5.53 ± 0.24 and 5.85 ± 0.44 mm, respectively). Like other typical bars indicate no significant difference (ANOVA, P > 0.05). idiobiont ectoparasitoids, O. mellipes larvae feed externally on the

Table 2 Effects of host species and host larval size on the number of emerged offspring and offspring sexratioof O. mellipes.

Host species n Host larval weight (mg)1 No. of offspring per host2 No. of offspring per host mass1 (mg) % Female offspring2

A. glabripennis 236 409.0 ± 17.7b 9.85 ± 0.39 0.036 ± 0.002b 77.5 ± 1.9 A. chinensis 40 739.0 ± 40.0 a 9.83 ± 0.77 0.016 ± 0.002c 79.4 ± 4.4 E. mucronatum 13 128.3 ± 15.4c 10.08 ± 1.03 0.094 ± 0.013 a 79.0 ± 2.0 M. carolinensis 88 492.3 ± 11.9b 15.10 ± 0.84 0.032 ± 0.002b 78.4 ± 3.3 M. notatus 31 473.5 ± 54.2b 10.01 ± 1.06 0.034 ± 0.007 bc 65.9 ± 6.9

1 Data were pooled from all parasitized hosts and all tests for each host species. Values are mean ± SE and different letters within the column indicate significant difference (P < 0.05, One-way ANOVA, Tukey HSD). 2 Data were subject to the analyses on the effects of both host species, host size and the interaction of these factors by GLM(seetext).

6 X. Wang, et al. Biological Control 137 (2019) 104028 paralyzed host and probably do not need to overcome interior physio- research of O. mellipes is required to quantify the host size preference logical host defenses (Strand and Obrycki, 1996). Thus, behavioral and the fitness consequence of host size selection (Zaviezo and Mills, adaptations to locate the host habitat and hosts could be the key to 2000). In terms of the realized reproductive outcomes per unit host successfully exploiting certain wood-boring host species by this para- mass, the parasitoid seems to perform best on E. mucronatum, poorest sitoid. Among the five parasitized host species, four species (A. glabri- on A. chinensis and equally well on A. glabripennis, M. carolinensis and M. pennis, A. chinensis, M. carolinensis and M. notatus) belong to the notatus. This suggests that E. mucronatum is likely one of the favored Monochamini tribe of the subfamily Laminnae and are phylogenetically native host species utilized by this parasitoid. more distant from the three unparasitized species (N. scutellaris, X. co- Although more effective biological control of A. glabripennis would lonus and X. sagittatus) which belong to the Clytini tribe of the subfamily likely be achieved through the introduction of host-specific parasitoids Cermbycinae. However, another parasitized species (E. mucronatum) collected in the native range, to date there have not been any suitable belongs to the Elaphidiini tribe of the subfamily Cerambycinae. This host-specific parasitoids found appropriate for classical biocontrol. An suggests that the parasitoid may be attracted to host insect cues re- indigenous parasitoid such as O. mellipes that has already adapted to leased by phylogenetically closely related cerambycid species, although local ecological conditions and can overcome behavioral and physio- our data sets are too small to conduct phylogenetical signal analysis logical defenses by A. glabripennis is the only viable biological control (Desneux et al. 2012). Ontsira mellipes successfully parasitized different agent so far discovered, and this species could be manipulated either hosts on two different trees (maple and pine), which suggests that host- through conservation or augmentation to help regulate this exotic pest. plant odors or other differences between maple and pine do not affect Our results have important implications for augmentation or con- this parasitoid’s host searching behavior. It is possible that the length of servation biological control of A. glabripennis. This parasitoid could be the ovipositor of female O. mellipes (3.91 ± 0.05 mm, n = 25) may mass-reared and released against A. glabripennis in areas where A. limit the parasitoid’s access to some of these host larvae that feed deep glabripennis populations are currently present to supplement the current inside the wood (Hanks et al., 2001). eradication management strategy. While mass rearing on A. glabripennis There was no evidence that O. mellipes showed a preference for A. is efficient (Golec et al., 2019), it can only be reared in quarantine fa- glabripennis over other attacked host species, regardless of the natal host cilities where space is limited. Ontsira mellipes could be mass reared on species of the parasitoid. Many parasitoids under choice tests prefer to some native hosts such as M. carolinensis as its offspring seems to per- attack hosts in or on which they previously developed (Morris and form as well as on A. glabripennis and the rearing host appears to not Fellowes, 2002; Gandolfi et al., 2003; Giunti et al., 2015). This phe- affect the parasitoid’s host preference. This would facilitate mass nomenon has been explained as preimaginal learning (learning during rearing of this parasitoid outside of a quarantine facility for augmen- the insect’s early life stages) and as early adult stage learning that could tative release against A. glabripennis. occur when newly emerged and naïve adult wasps learn volatiles The parasitoid fauna attacking larval woodborers consists pre- emitted from the natal host-plant complex. However, conclusive evi- dominantly of idiobiont, gregarious ectoparasitoids (Hanks et al., 2001; dence of such learning ability in parasitoids is still not substantial Wang et al., 2010; Belokobylskij et al., 2013; Paine, 2017). The gregar- (Turlings et al., 1993; Morris and Fellowes, 2002; Giunti et al., 2015). ious nature of these parasitoids seems to be consistent with the cryptic In our experiment, the cocoons of O. mellipes were removed from the nature of woodborers feeding within galleries in wood (Gauld, 1988) and sticks and adults emerged from the cocoons in clean capsules. Pre- host larvae that are often much larger than the parasitoids. Indeed, a imaginal learning and early adult learning apparently did not happen in recent survey of Cerambycidae and their associated parasitoids in Mid- O. mellipes. Additionally, parasitoids also often prefer to attack host Atlantic Forests in the US found that all Braconidae, including O. mellipes, species in or on which they had previously experienced contact or emerging from cerambycid-infested trees belonged to the subfamily successful oviposition (i.e., associative learning after ‘rewarding’ ex- Doryctinae (Duan et al. 2015a). Doryctinae are predominantly idiobiont perience) (Turlings et al., 1993). We cannot not rule out the possibility gregarious ectoparasitoids of larval woodboring coleopterans in the fa- of such associative learning by this parasitoid. Our experimental design milies Cerambycidae, Buprestidae and Curculionidae (Belokobylskij did not allow us to test the latter learning effect since we did not re-test et al., 2013). Given that the complex of parasitoids that tends to attack the female wasps after their first host selection, and further studies are woodboring insects generally have a broader range and may be able to needed to determine possible associative learning by this parasitoid. adapt to newly introduced woodborers, biotic resistance through con- For host species that were parasitized by O. mellipes, the sizes of host serving these native parasitoids may play a role in suppressing exotic larvae varied within and among the different host species. In addition to invasive woodboring insect pests such as A. glabripennis. the possible effect of host species, host size often affects the perfor- On one hand, the impacts of O. mellipes on the target pest (A. mance of idiobiont and gregarious parasitoids, as many fitness para- glabripennis) could be enhanced in the presence of available alternative meters can be strongly affected by host size at the time of oviposition and native hosts to support local parasitoid populations. On the other (Godfray, 1994; Zaviezo and Mills, 2000; Morris and Fellowes, 2002; hand, however, the presence of alternative hosts may affect the control Wang and Messing, 2004). We found that the relationship between the of the target pest if they are more significantly preferred by their shared number of emerged O. mellipes offspring and host size was not parasitoids. Ontsira mellipes shows no preference for these native hosts straightforward; it increased positively with host size in A. glabripennis over A. glabripennis or A. chinensis and seems to have the ability to and M. notatus but was not significant in the other three attacked host readily switch from the alternative hosts such as M. carolinensis to A. species. Perhaps this was due to the size range of tested host larvae for glabripennis. Thus, the presence of native hosts may increase the para- A. glabripennis (20–1285 mg) and M. notatus (40–1005 mg) being sub- sitism of these targeted pests. These introduced woodborers may in- stantially larger than those of A. chinensis (231–1281 mg), E. mucro- directly affect native woodborers via shared generalist parasitoids such natum (29–234 mg) or M. carolinensis (184–765 mg). Although O. mel- as O. mellipes, i.e., apparent competition (Holt and Lawton, 1994). lipes is able to develop on large or small host larvae, and native or non- Further studies are needed to evaluate the efficacy of O. mellipes in native host species, it was observed during the dissections that para- suppressing A. glabripennis populations under field conditions (cage sitoid larvae did not consume the entire host for some large host larvae and/or open release) within the quarantined area of this pest in the US, such as A. chinensis but consumed almost the entire host for some small and to monitor the potential impacts of the invasion of A. glabripennis host larvae such as E. mucronatum. Various factors, such as availability on other native cerambycids via possible apparent competition. Un- of mature eggs, the parasitoid’s ability to assess host size or the para- derstanding the ecological mechanisms underlying novel species in- sitoid’s reproductive strategy in terms of maximizing lifetime fitness teractions is necessary for optimizing management strategies such as gain verses maximizing fitness gain from individual hosts could affect biological control that aims to limit the impacts of invasive pests the reproductive outcome of an oviposition event. More detailed (Hokkanen and Pimentel, 1989; Heimpel and Mills, 2017).

7 X. Wang, et al. Biological Control 137 (2019) 104028

CRediT authorship contribution statement (Hymenoptera: Ichneumonidae and Braconidae). Biol. J. Linn. Soc. 35, 351–377. Giunti, G., Canale, A., Messing, R.H., Donati, E., Stefanini, C., Michaud, J.P., Benelli, G., 2015. Parasitoid learning: current knowledge and implications for biological control. Xingeng Wang: Conceptualization, Data curation, Formal analysis, Biol. Control 90, 208–219. Funding acquisition, Methodology, Supervision, Writing - original draft. Godfray, H.C.J., 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton Ellen M. Aparicio: Data curation, Methodology, Writing - review & University Press, Princeton, NJ. Golec, J.R., Duan, J.J., Aparicio, E., Hough-Goldstein, J., 2016. Life history, reproductive editing. Theresa C. Murphy: Data curation, Methodology, Writing - biology, and larval development of Ontsira mellipes (Hymenoptera: Braconidae), a review & editing. Jian J. 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