Biological Control Program Is Being Developed for Brown Marmorated Stink Bug by Jesus Lara, Charlie Pickett, Chuck Ingels, David R

Review Article Biological control program is being developed for brown marmorated stink bug by Jesus Lara, Charlie Pickett, Chuck Ingels, David R. Haviland, Elizabeth Grafton-Cardwell, David Doll, James Bethke, Ben Faber, Surendra K. Dara and Mark Hoddle

Brown marmorated stink bug (BMSB) is an invasive, polyphagous pest that has been Pennsylvania. Since then, BMSB has detected in 42 U.S. states. In 2010, it caused millions of dollars in crop damages to been detected in 42 U.S. states, with establishment (reproduction) confirmed in apple growers on the East Coast, where it arrived from Asia during the 1990s. In 2002, at least 26 states where nuisance and/or BMSB was reported in California; since then, it has been detected in 28 counties and agricultural problems associated with its is established in at least nine counties. Although this pest has not yet been found on presence and ensuing economic losses to commercial crops in the state, detections of BMSB in commercial orchards have been crops have been reported (NIPMC 2015). Crop losses from BMSB and aggrega- documented in Oregon and Washington. Proactive research in California has joined tions in human-made structures have national efforts led by U.S. Department of Agriculture researchers to develop a classi- been significant in the eastern United cal biological control program for BMSB. A study is under way to determine potential States, where BMSB first established (Rice non-target effects of a specialist egg parasitoid, Trissolcus japonicus (Hymenoptera: et al. 2014). The establishment of BMSB in this region confirms its tolerance to Platygastridae), imported from Beijing, China, part of the home range of BMSB. In addi- climates outside of its home range. Field tion, the role of BMSB natural enemies residing in California is being assessed. A review and laboratory research is needed to char- of the recent research outlines the possible opportunities for reducing the threat BMSB acterize the degree to which BMSB can poses to California. tolerate temperature stresses (i.e., winter cold and summer heat) and how this may influence population dynamics in other geographic locations within the United rown marmorated stink bug using its piercing-sucking mouthparts to States (Cira et al. 2016). In addition, the (BMSB), Halyomorpha halys (Stål) feed. Characterization of feeding injury invasion process of BMSB in the United B(Hemiptera: Pentatomidae), has a to marketable crops such as surface dis- native range that includes China, Japan, coloration, depressed areas, deformation Online: http://californiaagriculture.ucanr.edu/ Korea and Taiwan. Its host plant range or abortion of fruit bodies and internal landingpage.cfm?article=ca.v070n01p15&fulltext=yes extends to more than 170 species, among tissue damage can vary by crop (Rice doi: 10.3733/ca.v070n01p15 which are valuable ornamentals and ag- et al. 2014). BMSB was first detected in ricultural fruit, nut and vegetable crops the United States in 1996 in Allentown, (Lee et al. 2013; Rice et al. 2014). BMSB can cause direct injury to crops while

BMSB adult feeding on kumquat fruit. In California, BMSB populations are found mainly in urban locales, but there is risk they will move into agricultural areas.

http://californiaagriculture.ucanr.edu • JANUARY–MARCH 2016 15 Mike Lewis Mike States may have been facilitated by the to facilitate the development of strategic (> 5-kilometer) flights during a 24-hour lack of effective natural enemies and the BMSB management guidelines. period (Lee et al. 2014; Wiman et al. 2015). availability of host plants. Therefore, the When disturbed, BMSB nymphs and Origin and distribution influence of abiotic and biotic factors may adults hurriedly walk away, take flight play a significant role in determining Initial genetic comparisons detected (adults) or cease movement. These behav- BMSB establishment in regions where this low diversity among BMSB populations iors and the muted coloration of BMSB pest has arrived. in the United States (i.e., representative make it difficult to track and collect them The first BMSB detection in California insect specimens from 10 states, including in the environment when present at low was recorded in 2002, and populations are California) compared to BMSB popula- densities. This combination of traits also now established in at least nine counties. tions in Asia Although current BMSB populations are and identified Eggs 1st 2nd 3rd 4th 5th Male Female largely confined to urban areas, there is Beijing, China, risk of their movement into agricultural as the likely areas. Considering the evidence of BMSB origin of BMSB damage from the East Coast, researchers populations in California recognized a need to proac- in the United Mike Lewis All life stages (eggs, nymphs and adults) of BMSB. tively develop management strategies for States (Xu et BMSB in advance of potential infestations al. 2014). Follow-up molecular work being suggests that BMSB can readily reach (by in crop production areas. Seasonal moni- led by U.S. Department of Agriculture hitchhiking) and potentially colonize suit- toring for BMSB is essential in each detec- (USDA) researchers is adding further able new geographic areas. tion area to confirm whether populations resolution to the invasion origins of In California, reproductive popula- are established, characterize their yearly BMSB in the United States. Preliminary tions of BMSB have been known to oc- phenology and update statewide distribu- results suggest that there could have cur in Los Angeles County since at least tion maps (fig. 1), all of which are needed been multiple BMSB introductions into 2006. In fall 2013, reproductive BMSB the West Coast compared to the East populations were discovered in down- Coast. Including more BMSB samples town Sacramento (Ingels 2014; Varela and Del Norte from California as part of these analyses Elkins 2011). Tracking the spread of BMSB Siskiyou Modoc would help clarify whether the presence in California has been made possible of BMSB in California could have resulted through a network of monitoring traps, from accidental translocations from in- with more than 100 traps deployed during Trinity Shasta Lassen fested areas on the East Coast and intro- 2014 and 2015 by California Department Humboldt ductions from Asia as part of commerce of Food and Agriculture (CDFA), UC ANR Tehama Plumas and private activities. Cooperative Extension (UCCE), county Adult BMSB and developing instars agricultural commissioners and UC Mendocino Glenn Butte Sierra (second to fifth) have a relatively strong Riverside. In counties where BMSB popu-

YubaNevada Colusa Sutter Placer dispersal capacity. Nymphs can readily lations are established, trap collections Lake walk short distances (e.g., > 100 centime- suggest there are at least one, and likely Yolo El Dorado Sonoma Napa Sacra Alpine ters in less than 30 minutes on grassy two, BMSB generations per year in some mento Amador terrain and > 600 centimeters in areas of California, with peak activity oc- Marin Solano CalaverasTuolumne Contra San Mono 15 minutes on smooth plastic curring over summer. These monitoring Joaquin San Francisco Costa surfaces in the laboratory). efforts are ongoing and will help track Alameda Mariposa San Mateo Stanislaus Adult BMSB are ca- changes in BMSB phenology and geo- Santa Clara Merced pable of short (0- to graphic distribution in California. Madera Santa Cruz 5-kilometer) and Nuisance reports have been docu- San Inyo long-distance mented in Sacramento and Los Angeles Benito Fresno Tulare counties. Aggregation behavior typically Monterey Kings starts in late summer, with adult BMSB aggregating on outside walls as they seek San Luis refuge in garages, houses and apartment Obispo Kern blocks, for overwintering. This behavior Established San Bernardino is troublesome not only because of the Santa Barbara Detected inconvenience of having to clean up bugs Ventura Los Angeles and remove frass stains from surfaces, but also because of the pungent cilantro-like Riverside Orange stink BMSB produce. Growing concern San Diego Imperial Fig. 1. Known distribution of BMSB in California, As BMSB continues to spread to new as of December 2015. areas in California and populations build

16 CALIFORNIA AGRICULTURE • VOLUME 70, NUMBER 1 (A) (B) (C) Jesus Lara Jesus Lara Jesus Lara

(D) (E) (F) Jesus Lara Jesus Lara Jesus Lara

BMSB feeding on (A) apple, (B) grape, (C) pistachio, (D) Hass avocado, (E) green bean and (F) orange. up, there is warranted concern that this from BMSB infestations would increase al. 2014). Increased use of these pesticides polyphagous insect could become a pest the economic costs of invasive pests for can lead to secondary pest outbreaks on a variety of specialty crops in the state. California. and result in further economic losses. Metcalf (1995) estimated that established Nuisance problems associated with the California pest management programs invasive species cost California more than ability of BMSB to overwinter in human- could be similarly disrupted by BMSB if $3 billion per year (based on $100 per made structures and damage attributed populations spread to agricultural crops capita) in economic losses. When adjusted to BMSB feeding on crops, including and no effective and sustainable control for inflation to 2014 dollars and popula- apples, soybeans, tomatoes, peaches, measures are developed. tion census data (USCB 2015), the cost is corn, grapes and caneberries, have been There is a growing concern over BMSB approximately $6 billion. Crop damage documented in East Coast states (e.g., detections in agricultural areas in Oregon or quarantine trade restrictions resulting Delaware, Maryland, New Jersey, New on commercial crops such as hazelnuts, York, Pennsylvania, Virginia and West blackberries and wine grapes (Hansen Virginia) (Jentsch 2012; Leskey et al. 2012; and Mullinax 2014) and in Washington on Nielsen and Hamilton 2009; Pfeiffer et al. crops such as peppers, apples, peaches, 2012; Rice et al. 2014). The ability of BMSB plums and cherries (Eddy 2015). These to feed on a variety of crops explains the detections imply that if BMSB populations concern growers, researchers and the gen- continue to grow, they could eventually eral public have of its potential to cause have a significant economic impact on economic damage. Most notably, in 2010, agricultural production in this part of the apple growers in Mid-Atlantic states suf- country. One report of economic damage fered an estimated $37 million in losses by BMSB in the Pacific Northwest comes due to BMSB damage (Leskey et al. 2012). from a grower in Vancouver, Washington, As a result, pesticide applications for who attributed losses of apple to BMSB BMSB control increased, in some cases feeding (Hansen and Mullinax 2014). as much as fourfold. Some of these pesti- Although BMSB damage to commercial cides have broad-spectrum activity (e.g., agricultural crops has not been reported pyrethroids, neonicotinoids) for insects in California, the recovery of BMSB in fall and can be harmful to natural enemies 2014 from a monitoring trap in a Butte (Leskey et al. 2012; NIPMC 2014; Rice et County kiwi orchard (E. Symmes, area IPM advisor, UCCE Butte County, per- sonal communication) indicates that the A BMSB pheromone-based monitoring trap set up distribution of BMSB in California is still Jesus Lara in Los Angeles County. in transition.

http://californiaagriculture.ucanr.edu • JANUARY–MARCH 2016 17 Evidence of this distribution transition is being documented throughout the state (Warnert 2015). By September 2015, Siskiyou, Stanislaus and Yolo were added to the list of counties where BMSB is reproducing. In January 2016, CDFA confirmed the first detection of BMSB from trap samples collected during 2015 in Kern County, but it is not clear whether BMSB is established there; further monitoring in Kern County is planned for 2016. Establishment and detection of BMSB in several parts of the Sacramento Valley and San Joaquin Valley indicates that this pest has the potential to spread farther within California’s economically impor- Chuck Ingels tant Central Valley farming region, and Start of BMSB adult aggregation on an elm tree during August 2015 in Sacramento County. critical information on the types of crops that may be at risk is being documented problems caused by other exotic species field. Field surveys also revealed there as part of CDFA’s and UCCE’s monitoring for crops like citrus (under stress from are at least 12 North American species of efforts. Asian citrus psyllid and huanglongbing stink bug egg parasitoids (e.g., Anastatus During August and September 2015, disease) and avocado (threatened by the spp., Gryon sp., Ooencyrtus sp., Telenomus BMSB was found feeding on citrus, per- polyphagous shot hole borer and the spp. and Trissolcus spp.) in at least three simmons and apples in a Sacramento fungi it vectors). families (Encyrtidae, Eupelmidae, community garden. In July 2015 in Los Platygastridae) that parasitize sentinel Biological control research Angeles County, BMSB nymphs were (laboratory-sourced) BMSB egg masses found for the first time in traps placed in Field surveys in the United States deployed in the field (see Rice et al. 2014 close proximity to residential citrus, kiwi (i.e., Oregon, Delaware, Maryland, for complete species listing). and avocado trees; no external signs of Pennslyvania, Virginia) led by USDA These new host associations between damage to fruit attributable to BMSB were Agricultural Research Service (ARS) BMSB and resident parasitoid species will noted at those sites, but BMSB feeding and academic research institutions have need to be assessed experimentally for damage symptoms may take some time to documented evidence of host associa- their potential to provide some level of appear. tions between BMSB and resident natural natural BMSB control, as the presence of The full range of damage that could enemies. Several species of generalist resident natural enemies could comple- result from BMSB feeding is unknown predators (e.g., lacewings, mantids, ear- ment other promising BMSB biological for certain California crops that could be wigs, lady beetles, assassin bugs, minute control strategies. One of these strate- at risk. The addition of a polyphagous pirate bugs, big-eyed bugs and spiders) gies is classical biological control, under species and direct fruit-feeder like BMSB have been observed feeding on BMSB which a host-specific natural enemy could aggravate existing management egg masses and motile stages in the from the pest’s native range is reunited

(A) (B) (C) Chuck Ingels Chuck Ingels Charlie Pickett BMSB feeding on residential (A) persimmon, (B) apple and (C) citrus fruit in Sacramento County.

18 CALIFORNIA AGRICULTURE • VOLUME 70, NUMBER 1 Natural enemies Time-lapse photography from BMSB monitoring field sites in Sacramento su- pervised by CDFA in 2015 revealed that a generalist beetle, Laemostenus complanatus (Dejean) (Coleoptera: Carabidae), can feed on sentinel BMSB egg masses. L. complanatus is an adventive, or nonindig- enous, species whose presence has been documented in Northern and Southern California (Frank and McCoy 1995; SBNHM 2014; Sokolov and Kavanaugh 2014). In Southern California, predation of sentinel BMSB egg masses has been documented in Los Angeles County by UC Jesus Lara Riverside researchers; time-lapse photog- A Trissolcus japonicus female readily parasitizes raphy is planned to determine the identity eggs of BMSB in California. of predators. with the target pest in the introduced As part of the California BMSB Charlie Pickett range. To this end, Trissolcus japoni- monitoring program, traps baited with Adult Laemostenus complanatus opportunistically cus (Ashmead) and T. cultratus (Mayr) commercially available BMSB aggrega- feed at night on sentinel BMSB eggs deployed in Sacramento County. (Hymenoptera: Platygastridae) were tion pheromone during 2014 and 2015 sourced by USDA ARS Beneficial Insects also captured two specialized resident Introduction Research (ARS BIIR) from stink bug natural enemies: Euclytia flava and late-instar BMSB life stages on the parasitized BMSB eggs in Asia. These (Townsend) (Diptera: Tachinidae), a fly East Coast. species are under evaluation in quaran- that parasitizes motile stink bug life The impact these resident natural en- tine by USDA ARS BIIR as potential can- stages, and Astata spp. (Hymenoptera: emy species may have on BMSB popula- didates for classical biological control of Crabronidae), a wasp that attacks motile tion dynamics in California is yet to be BMSB in the United States. In Asia, levels stink bug stages. E. flava specimens were measured and may not be sufficient to of field parasitism of BMSB by T. japonicus captured in BMSB traps in Northern and provide adequate levels of population have been higher than T. cultratus (Haye Southern California. Astata spp. were suppression. For example, in the labora- 2014; Talamas et al. 2013), and this obser- captured from traps in Northern, Central tory E. flava has been successfully reared vation has directed the primary focus of and Southern California and species from P. maculiventris adults but not from classical biological control research on identifications are being confirmed. BMSB adults, even though E. flava females T. japonicus. Currently, all Astata specimens captured will lay eggs on BMSB. The contributions In California, UC Riverside and CDFA in Northern California have been identi- of other candidate resident species and have led research efforts since 2014 to fied as A. occidentalis Cresson, but field their potential impacts in agricultural ar- determine the potential of resident (i.e., observations in Sacramento demonstrate eas will need to be assessed as part of the native and naturalized species) and that adults of another species, A. unicolor emerging biological control program. promising foreign natural enemies (dem- Say, can attack BMSB and carry them Egg parasitoids onstrated to control BMSB in its home to their nest. Rice et al. (2014) reported range but not yet released in California) that Astata spp. and another parasitic fly, Understanding the suitability of BMSB for effective BMSB control. Field studies Trichopoda pennipes (Fabricius) (Diptera: eggs as a host for resident stink bug egg in Riverside, Los Angeles and Sacramento Tachinidae), were found attacking adult parasitoids is important. Ideally, this counties have documented resident natural enemies in California attacking BMSB egg masses, suggesting they may be useful for future management pro- Mike Lewis grams. Beginning in 2014, research at UC Jesus Lara Riverside focused on assessing the risk T. japonicus poses to native stink bugs, some of them beneficial predators such as the predatory stink bug Podisus maculiventris (Say). This nascent classical biological control program is being supported by UCCE, researchers at CDFA and USDA ARS, and some commodity boards (e.g., Euclytia flava, a native parasitoid of stink bugs, Astata species, a native predator of stink bugs, has been recovered from BMSB monitoring traps has been recovered from BMSB monitoring pear, pistachio and table grape). deployed in Los Angeles and Sacramento counties. traps in Los Angeles and Sacramento counties and parts of the Central Valley.

http://californiaagriculture.ucanr.edu • JANUARY–MARCH 2016 19 guild of natural enemies could provide TABLE 1. Some resident stink bug egg parasitoid California on cold-treated BMSB egg some level of control if they attack the species (Hymenoptera) found in California masses have not been always successful. first generation of BMSB egg masses laid Together, these observations highlight in the spring by female stink bugs coming Family Species the fact that some resident stink bug egg out of diapause. In California, there are at Encyrtidae Ooencyrtus californicus parasitoids may opportunistically exploit least 11 reported species of stink bug egg Ooencyrtus johnsoni BMSB eggs but ultimately may not be parasitoids (table 1). Egg parasitoid activ- Eupelmidae Anastatus pearsalli effective for controlling BMSB. Instead, ity is being monitored in Northern and Platygastridae Gryon obesum the establishment of a more host-specific Southern California by deploying sentinel BMSB egg parasitoid, like T. japonicus, as Psix tunetanus BMSB egg cards; eggs are killed by freez- part of a classical biological control pro- ing prior to deployment at field sites. Telenomus podisi gram may increase significantly parasit- During spring 2015, Anastatus pearsalli Trissolcus cosmopeplae ism of BMSB egg masses. Ashmead (Hymenoptera: Eupelmidae) Trissolcus basalis Classical biological control was recovered from one of more than 100 Trissolcus euschisti sentinel BMSB egg masses deployed in Trissolcus hullensis One possible factor contributing to the Sacramento. To our knowledge, this is the Trissolcus utahensis growing presence of BMSB in the United only reported Anastatus species associated Source: Ehler 2000. States may be the absence of host-specific, with stink bugs that occurs in this part of coevolved natural enemies from its home the state (Ehler 2000). Field data from the range. In China, T. japonicus can achieve East Coast suggests that A. pearsalli para- (UCR I&Q) facility to better assess the an average annual parasitism rate of 50%, sitism levels are low (around 4%) on BMSB suitability of BMSB as a developmen- but rates can range from 20% to 80% dur- eggs masses when compared to parasit- tal host for these natural enemies. The ing the field season (Lan-Fen 2007; Yang ism levels of another North American follow-up exposure experiments are nec- et al. 2009). These parasitism rates refer to congener, A. reduvii (Howard), which essary because freezing BMSB eggs prior the percentage of the egg mass attacked. caused 79% BMSB egg mass parasitism to field deployment likely disrupts their Other stink bug parasitoids associated at the same field study sites (Jones 2013). defense mechanisms and may make them with BMSB egg masses in China do not A. reduvii is a generalist parasitoid (Burks easier for nonspecialist egg parasitoids achieve parasitism rates higher than 10% 1967), and its occurrence in California to parasitize. Similar experiments were (Yang et al. 2009). These field data sug- needs to be investigated. conducted by Haye et al. (2015) in Europe gest that T. japonicus could be a promis- In Southern California, several sentinel with BMSB and native egg parasitoids ing candidate for classical biological egg cards from more than 100 deployed there. control of BMSB in the United States. Re- in Los Angeles County from June to The suitability of BMSB eggs for other establishing the trophic linkage between September 2015 were successfully parasit- California parasitoids reared from egg BMSB and T. japonicus in California at an ized by an unidentified Anastatus sp. and masses of resident stink bug species (e.g., early stage of this invasion may reduce other platygastrid parasitoids. Successful Banasa sp., Cholorochora sp. and Nezara pest densities and help mitigate nuisance parasitism of sentinel BMSB eggs has also viridula) or collected from sites with BMSB and agricultural problems caused by been observed in Riverside County, but pheromone traps is also being evaluated BMSB. BMSB has not established there. at the UCR I&Q facility. Field-collected T. Before T. japonicus can be deliberately Fresh BMSB egg masses are being basalis (Wollaston), T. utahensis (Ashmead) released for BMSB control in California exposed to resident parasitoids from and Telenomus ‘near’ podisi (Ashmead) and other parts of the United States, the Northern and Southern California at the have been exposed to fresh (24-hour-old) impact this egg parasitoid may have on UC Riverside Insectary and Quarantine BMSB egg masses in the laboratory. T. non-target stink bug species needs to be basalis collected from parts of France, assessed. One of the key components of Italy and Spain were introduced into parasitoid–host interactions for develop- California during the 1980s as a classical ing successful biological control programs biological control agent of another inva- is quantifying parasitism rates of para- 0.5 mm sive stink bug, Nezara viridula (Linnaeus) sitoid–host encounters. Consequently, a (Hoffmann et al. 1991). Levels of suc- variety of safety testing protocols (e.g., cessful parasitism of BMSB egg masses no-choice tests and choice tests described by these three candidate parasitoids are below) is being used to assess parasitism notably lower than those of T. japonicus levels by T. japonicus on BMSB in the con- under the same controlled conditions. text of potential non-target species. Furthermore, attempts to culture strains In California, T. japonicus is currently of these three resident species from reared in quarantine at UC Riverside on BMSB egg masses. Some of the representative non-target stink bugs being reared at UC Riverside for host range safety Anastatus pearsalli, a native species known to tests include Antheminia remota (Horváth), Serguei Triapitsyn Serguei parasitize BMSB egg masses in the United States. Agonoscelis puberula Stål, Banasa sp.,

20 CALIFORNIA AGRICULTURE • VOLUME 70, NUMBER 1 Bagrada hilaris (Burmeister), Chlorochroa Adult male platygastrid parasitoids, on guard, uhleri (Stål), P. maculiventris, Mecidea sp., N. wait for future female parasitoids to emerge from viridula and Thyanta sp. a parasitized sentinel BMSB egg card (parasitism indicated by dark color of eggs) that was deployed Safety testing is conducted in quaran- in Los Angeles County on avocado. tine and provides data on host use under highly artificial conditions as non-target species are exposed in vials, petri dishes to non-target species. These include the or small cages to candidate natural en- likelihood of natural encounters between emies. Laboratory experimental arenas T. japonicus and non-target species in the likely minimize the full range of cues environment. For example, there may be natural enemies use for locating hosts some climatic zones that support popula- and therefore facilitate determining the tions of non-target species in California, outcome of encounters. As part of the but these climatic conditions may rep- safety testing for T. japonicus, no-choice resent an establishment barrier to T. tests represent scenarios where a female japonicus, thus reducing risk of attack to Jesus Lara T. japonicus encounters an egg mass of non-target species. a single species stink bug (i.e., BMSB or Ecological niche modeling may help a non-target species) and the parasitoid delineate the potential distribution of T. results from each team are compiled by must decide whether to parasitize the host japonicus in California and reveal areas USDA ARS BIIR to provide a better un- egg mass. In choice tests, T. japonicus is where T. japonicus is likely to establish derstanding of potential non-target effects presented with egg masses of BMSB and and how likely populations of this natu- of T. japonicus across the United States. at least one non-target stink bug species to ral enemy will overlap with BMSB and Although safety testing is still in prog- elucidate its host preference. non-target stink bug populations. Under ress, preliminary results from no-choice Results from these types of tests are circumstances where some risk is deter- and choice studies at UC Riverside sug- used to quantify level of parasitoid emer- mined to be likely to some non-target spe- gest T. japonicus may have a preference gence, sex ratios, reproductive fitness of cies, a cost-benefit analysis will need to be for BMSB egg masses over egg masses of adults and other parameters that charac- conducted to guide the use of T. japonicus non-target species. Additional lab experi- terize the physiological host range and as a classical biological control agent of ments at Michigan State University by host specificity of T. japonicus. The physi- BMSB. Botch and Delfosse (2015) are under way ological host range refers to the number of Safety evaluations for T. japonicus are to provide further understanding of the species that can support the successful de- being spearheaded at the national level ecological host range of T. japonicus given velopment of T. japonicus and emergence by USDA ARS BIIR in Newark, Deleware, that added factors (i.e., the ability of the of adults from parasitized eggs; host with coordinated participation from other parasitoid to disperse between sites and specificity refers to the degree of prefer- states (e.g., California, Florida, Michigan its foraging success in different habitats) ence T. japonicus exhibits toward potential and Oregon). This team maintains an may moderate the level of interaction be- non-target species in the context of BMSB. open line of communication to design tween T. japonicus and non-target species, In addition, there are other key ele- science-driven biological control pro- thus reducing the risk to these species ments of host–parasitoid ecology influ- grams for BMSB specific to the regions even further. In 2016, UC Riverside ento- enced by the biology and ecology of each that individual members represent, and mologists plan to follow up on this line of interacting species that researchers are consequently, non-target stink bug species research on non-target stink bug species considering when assessing and interpret- from each region are being used in safety from California. ing risk by an introduced natural enemy tests with T. japonicus. Safety evaluation Interestingly, in fall 2014 and during 2015, field populations of T. japonicus were detected in Maryland (at three sites), Virginia (at one site) and Washington state

Jesus Lara (at one site) (HOL 2015; Talamas et al. 2015; Weiford 2015). Preliminary molecular analyses suggest that these field populations of T. japonicus were self-introduced separately on the West Coast and East Coast, possibly via parasitized BMSB egg masses on imported host plant material or hitchhiking adults entering the United

In California, the introduced egg parasitoid Trissolcus basalis parasitizes eggs of Nezara viridula (shown here) but its ability to successfully parasitize BMSB eggs is limited.

http://californiaagriculture.ucanr.edu • JANUARY–MARCH 2016 21 States (Acebes et al. 2015; Hoelmer and BMSB continues to be intercepted in coun- reflect a greater likelihood of BMSB estab- Dieckhoff 2015). ties where it may already reproduce. In lishment success in areas with a diversity The discovery of small populations of November 2015, adult BMSB were inter- of suitable host plants, such as Chinese T. japonicus on the East Coast and West cepted in urban areas in Orange County pistache (Pistacia chinensis), butterfly Coast does not preclude the need for and San Bernardino County and con- bush (Buddleja davidii) and tree of heaven California (and other states with BMSB firmed by entomologists at UC Riverside. (Ailanthus altissima), and an abundance of infestations) to complete the manda- overwintering sites such as human-made Future developments tory safety tests and submit host range structures. Urban areas may serve as year- and host specificity data to be included Data from monitoring efforts and round sources of BMSB populations; from in an environmental assessment report nuisance reports suggest the number them, adults could migrate to neighboring by USDA ARS. Furthermore, T. japoni- of reproductive BMSB populations and agricultural areas and once there establish cus cannot be moved across state lines their dispersal in California is increasing temporary populations that damage crops or purposefully released to facilitate its and this species has most likely not yet (Rice et al. 2014). dispersal without USDA Animal and achieved its full potential geographic dis- It is anticipated that biological control Plant Health Inspection Service (APHIS) tribution. At this time, the location of the will be an important component of a approval and the appropriate permits majority of discovered BMSB populations successful integrated pest management authorizing release. In the meantime, is limited to urban areas. In part, this may program for BMSB across various habitats (agricultural, urban and natural) where it may be difficult to implement spray programs targeting this pest as part of coordinated management efforts. Such programs would require costly, concerted efforts in searching, treating (with pesticides) and following up on the status of infestations on host plants that might harbor this pest. In this regard, biological control may be the only sustainable management solution for BMSB because stink bug parasitoids, native and introduced Agonoscelis Antheminia Bagrada species, are expected to have permanent, self-sustaining populations and could naturally disperse within habitats to effi- ciently find existing BMSB populations on host plants. Promoting biological control to lower BMSB populations in residential areas may reduce the size of adult populations invading houses and other buildings to overwinter, and in spring, when adult reproductive diapause breaks, fewer adults migrating out of urban areas in search of host plants could lessen pest pressure in agricultural areas. Banasa Chlorochroa Mecidea T. japonicus is a promising candidate for classical biological control of BMSB. Results of the safety testing, still in prog- ress, will be used to petition for its future release, in conjunction with other states. A general timeline for the completion of safety tests and the permit submission and approval process is still in development and will be influenced by results of safety evaluations. T. japonicus has yet to be found or released in California, but sentinel egg cards were deployed during 2014 and 2015 by CDFA and UC Riverside

Nezara Podisus Thyanta Mike Lewis to detect its possible arrival from locations within the United States or from Some exotic and native adult stink bugs (size not to scale) from California that are being used to Asia. Monitoring for T. japonicus will be determine host specificity of the BMSB egg parasitoid Trissolcus japonicus. expanded in California during 2016 and

22 CALIFORNIA AGRICULTURE • VOLUME 70, NUMBER 1 is expected to continue in other states References (e.g., Delaware, Virginia, Maryland, North Acebes A, Beers B, Bergh C, et al. 2015. Adventive popu- Lee DH, Short BD, Joseph SV, et al. 2013. Review of the Carolina, Washington). lations of Trissolcus japonicus, an Asian natural enemy biology, ecology, and management of Halyomorpha The multistate safety testing of T. ja- of Halyomorpha halys, in the USA. Poster presentation. halys (Hemiptera: Pentatomidae) in China, Japan, and 63rd Ann Entomol Soc of Am Meeting, Nov. 15–18, the republic of Korea. Environ Entomol 42(4):627–41. ponicus is essential, as it will help guide 2015. Minneapolis, MN. doi:10.1603/EN13006. future field studies by teams of research- Botch P, Delfosse ES. 2015. An endoparasitic egg hunt. Leskey TC, Short BD, Butler BR, Wright SE. 2012. Impact ers from each state (i.e., CDFA and Does habitat complexity mediate attack by Trissolcus of the invasive brown marmorated stink bug, Halyomor- japonicus (Hymenoptera: Platygastridae) on non-target pha halys (Stål), in Mid-Atlantic tree fruit orchards in the University of California) to monitor its stink bugs? Poster presentation. 63rd Ann Entomol Soc United States: Case studies of commercial manage- dispersal once it is approved for release of Am Meeting, Nov. 15–18, 2015. Minneapolis, MN. ment. Psyche 2012. doi:10.1155/2012/535062. or self-introduces, document its ecological Burks BD. 1967. The North American species of Ana- Metcalf R. 1995. Invasion of California by exotic pests. host range and measure its economic im- status Motschulsky (Hymenoptera, Eupelmidae). T Am Calif Agr 49(1):2. Entomol Soc 93(4):423–32. Nielsen AL, Hamilton GC. 2009. Seasonal occurrence pact on BMSB populations. In California, Cira TM, Venette RC, Aigner J, et al. 2016. Cold tolerance and impact of Halyomporpha halys (Hemiptera: Pen- safety testing with T. japonicus at UC of Halyomorpha halys (Hemiptera: Pentatomidae) across tatomidae) in tree fruit. J Econ Entomol 102(3):1133–40. Riverside may take another two to three geographic and temporal scales. Environ Entomol. doi:10.1603/029.102.0335. doi:10.1093/ee/nvv220. [NIPMC] Northeastern IPM Center. 2014. Chemical Con- years to complete. USDA ARS BIIR will Eddy D. 2015. Get Ready for Brown Marmorated Stink trols. www.stopbmsb.org/managing-bmsb/chemical- evaluate safety results from all research Bug in 2015. www.growingproduce.com/fruits/apples- controls/ (accessed Sept. 15, 2015). teams in the United States. At the same pears/get-ready-for-brown-marmorated-stink-bug- NIPMC. 2015. BMSB State-by-State Map. www. in-2015/ (accessed Sept. 1, 2015). time, the results of independent field work stopbmsb.org/where-is-bmsb/state-by-state/ (accessed Ehler LE. 2000. Farmscape Ecology of Stink Bugs in North- July 15, 2015). and laboratory studies led by CDFA and ern California. Lanham, MD: Entomological Society of Pfeiffer DG, Leskey TC, Burrack HJ. 2012. Threatening UC researchers is expected to elucidate America. p 59. the harvest: The threat from three invasive insects in the potential of resident natural enemies Frank JH, McCoy ED. 1995. Precinctive insect species in late season vineyards. In: Bostanian NJ, Vincent C, Isaacs Florida. Fla Entomol 78(1):21–35. doi:10.2307/3495663. R (eds.). Arthropod Management in Vineyards: Pests, Ap- to reduce BMSB populations in California. Hansen M, Mullinax TJ. 2014. Stinkbugs March on proaches and Future Directions. New York: Springer. p Data from these California projects will Washington. www.goodfruit.com/stinkbugs-march-on- 449–74. doi:10.1007/978-94-007-4032-7_19. be analyzed, and in conjunction with washington/# (accessed Sept. 1, 2015). Rice KB, Bergh CJ, Bergmann EJ, et al. 2014. Biology, ecology, and management of brown marmorated stink input from USDA ARS BIIR cooperators Haye T. 2014. Seasonal field parasitism of Halyomorpha halys and co-occurring non-target Species in China. bug (Hemiptera: Pentatomidae). J Integ Pest Manage on T. japonicus, the results will be used to Brown Marmorated Stink Bug Working Group Meeting, 5(3):A1–13. doi:10.1603/IPM14002. formulate a biological control program June 16, 2014. Georgetown, DE. [SBNHM] Santa Barbara Natural History Museum. 2014. The California Beetle Database. www.sbcollections.org/ for California that can be implemented in Haye T, Fischer S, Zhang J, Gariepy T. 2015. Can native egg parsitoids adopt the invasive brown marmorated cbp/cbpdatabase1.aspx (accessed April 18, 2015). residential and agricultural areas threat- stink bug, Halyomorpha halys (Heteroptera: Pentatomi- Sokolov IM, Kavanaugh DH. 2014. New records of ad- ened by BMSB infestations. c dae), in Europe? J Pest Sci 88:693–705. doi:10.1007/ ventive Carabidae (Coleoptera) found in California. Pan- s10340-015-0671-1. Pac Entomol 90(2):66–71. doi:10.3956/2014-90.2.66. Hoelmer KA, Dieckhoff C. 2015. Implementing a classi- Talamas EJ, Herlihy MV, Dieckhoff C, et al. 2015. Tris- cal biological control program for brown marmorated solcus japonicus (Ashmead) (Hymenoptera: Scelionidae) stink bug. Brown Marmorated Stink Bug Working Group: emerges in North America. J Hymenopt Res 43:119–28. J. Lara is Postdoctoral Scholar in the Department Synergizing IPM Research to Deliver Solutions. 63rd Ann doi:10.3897/JHR.43.4661. of Entomology at UC Riverside; C. Pickett is Senior Entomol Soc of Am Meeting, Nov. 15–18, 2015. Min- [USCB] United States Census Bureau. 2015. Annual neapolis, MN. Environmental Research Scientist at California Estimates of the Resident Population: April 1, 2010, to Hoffmann MP, Davidson NA, Wilson LT, et al. 1991. Im- July 1, 2014. factfinder.census.gov/faces/nav/jsf/pages/ Department of Food and Agriculture, Sacramento; C. ported wasp helps control southern green stink bug. index.xhtml (accessed Sept. 1, 2015). Ingels is UC ANR Cooperative Extension (UCCE) Farm Calif Agr 45(3):20–2. Varela LG, Elkins RB. 2011. New pest threat in orchards Advisor in Sacramento County; D.R. Haviland is UCCE [HOL] Hymenoptera Online. 2015. Trissolcus japoni- — Brown marmorated stink bug. CAPCA Adviser Farm Advisor in Kern County; E. Grafton-Cardwell cus General Information. http://hol.osu.edu/index. 15:32–3. is UCCE Entomology Specialist at UC Riverside and html?id=3249 (accessed Sept. 1, 2015). Warnert J. 2015. Brown Marmorated Stink Bug Found in Director of Lindcove Research and Extension Center; D. Ingels C. 2014. Brown marmorated stink bug update. Stanislaus County. ucanr.edu/blogs/blogcore/postdetail. Doll is UCCE Farm Advisor in Merced County; J. Bethke CAPCA Adviser 17(2):42–4. cfm?postnum=18597 (accessed Aug. 28, 2015). is UCCE Farm Advisor in San Diego County; B. Faber Jentsch P. 2012. Brown Marmorated Stink Bug in the Weiford L. 2015. New ‘Alien’ Wasp Discovered in Wash- is UCCE Farm Advisor in Santa Barbara and Ventura Hudson Valley. https://grapesandwine.cals.cornell.edu/ ington State. news.wsu.edu/2015/10/22/new-alien- newsletters/appellation-cornell/2012-newsletters/is- wasp-discovered-in-washington-state/#.VkUsmnarSUk counties; S.K. Dara is Strawberry and Vegetable Crops sue-12 (accessed Jan. 14, 2016). (accessed Nov. 12, 2015). Advisor and Affiliated IPM Advisor in San Luis Obispo, Jones AL. 2013. Indigenous Natural Enemies of the In- Wiman NG, Walton VM, Shearer PW, et al. 2015. Factors Santa Barbara and Ventura counties; M. Hoddle is UCCE vasive Brown Marmorated Stink Bug, Halyomorpha halys affecting flight capacity of brown marmorated stink Entomology Specialist at UC Riverside. (Hemiptera: Pentatomidae). Master’s thesis, Department bug, Halyomorpha halys (Hemiptera: Pentatomidae). J We thank the California Department of Food of Entomology, University of Maryland, College Park. Pest Sci 88(1):37–47. doi:10.1007/s10340-014-0582-6. and Agriculture Specialty Crop Block Grant Program, Lan-Fen Q. 2007. Studies on biology of the brown mar- Xu J, Fonseca DM, Hamilton GC, et al. 2014. Tracing the USDA Farm Bill, California Pistachio Research Board morated stink bug Halyomorpha halys (Stål) (Hemiptera: origin of US brown marmorated stink bugs, Halyomor- Pentatomidae), an important pest for pome trees in pha halys. Biol Invasions 16(1):153–66. doi:10.1007/ and Consolidated Central Valley Table Grape Pest and China and its biological control. Ph.D. dissertation, Chi- s10530-013-0510-3. Disease Control District for financial support of BMSB nese Academy of Forestry, Beijing. Yang ZQ, Yao YX, Qiu LF, Li ZX. 2009. A new species of biological control research. We also thank Marypat Lee DH, Nielsen AL, Leskey TC. 2014. Dispersal capacity Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs Stadtherr, Stephanie Rill, Jamie Nemecek, Minerva and behavior of nymphal stages of Halyomorpha halys of Halyomorpha halys (Heteroptera: Pentatomidae) in Gonzalez, Monty Lo, Fritz Light, Bryan Vander May, Cort (Hemiptera: Pentatomidae) evaluated under labora- China with comments on its biology. Ann Entomol Soc tory and field conditions. J Insect Behav 27(5):639–51. Am 102(1):39–47. doi:10.1603/008.102.0104. Hurley, Viola Popescu, Matt Jones, Matthew Kamiyama, doi:10.1007/s10905-014-9456-2. Gabriel Hernandez, Joshua Oliva, Vincent Jones, Jim Henrich, Tim Thibault and Dan Berry for assistance with BMSB monitoring. Special thanks to James Liebherr, Martin Hauser, Serguei Triapitsyn and Gary Gibson for assisting with insect identification.

http://californiaagriculture.ucanr.edu • JANUARY–MARCH 2016 23