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 es- tablishment (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