Review of the Biology, Ecology, and Management of Halyomorpha Halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea
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POPULATION ECOLOGY Review of the Biology, Ecology, and Management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea DOO-HYUNG LEE,1,2 BRENT D. SHORT,1 SHIMAT V. JOSEPH,3,4 J. CHRISTOPHER BERGH,3 1 AND TRACY C. LESKEY Environ. Entomol. 42(4): 627Ð641 (2013); DOI: http://dx.doi.org/10.1603/EN13006 ABSTRACT Native to China, Japan, Korea, and Taiwan, the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) was Þrst detected in the United States in the mid-1990s. Since establishing in the United States, this invasive species has caused signiÞcant economic losses in agriculture and created major nuisance problems for home and business owners, especially in the mid-Atlantic region. Basic and applied questions on H. halys have been addressed in its native range in Asia since the mid-1900s and the research outcomes have been published in at least 216 articles from China, Japan, and the Republic of Korea. In Asia, H. halys is described as an occasional or outbreak pest of a number of crops such as apple, pear, persimmon, and soybeans. This species is considered a nuisance pest as well, particularly in Japan. This review summarizes 100 articles primarily translated from Chinese, Japanese, and Korean to English. The content of this review focuses on the biology, ecology, and management of H. halys in Asia, with speciÞc emphasis on nomenclature, life history, host range, damage, economic importance, sampling and moni- toring tools, and management strategies. This information from the native range of H. halys provides greater context and understanding of its biology, ecology, and management in North America. KEY WORDS brown marmorated stink bug, invasive species, Asia The brown marmorated stink bug, Halyomorpha halys large numbers of invading adults subsequently over- (Stål) (Hemiptera: Pentatomidae), is an invasive spe- wintering in human-made structures (Hamilton 2009, cies native to China, Japan, Korea, and Taiwan (Hoe- Inkley 2012). beke and Carter 2003). First discovered in the United Basic and applied studies of Halyomorpha spp. in States in the mid-1990s in or near Allentown, PA (Hoe- Asia have been reported in at least 216 articles from beke and Carter 2003), the distribution of H. halys has China, Japan, and the Republic of Korea since the grown steadily and, as of 2013, it had been ofÞcially mid-1900s (e.g., Sasaki 1905; K. Funayama, personal detected in 40 states, the District of Columbia (www. communication) (Fig. 1; Supp. 1 and 2 [online only] stopbmsb.org), Hamilton, Ontario, Canada (Fogain for annotated bibliographies). The number of publi- and Graff 2011), Switzerland (Wermelinger et al. cations from Asia on Halyomorpha spp. has increased 2008), Liechtenstein (Arnold 2009), Germany (Heck- rapidly since the 1970s. However, only Ϸ15% of these mann 2012), and France (Callot and Brua 2013). Based publications were written entirely in English, while on climatic data, Zhu et al. (2012) predicted that the the rest were entirely in Asian languages or had partial eastern, central, and portions of the paciÞc northwest English text (e.g., abstract, tables, Þgure captions, and of the United States are favorable for widespread es- references). Consequently, this review encompasses tablishment of H. halys. Indeed, this invasive species information from a selection of publications from has emerged as a key pest in tree fruit in the mid- China, Japan, and the Republic of Korea. Of the Atlantic region, with damage reported on vegetables, known publications, 100 articles were selected for row crops, ornamentals, and potential risks to small inclusion in this review, based on their citation record fruit and grapes (Leskey et al. 2012). In addition, H. and breadth of scope. In this review article, we sum- halys has become a serious nuisance because of the marized information on H. halys published from Asia on the following topics: nomenclature, life history, host range, damage economic importance, sampling 1 U.S. Department of AgricultureÐAgriculture Research Service, Appalachian Fruit Research Station, 2217 Wiltshire Rd., Kear- and monitoring tools, and management strategies. neysville, WV 25430-2771. 2 Corresponding author, e-mail: [email protected]. 3 Department of Entomology, Virginia Tech, AHS AREC, 595 Lau- Nomenclature rel Grove Rd., Winchester, VA 22602. 4 Current Address: University of California Cooperative Extension, H. halys has had a confusing nomenclatural record, 1432 Abbott St., Salinas, CA 93901. having previously been referred to as H. mista or H. 0046-225X/13/0627Ð0641$04.00/0 ᭧ 2013 Entomological Society of America 628 ENVIRONMENTAL ENTOMOLOGY Vol. 42, no. 4 Fig. 1. Number of articles on Halyomorpha halys published by decade in China, Japan, and the Republic of Korea. brevis (synonyms), and H. picus (misidentiÞcation) 126Њ 31Ј E) and is reported to complete up to two (Rider et al. 2002). Ultimately, Josifov and Kerzhner generations in southern portions of the country (Bae (1978) determined that only one species of Halyo- et al. 2008, 2009). H. halys is also widely distributed morpha, H. halys, is present in eastern China, Japan, across Japan, and tends to be the principal species in and Korea. Therefore, all references to Halyomorpha cooler regions (Adachi et al. 2007). In Japan, one or spp. from these locations are considered synonymous two generations have been reported based on anec- with H. halys (Rider et al. 2002). In this review article, dotal evidence, as well as laboratory and Þeld studies we followed this nomenclatural veriÞcation. (Saito et al. 1964, Watanabe et al. 1978, Oda et al. 1980, Yanagi and Hagihara 1980, Kawada and Kitamura 1983a, Fujiie 1985, Katayama et al. 1993, Funayama Life History 2008). Watanabe (1980) suggested that H. halys is Studies of the life history and seasonal population univoltine and bivoltine in western and eastern Japan, dynamics of H. halys on economically important crops respectively, though no supporting data were pre- and in adjacent unmanaged landscapes have generally sented. revealed one or two generations in its native range in Overwintering Adults. H. halys adults begin moving Asia. The life history of H. halys has been described to overwintering sites in September (Saito et al. 1964, primarily based on the univoltine populations in the Kobayashi and Kimura 1969, Kawada and Kitamura studies reviewed here, although limited phenological 1992) (Fig. 3). This activity was reported to increase information of bivoltine H. halys populations is in- by mid-October (Qin 1990, Zhang et al. 1993) and to cluded. We have also incorporated results of studies continue into November (Kobayashi and Kimura focused on effects of photoperiod, temperature, and 1969, Watanabe et al. 1978, Yanagi and Hagihara 1980, diet on H. halys reproduction, development, survivor- Zhang et al. 1993, Funayama 2012b). The majority of ship, and diapause. H. halys become inactive below 9ЊC (Li et al. 2007). Distribution and Voltinism. In China, one or two Aggregations of adults are found in dark locations in generations of H. halys are commonly present (Qin overwintering sites and, once settled, the individuals 1990, Zhang et al. 1993, Li et al. 1996; as reviewed by are unlikely to leave (Toyama et al. 2011) unless stored Yu and Zhang 2007, Chu et al. 1997), although Hoff- nutrients in the fat body are depleted (Funayama man (1931) suggested that four or even six generations 2012b). Toyama et al. (2006) suggested that aggrega- may occur in the Kwangtung (Guangdong) province tions were the result of adults responding to tactile (23o N, 113o E) (Fig. 2). Bivoltine populations in and/or olfactory cues, but not visual cues. H. halys are China begin ovipositing in mid- to late May (Wang and commonly found overwintering in human-made Wang 1988, Zhang et al. 1993, Qiu 2007). Following structures (Kobayashi and Kimura 1969, Yanagi and these overwintered adults, Þrst generation adults be- Hagihara 1980, Watanabe et al. 1994c, Funayama gin to lay eggs from late June to early July (Qin 1990) 2003). Qin (1990) reported that more H. halys ßew to or mid- to late-July (Zhang et al. 1993, Qiu 2007), with the west-facing portion of buildings than other cardi- second generation adults observed between late Au- nal directions. Overwintering adults have also been gust (Qiu 2007) and early to mid-September (Qin reported in natural landscapes in litter and tree holes 1990, Zhang et al. 1993). H. halys has not been reported (Qin 1990), under the bark of cedar trees (Ueno and from Xinjiang (42Њ N, 85Њ E), Ningxia (37Њ N, 106Њ E), Shoji 1978a), and in dry, high elevation mountain Qinghai (35Њ N, 96Њ E), or Tibetan (32Њ N, 89Њ E) terrain (Wang and Wang 1988). provinces of China (as reviewed by Yu and Zhang Survivorship of overwintering H. halys has been 2007). H. halys has been found across the Republic of examined in relation to temperature. Kiritani (2007) Korea, including the southern island of Jeju (33Њ 25Ј N, cited a report (Plant Protection Division, MAFF 1986) August 2013 LEE ET AL.: REVIEW OF ASIAN LITERATURE ON Halyomorpha halys 629 Fig. 2. Number of generations of Halyomorpha halys reported in Asia. Numbers in the Þgure correspond to the following references: 1Bae et al. 2008; 2Chu et al. 1997; 3Fujiie 1985; 4Funayama 2008; 5Hoffmann 1931; 6Hou et al. 2009; 7Katayama et al. 1993; 8Kawada and Kitamura 1983a; 9Oda et al. 1980; 10Qin 1990; 11Saito et al. 1964; 12Watanabe et al. 1978; 13Yanagi and Hagihara 1980; 14Yang et al. 2009; 15Zhang et al. 1993. Map is not to scale. that related H. halys overwintering mortality to mean Funayama 2002a, Qiu 2007, Cai et al. 2008). Some temperatures in January and February, and concluded authors reported that adults exiting overwintering that each 1ЊC rise above 4ЊC would result in a 13.5% sites temporarily use host plants such as Chinese ar- increase in survivorship.