Halyomorpha halys has expanded its invasive range in the USA southward into Georgia, but prior to 2018 established reproducing populations have not been reported in Florida. Yellow pyramid traps placed in peach orchards detected adult H. halys in 2016, 2017, and 2018, with the number of positive sites and specimens captured increasing each year. During 2018, nymphs and eggs of H. halys were observed at a peach orchard in Lake County, Florida. This represents the first evidence of a reproducing population of H. halys in Florida. The range expansion into Florida is the lowest latitude observed in the invasive range of H. halys, suggesting this temperate species may be able to overcome the barriers to range expansion posed by the temperature and photoperiod regimes found at lower latitudes.
The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), has emerged as one of the most significant invasive pests worldwide (Haye et al. 2015). Halyomorpha halys is native to eastern Asia, from Korea and Japan south to Taiwan and the Indian subcontinent. First collected in North America in 1996 near Allentown, Pennsylvania, H. halys has spread throughout much of the USA and Canada (Hoebeke & Carter 2003; Leskey et al. 2012). Globally H. halys has become an invasive pest in Europe, from Switzerland and Liechtenstein eastward through the Balkans and into Russia and Georgia within the last decade (Wermelinger et al. 2008; Musolin et al. 2017). The only established population reported from South America is present in Chile (Faúndez & Rider 2017). While not present in Australia or New Zealand, H. halys has been intercepted numerous times on shipments bound for these countries and is considered to be a pest of regulatory concern (Duthie et al. 2012).
In temperate climates H. halys moves into sheltered areas or human structures such as homes and vehicles to overwinter. This overwintering behavior has increased the human-facilitated spread of H. halys, contributing significantly to its widespread distribution and invasive pest status (Hoebeke & Carter 2003; Gariepy et al. 2014). In Florida, H. halys frequently has been intercepted on vehicles moving south during the fall or winter from states with established H. halys populations. The extremely high propagule pressure suggests a significant likelihood of H. halys establishment in Florida; however, prior to the 2016 to 2018 survey of stink bugs in Florida peach orchards, there has been no evidence of H. halys establishment in Florida.
From 2016 to 2018, a survey of stink bug pests in Florida's subtropical peach industry was conducted. Yellow pyramids traps were deployed at peach orchards in Lake County (2 sites), Polk County (1 site), and St. Lucie County (2 sites), with the goal of providing representative coverage of Florida's developing subtropical peach industry (Fig. 1). Yellow pyramid traps were constructed following methods similar to Leskey and Hogmire (2005). Traps were baited with a multi-species stink bug pheromone lure (AgBio, Westminster, Colorado, USA) and checked biweekly from Jan to Jun.
Two orchards in Lake County, Florida, USA, were monitored during the 2016 to 2018 peach seasons. Lake County Site 1 (Lake Co. 1) was a small planting (less than 0.4 ha) of peaches. Three yellow pyramid traps were placed at Lake Co. 1 each year during the survey period. Lake County Site 2 (Lake Co. 2) was a larger planting (approximately 2 ha). A total of 5 yellow pyramid traps were placed at Lake Co. 2 during 2016, with the trap number increased to 7 during the 2017 and 2018 seasons. The 2 Lake County sites were approximately 3.65 km apart, with similar surroundings including citrus and pine plantings, as well as rural and residential land use. Both Lake County locations were certified organic and experienced minimal pest control intervention.
The Polk County site was located near Lake Alfred, Florida, USA. The orchard is approximately 6.9 ha and is situated in a residential area. Two moderate sized lakes are present on either side of the orchard. The primary agriculture in the area is citrus, with large groves several km away. A total of 10 traps were placed at the Polk Co. orchard.
Of the 2 orchards monitored in St. Lucie County, the northernmost site (St. Lucie Co. 1) had over 48.5 ha under cultivation, and the block monitored during the survey was approximately 4 ha, bordered by adjacent peach blocks on 3 sides, and a mowed grass lawn on the fourth side. A total of 5 yellow pyramid traps were deployed at this site in 2016, increasing to 7 traps in 2017 and 2018. The second St. Lucie county site, St. Lucie Co. 2, measured approximately 4 ha and was surrounded by citrus on the south, pasture on the north and east, and a small wooded area on the western side. Similar to St. Lucie Co. 1, trap density at St. Lucie Co. 2 increased from 5 traps in 2016 to 7 traps in 2017 and 2018. Chemical pest management was aggressive at both St. Lucie County sites during the survey period, reflective of a relatively high population of Euschistus servus (Say) (Hemiptera: Pentatomidae) in the area.
The survey detected adult H. halys in all 3 yr (2016–2018) as shown in Table 1. The discovery of adult H. halys in peach orchards represents the first detection of this species from an agricultural setting in Florida. Specimens were identified in the field, and confirmed by Susan Halbert at the Florida Department of Agriculture and Consumer Services, Division of Plant Industry. Voucher specimens were deposited in the Florida State Collection of Arthropods in Gainesville, Florida, USA. Adult females were dissected to determine reproductive status following the method of Penca and Hodges (2017). Of the 11 female brown marmorated stink bug dissected, 6 were gravid, 4 had clear oocyte development indicative of a post-diapause status, and 1 had regressed ovaries indicating diapause (Table 1). Gravid females were detected as early as mid-Feb, and continued to be observed into Jun, suggesting a large window for potential reproduction in Florida. Because adult detections may be the result of “hitchhiking” individuals on vehicles or other items transported from states with established populations, the repeated detection of adults in consecutive years at 3 separate sites (Lake Co. 1, Lake Co. 2, Polk Co.), while significant, does not provide conclusive evidence of establishment.
In 2018, the detection of 3 nymphs and 2 egg masses at 1 of the field sites (Lake Co. 2) represented the first observation of reproduc tion in Florida. Nymphal specimens and egg clutches were detected by visual survey within the vicinity of a baited yellow pyramid trap. Within the state of Florida, the Florida Department of Agriculture and Consumer Services, Division of Plant Industry is the plant protection agency with the regulatory authority to determine pest status. The Florida Department of Agriculture and Consumer Services, Division of Plant Industry has declared previous reports of adult H. halys as interceptions per the International Plant Protection Convention glossary of phytosanitary terms (IPPC 2007). The repeated detection of adult H. halys in 2016, 2017, and 2018, and the detection of reproductive stages in 2018 suggests H. halys is likely established at the Lake County 2 site. As such, the Lake County population of H. halys has been declared a pest incursion of limited distribution by the Florida Department of Agriculture and Consumer Services, Division of Plant Industry.
The extent of H. halys establishment in Florida is unknown due to limited survey and trapping efforts. The nearest recorded reproductive populations are in central Georgia, several hundred km from the Lake County, Florida, population. Considering the frequent interceptions of H. halys in Florida on travelers and at the agricultural interdiction stations, it is assumed that the Lake County population was introduced via human activity, and not through the natural spread of H. halys southward from Georgia. While H. halys is most abundant in temperate areas, its native range includes subtropical parts of China (Lee et al. 2013). In temperate areas the reported photoperiod required for diapause termination was estimated at 12.7 h (Nielson et al. 2017). The discovery of gravid females as early as mid-Feb, when the daylength is below 11.5 hours, suggests that cues directing diapause in H. halys may be less rigid than previously considered and may not pose a barrier to the expansion of this species into lower latitudes. Sustained monitoring of populations in Florida will provide more information on the ability of H. halys to expand its invasive range into subtropical regions.
Record of Halyomorpha halys capture in Florida peach orchards, 2016–2018.
The authors acknowledge Susan Halbert, Florida Department of Agriculture and Consumer Services for confirming the specimen identifications. The authors acknowledge Jennifer Carr, laboratory manager for the University of Florida, Entomology and Nematology Department, Biosecurity, Research, and Extension Laboratory for her assistance with trap construction and other logistical components of the survey. Partial funding for the pest survey was provided by “a survey of Hemipteran cat-facing insects and plum pox virus in Florida's emerging ‘low-chill’ peach industry,” funded by the USDA-APHIS-PPQ Farm Bill FY2017 Cooperative Agreement Number award number AP17PPQFO000C148. Partial funding for the pest survey also was provided by the USDA-NIFA Southern Regional IPM Center at North Carolina State University through award no. 2014-70006-22485 and titled “foundational research for the development of IPM in Florida's subtropical peach industry.”
- Duthie CD, Michael T, Stephenson B, Yamoah E, McDonald B. 2012. Risk analysis of Halyomorpha halys (brown marmorated stink bug) on all pathways.Biosecurity Risk Analysis Group, Ministry of Agriculture and Forestry of New Zealand, Wellington, New Zealand. Google Scholar
- Faúndez EI, Rider D. 2017. The brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) in Chile.Arquivos Entomolóxicos17: 305–307. Google Scholar
- Gariepy TD, Haye T, Fraser H, Zhang J. 2014. Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland.Journal of Pest Science87: 17–28. Google Scholar
- Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, Tassus X, Desneuz N. 2015. Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit, and vegetable crops worldwide.Journal of Pest Science88: 665–673. Google Scholar
- Hoebeke ER, Carter ME. 2003. Halyomorpha halys (Stål) (Heteromoptera: Pentatomidae): a polyphagous plant pest from Asia newly detection in North America.Proceedings of the Entomological Society of Washington105: 225–237. Google Scholar
- IPPC - International Plant Protection Convention.2007. Glossary of Phytosanitary Terms. International Standards for Phytosanitary Measures.Food and Agriculture Organization of the United Nations, Rome Italy. https://www.ippc.int/en/publications/glossary-phytosanitary-terms/ (last accessed 6 Jul 2018). Google Scholar
- Lee DH, Short BD, Joseph SV, Bergh JC, Leskey TC. 2013. Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea.Environmental Entomology42: 627–641. Google Scholar
- Leskey TC, Hogmire HW. 2005. Monitoring stink bugs (Hemiptera: Pentatomidae) in mid-Atlantic apple and peach orchards.Journal of Economic Entomology98: 143–153. Google Scholar
- Leskey TC, Short BD, Butler BR, Wright SE. 2012. Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), in mid-Atlantic tree fruit orchards in the United States - case studies of commercial management.Psyche: A Journal of Entomology2012: 1–14. Google Scholar
- Musolin DL, Konjević A, Karpun NN, Protsenko VY, Ayba LY, Saulich AK. 2017. Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in Russia, Abkhazia, and Serbia: history of invasion, range expansion, early stages of establishment, and first records of damage to local crops.Arthropod-Plant Interactions12: 517–529. Google Scholar
- Nielsen AL, Fleischer S, Hamilton GC, Hancock T, Krawczyk G, Lee JC, Ogburn E, Pote JM, Raudenbush A, Rucker A, Saunders M, Skillman VP, Sullivan J, Timer J, Walgenbach J, Wiman NG, Leskey TC. 2017. Phenology of the brown marmorated stink bug described using female reproductive development.Ecology and Evolution7: 6680–6690. Google Scholar
- Penca C, Hodges A. 2017. Pyriproxyfen treatment terminates Halyomorpha halys reproductive diapause, with an indirect mortality effect on its egg parasitoid Trissolcus japonicus.Journal of Pest Science90: 1269–1276. Google Scholar
- Wermelinger B, Wyniger D, Forster B. 2008. First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on wood ornamentals and fruit trees?Bulletin de la Société Entomologique Suisse81: 1–8. Google Scholar