First Report of Seasonal Trap Capture for Halyomorpha halys (Hemiptera: Pentatomidae) and Native Stink Bugs in Central Georgia

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is native to China, Taiwan, Korea, and Japan. Unfortunately, this invasive insect pest has spread to the United States, Canada, Switzerland, and Europe (Lee et al. 2013, Environ. Entomol. 42: 627–641). It is both an urban nuisance, due to its propensity for overwintering in structures (Inkley 2012, J. Entomol. Sci. 47: 125–130), and a serious economic pest of orchard crops, including apples and peaches, row crops such as field corn and soybeans, and vegetable crops including sweet corn, peppers, eggplant, and tomatoes (Leskey et al. 2012a, Psyche. DOI: 10.1155/2012/535062; Leskey et al. 2012b, Outlooks on Pest Manage. 23: 218–226; Rice et al. 2014, J. Integr. Pest Manag. 5: 1–13). The first known H. halys populations in the United States were reported in 1996 from Allentown, PA. To date, H. halys is present in 43 states and four Canadian providences (StopBMSB 2017, Stopbmsb.org).

In Georgia, urban pest management professionals began reporting overwintering H. halys aggregations in the metropolitan Atlanta area in 2011. In late August 2014, H. halys adults and 2nd through 5th instars were collected from a Euschistus spp. pheromone-baited stink bug trap at the University of Georgia Horticulture Farm near Watkinsville, GA (P.G.T. unpubl. data). When the immediate area was searched, H. halys nymphs and adults were found on catalpa, pecan, and ornamental hibiscus. In the summer of 2015, H. halys was collected feeding and reproducing on soybean in Pike Co. (Piedmont region) (G.D.B. unpubl. data) and on peaches and pecan in Peach Co. (Coastal Plain region) (T.E.C. unpubl. data). Currently, H. halys is considered an agricultural and nuisance pest in Georgia.

In Georgia, native stink bugs (Hemiptera: Pentatomidae)—mainly the green stink bug, Chinavia hilaris (Say); the brown stink bug, Euschistus servus (Say); the dusky stink bug, Euschistus tristigmus (Say); the red-shouldered stink bug, Thyanta custator custator (F.); and the southern green stink bug, Nezara viridula (L.)—are economic pests in most fruit, grain, vegetable, and row crops (McPherson and McPherson 2000,Stink Bugs of Economic Importance in America North of Mexico, CRS Press, New York, NY). In cotton, stink bugs feed on developing seeds and lint of cotton, causing shedding of young bolls, yellowing of lint, yield reduction, and transmission of a bacterial pathogen (Barbour et al. 1990, J. Econ. Entomol. 83: 842–845; Medrano et al. 2009, J. Econ. Entomol. 102: 36–42). In soybean, pod-feeding by stink bugs results in reduction in oil content and yield (McPherson et al. 1995, J. Entomol. Sci. 30: 216–236). Adult stink bugs are known to feed on and damage nuts of pecan (Yates et al. 1991, J. Am. Soc. Hort. Sci. 116: 42–46). Murgantia histrionica (Hahn), the harlequin bug, is an important pest of crucifer crops in Georgia (Miller 1971, J. Econ. Entomol. 6: 255–257). It feeds on plant sap resulting in wilting, browning, and eventual death (Ludwig and Kok 2001, Crop Prot. 20: 247–251).

With the expansion of H. halys into Georgia, this invasive pest can co-occur with native stink bug species in agricultural crops. Therefore, a study was conducted to monitor H. halys, as well as native stink bugs, using pheromone-baited traps placed near woodland field edges at a field crop farm in 2016.

This study was conducted at the University of Georgia Bledsoe Research Farm (N 33°17′74″, W 84°40′76″) in Pike Co., GA, in 2016. Four field crops, wheat, corn, soybean, and sorghum, were grown on the 82.6-ha farm. Black pyramidal traps (plum curculio trap base, Great Lakes IPM, Vestaburg, MI) baited with the Stink Bug Xtra Combo lure, i.e., the H. halys aggregation pheromone lure plus a methyl (E,E,Z)-2,4,6-decatrienoate lure (AgBio Inc., Westminster, CO), were used to sample H. halys and other attracted stink bug species. The insect-collecting device was made from a 2.8-L clear plastic PET^® jar (United States Plastic Corp., Lima, OH) with a screw-cap lid (10.2 mm in diameter) and seated atop the 1.22-m-tall pyramid base (Cottrell et al. 2000, J. Entomol. Sci. 35: 421–431). An insecticidal ear tag (10% λ-cyhalothrin and 13% piperonyl butoxide) (Saber Extra insecticide ear tags, Jeffers, Dothan, AL) was placed in the collecting device to kill stink bugs (Cottrell 2001, Florida Entomol. 84: 731-732). Insertion of small eyelets in the lid of the insect-collecting device allowed some smaller, nontarget species (e.g., stink bug parasitoids), but not stink bugs, to escape (Tillman et al. 2015, J. Econ. Entomol. 108: 2324–2334). Eight pheromone-baited stink bug traps were positioned around the woodland field borders of the farm. The minimum distance between traps was 110 m. The woodland habitat was composed of mixed pine, oak, and hickory with a few black cherry trees. Pheromone lures were replaced biweekly. Stink bugs were collected weekly in Ziploc^® bags and taken to the laboratory for identification. Percentage of parasitism of stink bug adults in traps also was determined. Stink bugs were monitored from the week of 16 May to 5 December. Voucher specimens of stink bug species were deposited in the USDA, Agricultural Research Service, Crop Protection and Management Research Laboratory in Tifton, GA. Chi-square analyses were used to compare frequencies of stink bug species in pheromone-baited traps overall and individually using PROC FREQ (SAS Institute 2012, SAS/STAT user's guide, version 9.3. SAS Institute, Cary, NC).

In addition, 35–40 plants were sampled for stink bugs along a field edge of corn on 28 July and 4 August; no insecticide was applied to the field edge. A soybean field at the farm was divided into 12 19.2 × 30.5–m plots; no insecticide was applied to the field. For each soybean sample, all plants within a 1.83-m length of row were shaken over a drop cloth, and the number of stink bugs per species was recorded. Soybean was sampled on 28 July (flower), 4 and 11 August (fruiting), and 25 August (dry fruit). For each sampling date, soybean was sampled at four locations per plot.

Halyomorpha halys and eight native stink bugs, E. servus, M. histrionica, E. tristigmus, T. c. custator, N. viridula, Holcostethus limbolarius (Stål), C. hilaris, and Trichopepla semivittata (Say), were captured in pheromone-baited traps. The frequency of occurrence for phytophagous stink bug species (n = 773) in traps was highest for H. halys (35.5%) and E. servus (33.8%) followed by M. histrionica (15.5%) and E. tristigmus (9.8%) (χ² = 1139.3; df = 8; P < 0.0001). The sex ratio of H. halys, E. servus, and E. tristigmus females to males was approximately 1:1. Frequency of occurrence was less than 5% for the remaining five stink bug species. Except for T. c. custator and T. semivittata, nymphs as well as adults were captured. Nymphal attraction to pheromones has been demonstrated for H. halys (Weber et al. 2014, J. Econ. Entomol. 107: 1061–1068) and E. servus and E. tristigmus (Tillman and Cottrell 2016, Fla. Entomol. 99: 678–682). Over the season, H. halys nymphs were captured in each trap, but nymphs were captured more often in a trap approximately only 9 m from a bearing hickory tree (38 %) than those captured in any of the seven remaining traps (χ² = 79.6; df = 7; P < 0.0001). Hickory produces mature fruit from summer to early fall and, thus may be a late-season host plant for H. halys. Stink bugs are capable of penetrating the hardened shell of pecan to feed on the kernel (T.E.C. pers. obs.) and may do the same on hickory nuts. The number of H. halys per trap ranged from 6 to 26 from early August to mid-September, but ranged from only 0 to 6 at other times during the monitoring period. Further research will be conducted to determine if hickory is a host plant for H. halys at this location. Two predatory stink bug species, Podisus maculiventris (Say) (single 4th instar) and Euthyrhynchus floridanus (L.) (one adult), also were captured in traps. Relative frequency of occurrence for native stink bugs in these traps was similar to that for native stink bugs captured in pheromone-baited traps in field borders of crops in southwest Georgia (Tillman and Cottrell 2016, Florida Entomol. 99: 363-370). Knowledge of the complex of native stink bug species and H. halys is necessary for development of appropriate management of stink bugs in the areas where H. halys has become established.

Halyomorpha halys were captured in pheromone-baited traps from mid-May to late October (Fig. 1). The traps first captured adults on 16 May, and nymphs were first captured the week of 30 May. The mean number of H. halys adults and nymphs captured in traps from June through mid-July ranged from 0 to 0.4 insects per trap. By 24 July, the number of nymphs in traps increased until peaking on 8 August. Adults peaked in traps from early to mid-August. Afterward, H. halys adults apparently moved to other areas, for trap capture was very low. This is the first seasonal trap capture for H. halys in Georgia in an area where the invasive species has become established. Seasonal trap capture of H. halys in Georgia was very similar to that of this invasive species in the northeast (Leskey et al. 2015, Environ. Entomol. 44: 746–756). This stink bug was not detected in corn or soybean at the farm this growing season. However, H. halys nymphs and adults were detected in soybean at the farm in 2015 (G.D.B. unpubl. data). Sampling for H. halys in field crops will continue in 2017.

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Euschistus servus were captured in pheromone-baited traps from mid-May to late November, a month after H. halys were last captured (Fig. 1). Trap capture for E. servus adults peaked midmonth from June through August and then early September. At least some of the adults captured in October and November were likely to become overwintering adults as previously determined for E. servus adults captured in traps in field borders of crops in southwest Georgia (Tillman and Cottrell 2016). In general, early-season trap capture was higher for E. servus compared to H. halys. Perhaps this was due to the presence of winter wheat in grain fill at the farm early in the season. This pest stink bug was not detected in corn, but it was present in soybean.

Trichopoda pennipes (F.) (Diptera: Tachinidae) parasitized adult H. halys (0.4%), E. servus (1.5%), E. tristigmus (1.3%), and T. c. custator (10.7%). Generally, T. pennipes parasitizes N. viridula and C. hilaris adults while Euthera tentatrix Loew and Cylindromyia binotata (Bigot) (Diptera: Tachinidae) parasitize E. servus adults (Jones 1988, Ann. Entomol. Soc. Am. 81: 262–273; McPherson et al. 1982, J. Econ. Entomol. 75: 783–786). Nevertheless, T. pennipes parasitizes E. servus although at lower rates compared to parasitism of N. viridula (McPherson et al. 1982; Todd and Lewis 1976, J. Georgia Entomol. Soc. 11: 50–54). Trichopoda pennipes has been reported to parasitize H. halys adults in the Northeast at rates of 1–5% (Rice et al. 2014, J. Integr. Pest Manage. 5: 1-13).