Biology and Management of the K. L. Kamminga,1,2 A. L. Koppel,3 D. A. Herbert, Jr.,4 and T. P. Kuhar1 1Department of Entomology, 216A Price Hall, Virginia Tech, Blacksburg, VA 24061. 2Corresponding author, e-mail: [email protected]. 3Department of Entomology, University of Kentucky, Lexington, KY 40292. 4Department of Entomology, Virginia Tech, Tidewater AREC, Suffolk, VA 23437.

J. Integ. Pest Mngmt. 3(3): 2012; DOI: http://dx.doi.org/10.1603/IPM12006

ABSTRACT. The green stink bug, Acrosternum hilare (Say) [Chinavia hilaris (Say)] (: ) is one of the most damaging native stink bug species in the United States. It is a pest of economic importance in a variety of commodities, including cotton (Gossypium hirsutum L.), [Glycine max (L.) Merr.], tomatoes (Solanum lycopersicum L.), and peaches [Prunus persica (L.) Batsch].Stink bug feeding can result in cosmetic damage as well as reduced quality and yield. Acrosternum hilare and other stink bugs have become a major challenge to integrated pest management systems because control options are basically limited to the application of broad-spectrum insecticides such as organophosphates, carbamates, and pyrethroids. However, neonicotinoids are generally effective for control of this stink bug and may be less disruptive to natural enemies. Further options for stink bug management that are being explored include the use of trap crops and enhancing beneficial parasitoid populations. The green stink bug is native and found throughout the United States. It has a wide host range, and is a pest of many agricultural commodities. The green stink bug can cause feeding injury to fruit, vegetable, and field crops that may require preventative management. Many strategies are available for its control, which include multiple chemical, cultural, and biological options. Broad-spectrum insecti- cides such as pyrethroids and organophosphates, as well as the less toxic neonicotinoids, are efficacious against the green stink bug. Cultural options, including trap cropping and the planting of resistant varieties, have been documented as decreasing crop injury by stink bugs. In addition, there are multiple natural enemies that reduce population numbers.

Key Words: green stink bug, Acrosternum hilare, cultural control, chemical control, crop damage

Stink bugs (Hemiptera: Pentatomidae) are significant economic pests Life Cycle and Seasonal Biology. The green stink bug overwinters as of many agricultural crops and are frequently one of the most difficult an adult, preferring to do so in litter and deciduous woodlands pests to control in crops such as [Glycine max (L.) Merr.], (Underhill 1934). It emerges from when temperatures sur- cotton (Gossypium hirsutum L.), tomato (Solanum lycopersicum L.), pass 18°C (McPherson 1982). Adults are most active when tempera- and many fruit crops. The green stink bug, Acrosternum hilare (Say) tures exceed 24°C, and are more prone to flight when temperatures (Fig. 1), is native to North America and is a pest found throughout the exceed 27°C (Underhill 1934). United States. It is one of several important stink bug species that After emerging from diapause, the adult females are not reproduc- inflict serious economic injury to agricultural commodities. tively mature and require a preovipositional period to develop (Kam- Identification. The green stink bug is Ϸ1.3–2.0 cm long and 0.8 cm minga et al. 2009a, Nielsen and Hamilton 2009). The ovipositional wide. It is usually bright green and may have a yellow border around period of overwintered adults in eastern North America begins in the the margin of the abdomen, head, and thorax (Underhill 1934). Al- middle of June and ends the first week of September, with peak egg though rare, an orange color morph of this exists (Fig. 1b). laying occurring the third week of July (Underhill 1934, Javahery Green stink bug adults are similar in appearance to the southern 1990). The largest populations of first generation egg masses are green stink bug, viridula (L.), but can be differentiated by found near the woods where adults have overwintered. This genera- black bands on the antenna and a pointed abdominal spine, instead of tion continues to feed on weedy hosts and migrates into nearby crops once they become attractive as a food source (i.e., budding or fruiting red antennal bands with a rounded abdominal spine (Fig. 2) (Miner structures). Miner (1966) reported that the second generation remains 1966, McPherson 1982, McPherson and McPherson 2000). The in the cropping system throughout its life stages. nymphs of the green stink bug are easily distinguishable from those of The green stink bug has a single generation in northern areas the southern green stink bug. Southern green stink bug nymphs have such as Canada (Javahery 1990), but in more favorable southern two rows of white dots on their abdomen, whereas the green stink bug conditions there may be two generations (Sailer 1953, Kamminga nymphs do not. Color morphs are found in both species of nymphs, et al. 2009a). It is thought that the differences in reproductive and both dark and light colorations are commonly exhibited by green cycles may reflect differences in climate. Wilde (1969) reported stink bug nymphs (Figs. 3 and 4). that photoperiod is the primary determinant of generation number, . The green stink bug first was described by Thomas Say as opposed to temperature. as Pentatoma hilaris in 1832 (Say 1832). Its scientific name was Newly eclosed females begin copulating after Ϸ22 d, and lay their changed several times, and eventually in 1915, it was changed to its first egg masses about 3 wk later (Miner 1966). Females can lay a new current name, A. hilare (Parshley 1915). However, it has been sug- egg cluster every 8–10 d. These eggs are deposited vertically in gested recently that the green stink bug is misnamed and should be clusters of 1–72 (Underhill 1934) with an average of 32 eggs per egg classified as Chinavia hilaris (Say) (D. Rider, personal communica- mass (Miner 1966). However, Ͼ130 eggs per cluster have been tion). According to their findings, the genus Acrosternum belongs to observed under laboratory conditions (Miner 1966, Javahery 1990). smaller Palearctic species of stink bugs that live in arid environments. Time between egg mass depositions typically decreases after the first However, because the Entomological Society of America has not mass is laid (Underhill 1934, Nielsen et al. 2008). officially changed the species name of the green stink bug, this paper Eggs are usually adhered to the underside of . The eggs are will use the nomenclature A. hilare (ESA 2012). barrel-shaped and change from light green to yellow (Fig. 5), and then 2 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 3, NO. 3

Fig. 1. Green stink bug, A. hilare, adults. Normal green coloration (A) and the atypical orange coloration (B) (Photos by K. Kamminga).

al. 1988). Development time of the nymphs can vary based on the host and temperature, and development of each instar occurs most rapidly at 27°C (Simmons and Yeargan 1988). Adulthood is reached in Ϸ36 d (Underhill 1934, Miner 1966). A complete description of each life stage is available by Miner (1966). Host . The green stink bug is polyphagous and feeds on a variety of plants, but prefers woody tissue (McPherson 1982). A comprehensive list of host plants is included in Schoene and Underhill (1933), Underhill (1934), and McPherson (1982). To complete its development, the green stink bug typically requires a series of plants with overlapping periods of seed and fruit production (Underhill 1934). It prefers woody hosts including basswood, Tilia americana L.; Fig. 2. Pointed abdominal spine on the ventral surface of the green mulberry, Morus spp.; pear, Pyrus spp.; maple, Acer spp; American (A) and rounded abdominal spine of the southern green stink bug (B) elder, Sambucus canadensis L.; and black locust, Robinia pseudoacia (Diagram courtesy of T. FisherPoff). L.; yet it is a common pest of vegetable and field crops such as lima beans, Phaseolus lunatus L.; green beans, Phaseolus vulgaris L.; soybean, Glycine max (L.) Merr.; tomato, Solanum lycopersicum L.; cotton, Gossypium hirsutum L.; eggplant, Solanum melongena L.; and cucumber, Cucumis sativus L. (Capinera 2001). The green stink bug also has been recorded as feeding on the herbaceous weeds goldenrod, Solidago spp.; ironweed, Vernonia spp.; horseweed, Conyza spp.; and jimsonweed, Datura stramonium L. (McPherson 1982, Capinera 2001). Crop Damage The green stink bug is one of several species of agriculturally important stink bugs in the United States. Similar to other stink bugs, green stink bug populations reach their peak in late summer. Crop injury is accrued when the feeding stylet penetrates plant tissue. The economic injury potential of green stink bug feeding varies by crop. Tomato. Several species of stink bugs, including green stink bug, are reported as economic pests of the tomato (Lye et al. 1988, Zalom et al. 1997, McPherson and McPherson 2000, Nault and Speese 2002). Stink bugs inject a toxin into the fruit when they feed, which can result in a spongy white area. This renders it unmarketable for processing and fresh market tomatoes (Fig. 6) (Kennedy et al. 1983). Stylet Fig. 3. A dark color morph of a third-instar green stink bug (Photo insertion also leads to premature ripening and smaller fruit (Lye et al. by K. Kamminga). 1988). Nault and Speese (2002) reported stink bugs as causing more damage to spring tomatoes in Virginia than either thrips or lepidop- terans. In addition, Kennedy et al. (1983) stated that the green stink to light pink before hatching in about 1 wk (Miner 1966). The duration bug is one of the most damaging pests of tomato in North Carolina. of the egg stage depends on temperature. Shorter durations occur in Peach. Stink bug feeding on fruit trees can result in extensive warmer temperatures, and longer durations in cooler temperatures damage, and feeding injury in the early developmental stage of the (Underhill 1934, Capinera 2001). Upon hatching, they undergo five fruit results in the most damage (McPherson and McPherson 2000). In instars before becoming adults (Underhill 1934, Miner 1966). peaches, feeding injury results in blemishes on the skin, yield loss, The first instars do not feed and remain clustered together around misshapen fruit, or catfacing (Fig. 7) (Rings 1957, McPherson and the egg mass. Second instars are less gregarious and begin to feed. McPherson 2000). Catfacing occurs because the site of the feeding Third instars behave in a similar manner to second instars, but are puncture does not grow, although the areas around it continue to grow. slightly larger in size. Feeding by the fourth and fifth instars can result This results in bumpy areas on the surface of the fruit, making it in as much economic damage to the plants as from adults (Barbour et unmarketable (Rings 1957). This same dimpling and damage to the SEPTEMBER 2012 KAMMINGA ET AL.: PROFILE OF THE GREEN STINK BUG 3

Fig. 4. A dark (A) and light (B) color morph of a fifth-instar green stink bug (Photos by K. Kamminga).

Fig. 7. Catfacing on peaches (Photo by S. Villanassery Joseph).

Euschistus servus (Say), and the dusky stink bug, Euschistus tristig- mus (Say), in the eastern United States (Hogmire 1995). More re- Fig. 5. Green stink bug eggs on a soybean leaf (Photo by K. Kamminga). cently, the brown marmorated stink bug, Halyomorpha halys (Stål), has caused the greatest economic loss to peaches in the mid-Atlantic states (Leskey and Hamilton 2010). Soybean. Stink bug feeding preference varies with the developmen- tal progress of the crop. The typically move into a soybean field after flowering and remain through plant maturity. A survey of soybean and cotton in southeastern Virginia determined that brown and green stink bugs were the most common species in 2005 and 2006 (Kamminga 2008). More recently, the brown marmorated stink bug has become a dominant stink bug in many agricultural commodities in the mid-Atlantic, including areas of New Jersey, Maryland, Delaware, Pennsylvania, West Virginia, and Virginia. It was reported that the brown marmorated stink bug outnumbered all native species in soy- bean fields in Pennsylvania (Nielsen et al. 2011). Stink bug feeding on soybean can cause green stem syndrome, a plant response that results in green stems past maturity. Feeding also results in reduced seed quality (Fig. 8); decreased yield (Underhill 1934, McPherson and McPherson 2000); and less oil than undamaged beans (Daugherty et al. 1964). Feeding punctures from green stink bug stylets may also increase the possibility of infection by a pathogen. Fig. 6. Stink bug feeding injury tomato can result in a spongy white The insect has been shown to transmit the causative agent of yeast- area (Photo by K. Kamminga). spot disease (McPherson and McPherson 2000). Importers may reject seeds if too much stink bug damage is present (Chyen et al. 1992), surface of the peach can also occur later in the development of the fruit resulting in even greater economic loss. (Rings 1957, McPherson and McPherson 2000). Cotton. Stink bugs have been considered to be pests of cotton since Historically, green stink bug was considered an economically the early 1900s (Morrill 1910). Historically, stink bugs were con- important stink bug pest of peaches along with the brown stink bug, trolled by broad-spectrum insecticide sprays, intended to control other 4 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 3, NO. 3

Fig. 8. Stink bug feeding injury to soybean (Photo by S. Malone).

Fig. 10. Black light trap (Photo by K. Kamminga).

punctures (sunken lesions) and internal injury; however, it is still difficult to accurately correlate the two (Blinka et al. 2010). Monitoring and Management Options Sweep Nets and Beat Sheets. Sampling of insects on crops is traditionally performed to assess the pest complex in relation to economic thresholds. Sweep net and beat sheet sampling methods are recommended for monitoring stink bugs in field crops (Todd and Herzog 1980). For fruits and vegetables, beat sheets are more common (Nielsen and Hamilton 2009). Fig. 9. Sink bug feeding injury to cotton can cause stained lint and Stink bug thresholds vary according to the crop. For example, the internal warts (Photo by C. R. Phillips). threshold for tomatoes is one stink bug per three beat sheet samples (Brust and Zalom 2005). For soybeans, recommendations for stink bug thresholds can also vary by state (Parker 2012). In many southern pests such as the boll weevil, Anthonomus grandis grandis Boheman states, a beat sheet sample containing above one stink bug per 0.3-row (Coleoptera: Curculionidae), and the bollworm, Helicoverpa zea meter may require an insecticide application (Parker 2012). However, (Boddie) (Lepidoptera: Noctuidae) (Greene et al. 1997). Recently, thresholds can also vary by maturity (Parker 2012) and seed spacing stink bug populations in cotton have increased. This is in part because (Herbert 2012). Current practices in cotton recommend a dynamic of fewer insecticide sprays targeting boll weevil, resulting from a threshold based on the age of the boll and the percent internal dam- widely successful eradication program throughout most of the south- aged bolls per field. Moreover, Herbert (2012) indicates that one stink ern United States. In addition, B.t., Bacillus thuringiensis Berliner, bug per 25 sweeps or one stink bug per two-row meters may be above crops have increased in acreage and provide control over many lep- economic threshold. idopteran pests without the need to spray insecticides. These advance- Establishing accuracy of the sampling methods is complex, as this ments have decreased the number of broad-spectrum insecticide can depend on the life stage and density of both crops and insects, as sprays on cotton, resulting in an increase in stink bugs. well as time of day (Reay-Jones et al. 2009). Sampling using sweep A complex consisting of the four primary stink bugs, the green, nets and beat sheets can help determine the seasonality and life stage southern green, redbanded, Piezodorus guildinii (Westwood), and of stink bugs, but they may drop to the ground or fly away when brown stink bug are found in cotton throughout the southeast. Reay- disturbed. Other monitoring methods, like pheromone and blacklight Jones et al. (2009, 2010) reported the green stink bug as being the traps, may offer additional information as to the species, relative primary stink bug collected during sampling in cotton in South Car- abundance, and flight activity of stink bugs on farms. olina and Georgia in 2008 and 2007. In addition, surveys in Virginia Blacklight Trapping. Many insects, including stink bugs, can be also determined that the green stink bug is a prominent stink bug in the monitored using blacklight traps (Fig. 10). Blacklight trap catch may cotton system (Kamminga 2008). be useful for improving the timing of scouting and management Stink bugs feed on young, tender cotton bolls resulting in injured methods for stink bugs (Kamminga et al. 2009a, Nielsen and Hamilton seeds and lint, and lower yield (Fig. 9) (Barbour et al. 1988, 1990). 2009). In addition, flight activity and distribution can be determined Researchers have investigated an association between external feeding for native and possible invasive species. SEPTEMBER 2012 KAMMINGA ET AL.: PROFILE OF THE GREEN STINK BUG 5

tion (Aldrich et al. 1989, 1993). However, synthesis of the aforemen- tioned pheromone is expensive and currently inhibits widespread use of this technique. Chemical Control. Broad-spectrum insecticides, such as organo- phosphates and pyrethroids, are the most frequently applied insecti- cides for stink bug management (Kuhar et al. 2006, Herbert 2012), and both classes provide efficacy against Acrosternum spp. (Willrich et al. 2003). Dicrotophos, an organophosphate, has been cited as having a high toxicity to various stink bug species (Tillman and Mullinix 2004, Snodgrass et al. 2005), and it is suggested that it provides consistent control of the green stink bug (Willrich et al. 2003, Snodgrass et al. 2005, Kamminga et al. 2009c). The green stink bug also has been

reported as having a lower LC50 (lethal concentration required to kill 50% of the insects tested) value to pyrethroids and organophosphates than the brown stink bug (Greene et al. 2001, Snodgrass et al. 2005). In addition, Kamminga et al. (2009c) performed efficacy trials on stink bug nymphs and adults in southeastern Virginia, and found that the green stink bug was especially susceptible to all of the pyrethroids tested. Neonicotinoids also were effective against green stink bug adults. In particular, thiamethoxam, dinotefuran, and imidacloprid were found to be efficacious against green stink bug adults; whereas dinotefuran and clothianidin were efficacious against green stink bug nymphs. In a similar study, Tillman (2006b) reported that acetamiprid and thiamethoxam exhibited some residual contact and ingestion activity on nymphs, but not adults, of the southern green stink bug. Differences in the susceptibility of stink bug life stages to insec- ticides are common (McPherson et al. 1979; Willrich et al. 2002, 2003; Kamminga et al. 2009c). Willrich et al. (2003) reported that brown stink bug nymphs were more susceptible to the pyrethroid lambda-cyhalothrin than the adults. Conversely, southern green stink Fig. 11. Yellow pyramid trap with pheromone for monitoring stink bug nymphs were less susceptible to the pyrethroids cypermethrin and bugs (Photo by K. Kamminga). lambda-cyhalothrin than the adults. McPherson et al. (1979) and Willrich et al. (2002) reported that the LD50 (lethal dose required to kill 50% of the insects tested) of methyl parathion on late instars of

brown, green, and southern green stink bugs was higher than the LD50 during the adult stage. Very little research has been done to test the efficacy of Organic Materials Review Institute-certified (organic) insecticides against stink bugs. The research that has been published primarily investigates the effects of the extract azadirachtin from the neem tree, Azadirachta indica (A. Juss), on stink bug nymphs. Azadirachtin acts as an anti- feedant (Seymour et al. 1995, Abudulai et al. 2003, Kamminga et al. 2009b), but mixed results have been reported in its efficacy against stink bugs (Kamminga et al. 2009b). Azadirachtin is also an insect growth regulator and has been reported as disrupting the molting of stink bug nymphs (Abudulai et al. 2003, Riba et al. 2003), but research also has indicated that it is not always efficacious against stink bug nymphs that were fed an azadirachtin-treated food source (Overall 2008, Kamminga et al. 2009b). Fig. 12. Tachinid fly, T. pennipes (F.) (Photo by Russ Ottens, Pyrethrins and an organic formulation of spinosad have been found University of Georgia, Bugwood.org). to be effective against stink bug nymphs (Overall 2008, Kamminga et al. 2009b). Pyrethrins were reported as repelling stink bugs, whereas spinosad attracted them (Kamminga et al. 2009b). Spinosad also was

Pheromone Trapping. Pheromone traps have been used to monitor determined to have a lower LC50 on harlequin bug nymphs, Murgan- green stink bug populations in peach, Prunus persica (L.) Batsch; tia histrionica (Hahn), than either pyrethrins or azadirachtin (Overall apple, Malus domestica Borkh. (Leskey and Hogmire 2005); and 2008). In addition, in behavioral bioassays, stink bugs were found to pecan, Carya illinoinensis (Wangenh.) K. Koch, orchards (Mizell and feed more on spinosad-treated tomatoes than untreated-, azadirachtin-, Tedders 1995). A yellow base pyramid trap with a pheromone lure is and pyrethrin-treated tomatoes. Spinosad caused high mortality when commonly used to monitor green stink bug populations (Fig. 11) green and brown stink bug adults were fed treated green beans, but (Leskey and Hogmire 2005, Hogmire and Leskey 2006). The aggre- mixed results were obtained when tested against nymphs (Kamminga gation pheromone blend for the green stink bug has been identified as et al. 2009b). a 95:5 cis:trans blend of (4S)-cis-Z-bisabolene epoxide and (4S)- Cultural Control. Trap crops are designed to intercept and allow for trans-Z-bisabolene epoxide (Aldrich et al. 1989, 1993; McBrien et al. the removal of a pest before it moves into a cash crop by providing a 2001). Cross attractiveness of the green stink bug to the southern green preferred food source. This method has been found to be an effective stink bug pheromone also has been documented (Tillman et al. 2010) management technique for stink bugs (Todd and Schumann 1988, and may occur because of the similarities in their chemical composi- Hokkanen 1991). For example, sorghum, Sorghum bicolor L. Mo- 6 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 3, NO. 3

Host Plant Resistance. Stink bug resistant varieties of soybean have been shown to have a lower population of pentatomids than other varieties (Gilman et al. 1982, Jones and Sullivan 1982). More recent studies have indicated that certain breeding lines of soybean may be possible genetic material for stink bug resistant soybeans (McPherson et al. 2007, Campos et al. 2010). These resistant lines may decrease damage caused by stink bug feeding and insecticide applications for stink bug control in soybeans. Biological Control. Biological control, which relies upon natural enemies of the pest to manage the pest population and reduce com- modity damage, is a part of stink bug pest management. Stink bugs are vulnerable to multiple predators, parasites, and parasitoids. Mermithid nematodes have been reported as infesting stink bug adults and nymphs (Fuxa et al. 2000, Riberiro and Castiglioni 2008). Lacewing larva; spined soldier bugs, Podisus maculiventris (Say); and birds are common predators of stink bugs (Underhill 1934, McPherson 1982, McPherson and McPherson 2000). Most stink bug parasitoids are tachinid flies that oviposit on the abdomen of the host. A common example is (F.) (Diptera: Tachinidae) (Fig. 12) (Capinera 2001). The female fly deposits one or multiple small gray- ish eggs on the abdomen of adults or nymphs. The eggs hatch in Ϸ30 Fig. 13. Egg parasitoid, T. podisi, on stink bug eggs (Photo by A. h and the larvae then burrow into the body of the host. After Ϸ16 d, Koppel). a single larva will emerge as a maggot from the host. This maggot pupates and an adult fly emerges in 2–4 wk (Worthley 1924). Over- wintering larvae remain in their host throughout the winter and emerge in the spring. Other egg parasitoids include wasps of the genera Trissolcus, Anastatus, and Telenomus (Fig. 13). Wollaston (Hymenoptera: Scelionidae) (Fig. 14) has shown potential against southern green stink bugs in soybean (Ehler 2002). Inoculative re- leases of 15,000 T. basalis adults per hectare in a trap crop of early maturing soybean reduced the stink bug density an average of 58% in the main crop of late planted soybeans (Correˆa-Ferreira and Moscardi 1996), maintaining it below economic threshold. Koppel et al. (2009) reported 47% green stink bug egg parasitism during a survey of crops in the mid-Atlantic United States. Orr et al. (1986) reported an egg parasitization rate of 14–22% in Louisiana soybeans. The Louisiana and Virginia egg parasitoid surveys determined that green stink bug eggs were parasitized by Trissolcus euschisti Ashmead, T. basilis, Trissolcus edessae Fouts, and Telenomus podisi Ashmead (Orr et al. 1986, Koppel et al. 2009). An additional parasitoid species, Telenomus cristatus Johnson, also was identified as parasitizing green stink bug eggs in Louisiana (Orr et al. 1986). Acknowledgments We thank our colleagues D. G. Pfeiffer, S. Malone, and S. M. Fig. 14. A common egg parasitoid of the green stink bug, T. basalis Salom (Virginia Tech, Department of Entomology), and K. A. Hoe- (Photo by A. Koppel). lmer (USDA-ARS Beneficial Introductory Research Laboratory) for research and writing support. ench, (Tillman 2006a) and soybeans (Bundy and McPherson 2000) have been successfully used as trap crops of stink bugs to protect References Cited Abudulai, M., B. M. Shepard, and P. L. Mitchell. 2003. Antifeedant and toxic cotton. Planting a perimeter of earlier maturing soybean than the main effects of a neem (Azadirachta indica A. Juss)-based formulation Nee- crop was found to be an effective control method in soybean, espe- mix(R) against Nezara viridula (L.) (Hemiptera: Pentatomidae). 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