Duration: 08/01/2011 to 09/30/2013

Administrative Advisor(s):

NIFA Reps:

Non-Technical Summary

Statement of Issues and Justification

Statement of Issue: The brown marmorated stink bug, Halyomorpha halys Stål is a highly polyphagous stink bug of Asian origin. In its native range of China, Korea and Japan, it is considered an agricultural pest of soybeans, tree fruit and various ornamental crops. The brown marmorated stink bug is also a nuisance pest in these countries due to its overwintering behavior of entering enclosed structures such as residences in large numbers each fall. Since its introduction into the United States around 1996, it has spread to numerous states, become a homeowner nuisance wherever it occurs and in the eastern United States, become a severe agricultural pest with little or no management options.

Need: A rapid response to this issue is warranted given the heavy losses incurred by agricultural producers in the eastern United States during the last two growing seasons. In 2010, yield losses due to this insect in the tree fruit growing regions of Virginia and West Virginia approved 95%. Organic producers in this area also observed similar amounts of damage to numerous fruits and vegetables. In 2011, similar damage levels were again observed in these and other eastern states and crops (apples, pears, peaches, tomatoes, peppers, grapes, brambles sweet and field corn and soybeans) from Virginia to New York.

Justification: The brown marmorated stink bug was first observed in the United States in Allentown, PA around 1996 but was initially misidentified as a native pentatomid species. Following correct identification in 2001, it has been found throughout the United States east of the Mississippi river and in Arizona, California, Colorado, Iowa, Minnesota, Nebraska, Oregon and Washington. In several eastern states, its presence in agricultural crops has been confirmed in 2009 and was documented causing severe damage to apples, peaches, pears, peppers and tomatoes. In 2010, damage by this insect was also observed in brambles, field corn, grapes, ornamentals, soybeans, and sweet corn.

Traditionally, management of stink bugs in soybeans, tree fruit and horticultural crops was accomplished through the use of targeted applications of organophosphate insects. However, with the passage of the Food Quality Protection Act in 1996, these materials have been slowly phased out resulting in increased damage by stink bugs in these crops. The addition of BMSB with its high rates of reproduction and survival puts these crops at greater risk. Many of the insecticides currently available to growers have variable effects on resident populations and little or no residual effects on future invaders into treated fields and orchards. In the laboratory pyrethroid insecticides, the replacement for organophosphate insecticides in many cases, exhibit high levels of toxicity to the brown marmorated stink bug fifth instars and adults but have not tested under field conditions. In addition, their use is discouraged in tree fruit and vegetables because of their negative effects natural enemies.

In Asia, the brown marmorated stink bug is attacked by several egg parasitoids and one species of tachinid fly. However, as is customary with newly introduced species, natural enemies are rarely introduced at the same time. Two egg parasitoids and a tachinid fly have been observed attacking the brown marmorated stink bug in Pennsylvania and New Jersey but are generalist natural enemies and therefore not specific to the brown marmorated stink bug. The use of microbial agents is another potential non-chemical control method. However, to date, screening for possible candidates with toxicity to the brown marmorated stink bug has had limited success.

In addition, wherever, the brown marmorated stink bug occurs it has become a severe residential nuisance pest. Currently, there are no adequate pest management alternatives to prevent overwintering brown marmorated stink bug adults from entering residences in areas where they occur. Current recommendations for caulking of windows and/or the sealing of cracks and voids in exterior walls, eaves, etc. are only stop gaps. The use of insecticides to control the brown marmorated stink bug has proven effective in Japan; however, their usage is not currently labeled in the United States and therefore, is not currently an option. Unfortunately, homeowners and pest control professionals are creating their own potential solutions through the illegal use of bug bombs in attics and treatment of exterior/interior walls and eaves with insecticides. These practices pose health risks to homeowners, their families and the environment. Previous Work: In 1996, the brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), was accidentally introduced into Allentown, PA from Asia (Hoebeke and Carter, 2003). Since its initial introduction, H. halys has established throughout most of PA. In July of 2004, a website (www.rce.rutgers.edu/stinkbug/; Hamilton, 2004) was created that allows the public to report sightings of the insect. Since its creation, over 15,000 reports have been received. As a result, we have been able to track the spread of H. halys in PA and NJ and in the northeast confirm its presence and spread in CT, DE, MD, NH, NY, RI, VA, Washington D.C. and WV. Halyomorpha halys populations are also rapidly increasing wherever they have been found. For instance, in Beltsville, MD, populations have increased by over 300% since 2004. In January of 2005, H. halys was first confirmed in Oregon (Rose 2005) and was also found in Vallejo, CA in a shipment of furniture originating in Allentown, PA in February of 2005 (Eberling 2005). In 2006, H. halys was first confirmed in Los Angeles and Orange County, CA. As of 2011, we have also confirmed that BMSB is either establiched or has been found over 30 states. In Asia, H. halys reportedly has a very wide host range including tree fruit (Hoebeke and Carter, 2003). Watanabe (1996) discussed H. halys feeding damage on cherry in Japan. Funayama (1996) found that damage was heavier in early and mid-harvest apple cultivars in Japan. In Korea, H. halys is the dominant pest species of Citrus junos Sieb. (Yuzu or Japanese citron) causing black concave spots during the fruit enlargement and yellowing period (Choi et al., 2000). Halyomorpha halys has also been observed damaging apricots, peaches and plums (Watanabe 1996; NPAG 2001). In the U.S., Bernon (2004) reported that in addition to apples, peaches and pears, H. halys has been found feeding on at least 20 ornamental trees and shrubs including crabapple, Norway maple, empress trees (Paulownia tomentosa), and roses. Specimens have also been collected feeding on tomatoes, peppers, asparagus fronds, raspberry, grapes, field and sweet corn, green beans, squash, pumpkins, soybeans and wheat. Since its introduction into the U.S., H. halys has caused significant crop losses in fruit orchards (Nielsen and Hamilton, 2009a, Leskey, unpublished data). Typical methods for monitoring or trapping stink bugs include the use of pheromone traps, beat sampling and black light trapping. Cullen and Zalom (2000) used both beat sampling and pheromone trapping to create a phenology model for monitoring nymphs of Euschistus conspersus Uhler (Heteroptera: Pentatomidae). In low growing vegetable crops, canopy shake sampling was the most effective method to determine Euschistus sp. population densities along with observations of the soil surrounding the plants. Black light traps in Japan have been used to show gradual increases in H. halys populations in July and August (Moriya et al., 1987) and has also been an effective way to monitor BMSB populations in the US (Nielsen and Hamilton, 2009b). Khrimian et al. (2008) showed that the aggregation pheromone of the brown-winged green bug, Plautia stali Scott, methyl (2E,4E,6Z)-decatrienoate and its isomers are attractive to H. halys. Halyomorpha halys is attracted not only to the EEZ-isomer, but also to at least two other isomers, including methyl (2E,4Z,6Z)-decatrienoate, a compound known to be part of pheromones of pentatomids in genus Thyanta. The ZEZ-isomer, not previously known to be attractive to H. halys, was moderately attractive in the field. Analyses of volatiles collected from dispensers used in field trials showed that all three compounds rapidly isomerize under daylight to form complex mixtures that seemed more attractive to H. halys than the individual isomers. Traps baited with this aggregation pheromone to capture overwintering adults have been used to forecast potential H. halys infestations rates in the early spring (Tada et al., 2001).A similar case of cross-attraction between heteropterans within the same trophic level has recently been reported by Endo et al. (2006). Nevertheless, the search for an aggregation pheromone from H. halys is ongoing (J. Aldrich, pers. comm.) and, if such a pheromone can be identified and easily synthesized, it would improve our ability to utilize semiochemical-baited traps for monitoring purposes. Other types of monitoring systems have been tested to monitor H. halys. In Japan, Watanabe et al. (1994a, b) showed that slit-traps were attractive to H. halys seeking overwintering sites, and that unpainted traps coated with a clear lacquer were more attractive than traps painted black or white. For monitoring using semiochemicals to be effective against a pest, trap efficiency, trap density and lure strength parameters must be understood (El-Sayed, 2006). We have addressed the issue of trap efficiency. In 2004, a three year study using rubber septa treated with 2.5 mg of attractant was begun to evaluate different traps types (pyramid, football, smart trap and apple trap) available to monitor stink bug populations in ornamentals and soybeans. In 2004 and 2005, significantly higher trap catches were observed in pyramid traps in both ornamental trees and soybeans (Nielsen and Hamilton, unpublished data). We have addressed the issue of lure strength. In 2007, we completed a two year study examining the response of H. halys to traps baited with different trap loading rates. This work showed that the 25 mg/trap load caught significantly more individuals than all other treatments each year (Khrimian, Hamilton and Shearer, unpublished data). In addition, the use of a trap loaded with 7.5 mg lure attracted significantly more H. halys than did the 2.5, 0.5 and 0 mg treatments. These results indicate that traps baited with a 25 mg/septum attractant may have potential for use in a mass trapping effort. Stink bugs have historically been managed using organophosphorus insecticides, however, changes in insecticide chemistries and U.S. Environmental Protection Agency decisions that limit or prohibit the use of this class of insecticides has led researchers to investigate other management options. Currently, materials to control stink bugs include various pyrethroids (cyfluthrin, »-cyhalothrin, esfenvalerate, fenpropathrin and permethrin), carbamates (oxamyl and methomyl), and neonicotinoids (imidacloprid, thiamethoxam, dinotefuran, clothianidin) (Ward, 2010). Nielsen et al. (2008) demonstrated in the laboratory that pyrethroids were toxic to BMSB, but to date, none have been field tested against BMSB. Another potential option for managing BMSB is biological control. Relatively little information exists regarding BMSBs natural enemies in Asia, although a few natural enemies have been recorded in the literature. Several egg parasitoids, Trissolcus mitsukurii, T. plautiae, T. itoi, (Arakawa & Namura 2002) and Gryon japonicum (Noda 1995) have been reported in Japan. Recent studies in Japan have reported one or more new species of Trissolcus from BMSB (M. Toyama, pers. comm.). Until very recently there were no published studies for natural enemies in China, but a new species, T. halyomorphae, was recently described (Yang et al. 2009). A parasitic tachinid fly, Bogosia spp., is reported to attack the adult BMSB in Japan (Kawada & Kitamura, 1983b). Studies conducted through a cooperative agreement with Seoul National University identified a tachinid fly, Pentatomophaga latifascia, attacking adult BMSB in Korea, but evidence to date suggests it has a wide host range and little specific impact. No nymphal parasitoids are reported from pentatomids. In the U.S., Bernon (2004) reared two egg parasitoids, Telenomus podisi Ashmead (Hym.: Scelionidae) and Anastatus sp. (Hym.: Eupelmidae), from an early survey of eggs of H. halys on Paulownia. The former is a well-known parasitoid of southern green stink bug, Nezara viridula, and many other stinkbugs (Jones 1988), whereas Anastatus spp. are broadly polyphagous within their search habitats and attack eggs of many different insect families and orders. Bernon (2004) noted an unidentified tachinid fly stalking H. halys on Paulownia and collected dead adult BMSB with apparent tachinid exit holes. Tachinids were found in pheromone-baited traps being tested to attract the bug (Aldrich et al. 2006), but inspection of nearly a thousand wild adults at ARS BIIR laboratory in Newark over the past several years showed that only about 5% contained tachinid eggs, and no adult flies were reared from any of these (Hoelmer, unpublished data). This suggests that at least some indigenous tachinids will recognize and attack BMSB as a potential host, but are not physiologically suited to complete development in this host stink bug. ARS BIIR surveys identified two species of Anastatus and two or three species of Trissolcus (Hym.: Scelionidae) from wild-collected and sentinel egg masses. A majority of the low levels of parasitism seen was due to the Anastatus species. Although Trissolcus sps. are typically restricted to pentatomids, and are capable of high levels of parasitism (e.g., Koppel et al 2009), these species parasitized only 1-2% of BMSB eggs. Much higher levels of BMSB parasitism are reported in Asia (Toyama, unpublished data). Surveys to date have focused solely on Paulownia as a host plant of BMSB egg masses. Additional surveys need to be conducted to determine whether levels of parasitism vary among different host plants in different crop environments, as there may well be unknown differences in regional and habitat-specific composition of parasitoid species that will search for and attack BMSB in tree fruits, on vegetables, and in native and introduced ornamental species. This information will be very important in evaluating the need for a classical biological approach. Screening for egg parasitoids in soybeans and ornamentals has been initiated in DE, NJ and PA with limited success (Hoelmer et. al., 2008).

Types of Activities

Objective 1. Assess the extent and nature of injury caused brown marmorated stink bug. Depending on individual state priorities we will establish research plots in field crops, fruit, nursery and vegetables to evaluate damage caused by the brown marmorated sting bug. Beginning with the first appearance of adults, eggs or nymphs in plots, sentinel plants will be evaluated for damage on weekly basis. At harvest, yield estimates and damage evaluations from a subsample of plants within each plot. Objective 2. Develop monitoring methods for brown marmorated stink bug. Depending on individual state priorities we will establish research plots in field crops, fruit, nursery and vegetables to develop and evaluate monitoring methods in these crops. Plots will be maintained using standard practices but without the use of insecticide. Depending on the crop, adult brown marmorated stink bugs will be monitored using a combination of blacklight traps, pheromone traps, direct visual counts or sweep netting. Nymphal populations will be monitored using weekly direct counts only. Data collected for blacklight and pheromone traps will be correlated with the first presence of adults and nymphal BMSB in plots. All other methods will be compared for differences in population estimates between methods. Objective 3. Determine the potential for biological control of the brown marmorated stink bug. This objective will be fulfilled using the plots established in each state for either objective 1 or 2. Sentinel brown marmorated stink bug egg masses will be outsourced on a minimum of eight randomly selected plants within plots. This will be initiated when naturally colonizing adults are observed in the plots and will be repeated every other week throughout the growing season. Each egg mass be examined 24 h later to detect predation. After 48-h, all egg masses will be collected, brought to the laboratory, examined for predation and then, held for emergence of adult parasitoids. The frequency of egg parasitization by a single parasitoid or combination of parasitoids will be calculated for the sentinel egg masses. Objective 4. Determine the toxicity and field efficacy of selected insecticides for brown marmorated stink bug control We will conduct small-plot field experiments in field crops, fruit, nursery and vegetables in states where heavy infestations of brown marmorated stink bug occur to evaluate the efficacy of both conventional and organic insecticides/materials against brown marmorated stink bug nymphs and adults. A suite of conventional insecticides including, where appropriate, foliar contact, foliar systemic and soil-applied systemic products will be tested. Objective 5. Develop best management practices for the brown marmorated stink bug. Using the information, developed under objectives 1-3, we will develop crop specific best management plans (BMPs) for the brown marmorated stink bug. This will be done during the projects yearly annual meeting. Objective 6. Deliver research based IPM recommendations to growers. We will incorporate the information and BMPs developed by this project into current grower recommendations. We will also deliver this information via websites, emails, newsletters, grower meetings, etc.

Objectives

1. Assess the extent and nature of injury caused brown marmorated stink bug.
   
2. Develop monitoring methods for brown marmorated stink bug.
   
3. Determine the potential for biological control of the brown marmorated stink bug.
   
4. Determine the toxicity and field efficacy of selected insecticides for brown marmorated stink bug control in field crops, fruit, nursery and vegetables
   
5. Develop best management practices for the brown marmorated stink bug.
   
6. Deliver research based IPM recommendations to growers
   

Expected Outputs, Outcomes and/or Impacts

OUTPUTS This project will document the development and evaluation of several IPM tactics including monitoring, biological control and targeted use of pesticides. Information about the tactics will be discussed by each of the PIs at state and regional grower meetings and will result in information being made available at www.rce.rutgers.edu/stinkbug/ and NE IPM Centers Brown Marmorated Working Group website (http://www.northeastipm.org/working-groups/bmsb-working-group/). Placing this information on the web will allow distribution to growers throughout the US. OUTCOMES OR PROJECTED IMPACTS We anticipate this project to have the following impacts: 1. The IPM tactics we propose to develop will be adopted by farmers in 23 states thereby potentially impacting hundreds of thousands of people through reductions in pesticide residues on field, fruit, nursery and vegetable crops. It would result in the cessation of illegal pesticide applications to control H. halys by farmers. Adoption of this program over large areas also has the potential to reduce the spread of this invasive insect to agricultural areas in other states not currently impacted by BMSB. 2. This project will result in economic benefits in the form of decreased monetary looses due to yield reductions caused by this insect. It will also result in increased time being available for marketing of the crop that would otherwise be spent managing this insect. Finally, this project will ultimately result in fewer costs in managing this pest due to reductions in pesticide use.

Projected Participation

View Appendix E: Participation

Literature Cited

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Cullen, E.M. and F.G. Zalom. 2000. Phenology-based field monitoring for consperse stink bug (Hemiptera: Pentatomidae) in processing tomatoes. Environ. Entomol. 29(3): 560-567. Eberling, B. 2005. Non-native pest found in Vallejo. Daily Republic, Online Edition. Available at: http://www.dailyrepublic.com/articles/2005/03/05/local_news/news04.txt. El-Sayed, A.M., D.M. Suckling, C.H. Wearing, and J.A. Byers. 2006. Potential of mass trapping for long-term pest management and eradication of invasive species. Endo, N., Wada, T., Nishiba, Y., and Sasaki, R. 2006. Interspecific pheromone cross-attraction among soybean bugs (Heteroptera): Does Piezodorus hybneri (Pentatomidae) utilize the pheromone of Riptortus clavatus (Alydidae) as a kairomone? J. Chem. Ecol. 32:1605-1612. Funayama, K. 1996. Sucking injury on apple fruit by the adult of brown Marmorated stink bug, Halyomorphamista (Uhler). Annual Ann. Rept. Plant Prot. North Japan 47: 140-142. Hamilton, G.C. 2004. 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Attachments

Land Grant Participating States/Institutions

AL, CT, DE, KY, LA, NJ, PA, TX, VA, WV

Non Land Grant Participating States/Institutions

Kentucky State University