The brown marmorated stink bug was first identified in the United States in Allentown, PA, in the mid-1990s (Hoebeke and Carter, 2003). Since then, it has spread to at least 42 states and two Canadian provinces (Leskey, 2014). The brown marmorated stink bug was first identified in Tennessee in 2008 and in Kentucky 2 years later (Hamilton, 2011). The brown marmorated stink bug is able to rapidly extend its range into a diverse array of climatic regions because of its ability to overwinter in human-made structures that are often actively heated in colder areas (Nielsen et al., 2008) and wide dietary range that provides this stink bug with acceptable food sources in various habitats (Lee et al., 2013a). As the populations of the brown marmorated stink bug build within invaded territories, the stink bug progresses from a household nuisance into a major agricultural pest that can inflict massive crop yield losses during outbreak years (Funayama, 2008). In Asia, where the brown marmorated stink bug is native, injury levels of 90% on cucumber (Cucumis sativus) and eggplant (Solanum melongena), 70% on sweet corn (Zea mays), 60% on asparagus (Asparagus officinalis), and 8% on bell pepper have been reported (Fukuoka et al., 2002). Despite being targeted by several egg parasitoids and invertebrate predators in Asia (Lee et al., 2013a), the brown marmorated stink bug can be a major agricultural pest in outbreak years, potentially due to fluctuation in the populations of native natural enemies. In the United States, brown marmorated stink bug injury on sweet corn has reached 100% in some fields (Leskey et al., 2012a). Injury on other vegetable crops including pepper, tomato (Solanum lycopersicum), eggplant, and okra (Abelmoschus esculentus) has exceeded 20% in research plots (Leskey et al., 2012a). Economic damage inflicted by this new invasive stink bug is creating an urgent need for effective controls to counter it.
Both brown marmorated stink bug adults and nymphs feed on a wide range of crops, including apple (Malus domestica), peach (Prunus persica), tomato, pepper, sweet corn, soybean (Glycine max), cotton (Gossypium sp.), and field corn (Z. mays) (Lee et al., 2013a, 2013b; Nielsen et al., 2008; Owens et al., 2013; Zhu et al., 2012). Adult brown marmorated stink bugs overwinter under the bark of trees and feed on various types of trees after their emergence in the spring including lilac (Syringa vulgaris), maple (Acer sp.), redbud (Cercis sp.), london planetree (Platanus acerifolia), and ornamental cherry (Prunus sp.) (Leskey et al., 2012a). Generally, brown marmorated stink bugs disperse into nearby agricultural fields after the crops have flowered (Lee et al., 2014). Feeding early in the growing season on fruits and vegetables such as apple, tomato, pepper, and eggplant after flowering can cause abscission, the premature dropping of fruit from the plant (Lee et al., 2013a; Nielsen and Hamilton, 2009). Feeding that occurs later in the growing season can leave the fruit externally and internally scarred, decreasing the percentage of marketable fruit (Lee et al., 2013a; Nielsen and Hamilton, 2009). External feeding wounds may also serve as a point of entry for pathogens, such as Erwinia carotovora, that cause bacterial soft rot (Cerkauskas, 2004).
Because the brown marmorated stink bug damages crops throughout a large part of the growing season and disperses from one crop to another, the continual application of control measures is costly and time consuming to growers. The most severe economic damage to fruit crops has occurred in the eastern United States, including Maryland and West Virginia, where the brown marmorated stink bug has been established longer (Leskey et al., 2012a, 2012b). During the outbreak of 2010, brown marmorated stink bug damage inflicted on apple cost the industry over $37 million, along with a 4-fold increase in pesticide applications (Quarles, 2014). Vegetable crops such as bean (Phaseolus vulgaris), tomato, pepper, and eggplant are affected (Kuhar et al., 2012) and sweet corn seems to be a preferred vegetable host. Feeding on corn kernels and beans can cause these structures to shrivel and discolor (Kuhar et al., 2012; Owens et al., 2013). Feeding on tomato and pepper fruits produces a light-colored blemish at the feeding sites and causes a white, corky texture to form underneath the externally injured areas (Kuhar et al., 2012). Native stink bug species, including the green stink bug (Chinavia hilaris) and the brown stink bug (Euschistus servus), cause similar types of injury on a broad range of plants that are targeted by the brown marmorated stink bug, including vegetables crops such as tomato (Kamminga et al., 2009, 2012). Management strategies developed for the brown marmorated stink bug may also help reduce crop injury caused by these native stink bugs.
Organic growers have limited options of National Organic Program-compliant products to combat the brown marmorated stink bug and these are often less effective than their conventional counterparts. Ideally, a diverse range of control tactics including cultural and biological control need to be available to provide growers with ample options. Organic control tactics currently being explored include using insectary plantings to bolster natural enemies (Rice et al., 2014), using trap crops to lure the brown marmorated stink bug away from valuable cash crops (Lee et al., 2013a), and exploiting biological control agents that are native or imported (Talamas et al., 2015).
This study focused on the use of plastic mesh barrier screens to physically exclude the brown marmorated stink bug and other stink bug pests from crops. Exclusion has been used in other agricultural integrated pest management (IPM) programs by constructing screen houses that cover the crop in the field (Ausher, 1997). These screen houses have been widely adopted and proven to be economically feasible in Israel, where they are incorporated into IPM programs to physically exclude the silverleaf whitefly (Bemisia tabaci) from tomato (Taylor et al., 2001). Not only would screens need to exclude target pests, but ideally they would allow for some movement of natural predators through the mesh to prevent secondary pest outbreaks under the screens. However, netting does increase shading of plants and may reduce yields (Ajwang et al., 2002). Studies investigating the shading effects of barrier screens on specific pepper varieties, including Dolmi (Kitta et al., 2014) and yellow lantern chili (Capsicum chinense; Jaimez and Rada, 2006) concluded that the pepper plants actually compensated for the shading effects and produced fruit that was not significantly different from fruit produced in unscreened counterparts. These studies suggest pepper may be an ideal crop to protect from stink bugs with barrier screens because of their shading compensation and were, therefore, selected as the study crop for these screen trials. Screens were tested in organically managed, pepper crop settings in Kentucky and Tennessee, allowing the study to compare results from regions that have supported brown marmorated stink bug populations for different timeframes.
AjwangP.TantauH.Von ZabeltitzC.2002Insect screens for integrated production and protection in greenhouses: A review of the physical and technical basicsGartenbauwissenschaft.674549
FukuokaT.YamakageH.NiiyamaT.2002Sucking injury to vegetables by the brown marmorated stink bug, Halyomorpha halys (Stal)Annu. Rpt. Soc. Plant Protection North Jpn.53229231
FunayamaK.2008Seasonal fluctuations and physiological status of Halyomorpha halys (Stal) (Heteroptera: Pentatomidae) adults captured in traps baited with synthetic aggregation pheromone of Plautia crossota stali Scott (Heteroptera: Pentatomidae)Jap. J. Appl. Entomol. Zool.526975
HamiltonG.2011Year brown marmorated stink bug detected by state. 4 Sept. 2015. <http://www.stinkbug-info.org/index.php/insect/P1>
HoebekeE.R.CarterM.E.2003Halyomorpha halys (Stal) (Heteroptera: Pentatomidae): A polyphagous plant pest from Asia newly detected in North AmericaProc. Entomol. Soc. Wash.105225237
JaimezR.E.RadaF.2006Flowering and fruit production dynamics of sweet pepper (Capsicum chinense Jacq) under different shade conditions in a humid tropical regionJ. Sustain. Agr.2797108
KammingaK.L.HerbertD.A.JrKuharT.P.MaloneS.DoughtyH.2009Toxicity, feeding preference, and repellency associated with selected organic insecticides against Acrosternum hilare, and Euschistus servus (Hemiptera: Pentatomidae)J. Econ. Entomol.10219151921
KittaE.KatsoulasN.KandilaA.Gonzalez-RealM.M.BailieA.2014Photosynthetic acclimation of sweet pepper plants to screenhouse conditionsHortScience49166172
KuharT.P.KammingaK.L.WhalenJ.DivelyG.P.BrustG.HooksC.R.R.HamiltonG.HerbertD.A.2012The pest potential of brown marmorated stink bug on vegetable cropsPlant Health Prog.05230501
LeeD.H.NielsenA.L.LeskeyT.C.2014Dispersal capacity and behavior of nymphal stages of Halyomorpha halys (Hemiptera: Pentatomidae) evaluated under laboratory and field conditionsJ. Insect Behav.27639651
LeeD.H.ShortB.D.JosephS.V.BerghJ.C.LeskeyT.C.2013aReview of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of KoreaEnviron. Entomol.42627641
LeeD.H.WrightS.E.LeskeyT.C.2013bImpact of insecticide residue exposure on the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae): Analysis of adult mobilityJ. Econ. Entomol.106150158
LeskeyT.2014Where is BMSB? 23 Apr. 2015. <http://www.stopbmsb.org/where-is-bmsb/>
LeskeyT.C.HamiltonG.C.NielsenA.L.PolkD.F.Rodriguez-SaonaC.R.BerghJ.C.HerbertD.A.KuharT.P.PfeifferD.DivelyG.P.2012aPest status of the brown marmorated stink bug, Halyomorpha halys in the USAOutlooks Pest Mgt.23218226
LeskeyT.C.ShortB.D.ButlerB.R.WrightS.E.2012bImpact of the invasive brown marmorated stink bug, Halyomorpha halys (Stal), in mid-Atlantic tree fruit orchards in the United States: Case studies of commercial managementPsyche (Stuttg.)2012114
NielsenA.L.HamiltonG.C.2009Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruitJ. Econ. Entomol.10211331140
NielsenA.L.HamiltonG.C.MatadhaD.2008Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae)Environ. Entomol.37348355
OwensD.R.HerbertD.A.DivelyG.P.ReisigD.D.KuharT.P.2013Does feeding by Halyomorpha halys (Hemiptera: Pentatomidae) reduce soybean seed quality and yield?J. Econ. Entomol.10613171323
RiceK.B.BerghC.J.BergmannE.J.BiddingerD.J.DieckhoffC.DivelyG.P.FraserH.GariepyT.HamiltonG.HayeT.2014Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae)J. Integrated Pest Mgt.5A1A13
SaxtonA.AugeB.2014Stats design and analysis web guide. 23 Apr. 2015. <http://dawg.utk.edu/>
TalamasE.J.HerlihyM.V.DieckhoffC.HoelmerK.A.BuffingtonM.L.BonM.WeberD.C.2015Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North AmericaJ. Hymenopt. Res.43119128
TaylorR.A.J.ShalhevetS.SpharimI.BerlingerM.J.Lebiush-MordechiS.2001Economic evaluation of insect-proof screens for preventing tomato yellow leaf curl virus of tomatoes in IsraelCrop Prot.20561569
U.S. Department of Agriculture (USDA)2005United States standards for grades of sweet peppers. 18 Dec. 2015. <http://www.ams.usda.gov/sites/default/files/media/Sweet_Pepper_Standard%5B1%5D.pdf>
ZhuG.P.BuW.J.GaoY.B.LiuG.Q.2012Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys)PLoS One710