The invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a polyphagous agricultural pest that feeds on over 170 plant species, including many cultivated fruits, vegetables, row crops, ornamentals, and wild host plants (Leskey & Nielsen 2018). Native to Asia, the earliest record of H. halys in North America is from 1996 in Allentown, Pennsylvania, in the eastern USA (Hoebeke & Carter 2003). It has since spread throughout much of North America, causing widespread economic harm (Rice et al. 2014; Leskey & Nielsen 2018). In 2014, an Asian egg parasitoid, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), was found successfully parasitizing laboratory reared, field deployed (sentinel) H. halys egg masses in Beltsville, Maryland, USA (Talamas et al. 2015; Herlihy et al. 2016). Several other field populations have since been reported in the mid-Atlantic and Pacific Northwestern regions of the US (10 states and Washington, DC, Hoelmer personal communication), which likely represent multiple independent introductions of the parasitoid (Milnes et al. 2016; Lara et al. 2016; Hedstrom et al. 2017). It is unclear through what pathways T. japonicus entered North America, but genetic data indicate that the parasitoid did not escape from quarantine facilities where it is being studied as a potential classical biological control agent of H. halys (Bon et al. 2017).
The recent introductions of T. japonicus in North America may increase biological control of H. halys. However, to our knowledge, T. japonicus has yet to be documented parasitizing H. halys within North American cultivated crops. All published recoveries of adventive T. japonicus in North America have occurred in non-agricultural, largely woody habitat despite surveys in crops (Talamas et al. 2015; Cornelius et al. 2016a, b; Herlihy et al. 2016; Ogburn et al. 2016; Hedstrom et al. 2017; Morrison et al. 2018) that has led to concern that introduced strains of T. japonicus may have limited biological control potential in North America. During the invasion process, genetic bottlenecks can affect life history characteristics, such as ecological host range (i.e., the number of host species that a parasitoid is able to complete development on in the field), and may limit the ability of introduced biological control agents to attack pests across the same breadth of habitat as in their native range (Hufbauer 2002).
We conducted surveys in 2 commercial apple and 3 peach orchards in southern New Jersey, USA (apple: Monroeville, Gloucester County [39.6877°N, 75.1875°W] and Richwood, Gloucester County [39.7355°N, 75.1748°W]; peach: Richwood, Gloucester County [39.7355°N, 75.1748°W], Glassboro, Gloucester County [39.7085°N, 75.1331°W], and Salem, Salem County [39.5665°N, 75.4248°W]) that had previous pest issues with H. halys. On each farm, contiguous blocks were selected ranging from 2.0 to 9.7 ha of peach or apple, and assigned to 1 of 2 management regimes: Integrated Pest Management - Crop Perimeter Restructuring (IPM-CPR) or grower standard. There were 3 IPM-CPR blocks and 1 grower standard block replicated on 4 orchards for peach and 2 orchards for apple. Blocks within the IPM-CPR (Crop Perimeter Restructuring; described in detail in Blaauw et al. ) management protocol applied insecticides only to the orchard border plus the first full row for H. halys management. In peach, this began at 100 DD14 and continued weekly until harvest. In apple, border-based management was initiated when a cumulative threshold of 10 adult H. halys were found in any aggregation pheromone-baited H. halys trap (Short et al. 2016) and then continued until harvest. All IPM-CPR blocks per farm had a companion grower standard block of a minimum of 2.0 ha, managed according to recommendations from Rutgers University Fruit Management Guidelines (NJAES 2017). In each block, sentinel H. halys egg masses < 24 h old were sourced from the New Jersey Department of Agriculture, Trenton, New Jersey, USA, and deployed on orchard trees at 3 time points in apples (11 Jul, 27 Jul, and 8 Aug 2017) and 4 time points in peach (20 Jun, 11 Jul, 27 Jul, and 8 Aug 2017). Sentinel egg masses were glued using Elmer's Multi-purpose Glue-ALL (Elmer's Products, Inc., High Point, North Carolina, USA) onto paper cardstock and deployed by attaching an egg mass card to the underside of a leaf using a paper clip. Egg masses were deployed on 2 border trees and 2 interior trees (about 6 trees = 18.3 m) in a transect, and placed between 2 and 3 m from the ground. Trees on the border were adjacent to a pheromone baited H. halys trap. There were 192 sentinel H. halys egg masses (5,458 individual eggs) deployed in peach, and 48 in apple (1,321 individual eggs) (Table 1). Egg masses were left in orchards for about 48 h, then returned to the laboratory where each egg mass was placed separately in closed plastic containers, placed in an incubator (25 °C, 60–70% RH, 16:8h (L:D) photoperiod), monitored until emergence of H. halys or parasitoids, and the species identified based on adult morphological characteristics. If parasitoids emerged from an egg mass, or a guarding female was found in association with the retrieved egg mass, after waiting > 1 mo, the remaining unhatched eggs were dissected and inspected for dead parasitoids (larvae or pharate adults) or H. halys nymphs.
The effect of management strategy on the number of parasitized egg masses was analyzed using a 2-sided Fisher's exact test (FET) (Sokal and Rohlf 1995), pooling border and interior trees. The analysis was conducted on a 2 × 2 contingency table of management regime (IPMCPR vs. grower standard) and parasitism status (parasitized vs. unparasitized egg mass). The GPS locations of sentinel egg masses were recorded in the field, and the distances of successfully parasitized egg masses to field edge and the nearest woody border were estimated in Google Earth Pro.
Sentinel egg masses deployed and number of exotic (Trissolcus japonicus) and native (Trissolcus edessae) parasitoids emerging as adults.
No successful parasitism was found on eggs placed in apple orchards. In peach, 4 (2.2%) of 185 retrieved egg masses were successfully parasitized (7 egg masses were not recovered from the field). All successful parasitism in peach occurred under IPM-CPR management; however, the effect of management regime was not statistically significant (P = 0.57, FET). In total, 74 T. japonicus adults emerged from 3 egg masses, with an average proportion parasitism of each successfully parasitized egg mass of 0.917 (± 0.083 SEM), and no emerging H. halys. One of the egg masses parasitized by T. japonicus was deployed on 20 Jun, and 2 were deployed on 8 Aug 2017. Egg masses parasitized by T. japonicus had a distance to the nearest wooded border ranging from 19.7 m to 68.3 m (mean = 40.0 m, SEM = 15.3) (Fig. 1). Two adults of the native parasitoid Trissolcus edessae Fouts (Hymenoptera: Platygastridae) emerged from a single egg mass, along with 1 H. halys nymph and 15 eggs without emergence. Dissection of the 15 unhatched eggs uncovered 8 dead parasitoid larvae, 1 dead pharate parasitoid adult, and 6 with no clear insect development. The egg mass was deployed on 11 Jul at an interior location, 27.8 m (6 trees) from the nearest orchard edge that interfaced a soybean field, and 117 m from the nearest wooded border. One native adult female parasitoid, Telenomus astrictus Johnson (Scelionidae), was captured guarding an egg mass, deployed on 8 Aug and collected on 10 Aug, at a border location in an IPM-CPR peach orchard, 19.9 m from the nearest wooded border. Twenty-two H. halys nymphs successfully emerged from the guarded egg mass, and 6 eggs did not hatch. Dissection of the 6 unhatched eggs uncovered 4 dead parasitoid larvae, 1 dead partially developed H. halys nymph, and 1 with no clear insect development. Whereas H. halys nymphs and adults are highly mobile (Lee et al. 2014; Lee & Leskey 2015), it is not clear how far T. japonicus moves during its lifetime. In frequently disturbed agricultural habitat, T. japonicus may be able only to disperse from source habitats like a wooded field border.
To our knowledge, these are the first observations of successful parasitism of H. halys by T. japonicus on a cultivated crop in the US that occurred in 2 different orchards. In China, the percentage of each H. halys egg mass attacked by T. japonicus ranges between 20% and 80% of eggs, with a season-long average parasitism of each egg mass of 50% among field collected egg masses on fruit and forest trees (Yang et al. 2009; Lara et al. 2016). In northern China, T. japonicus was the dominant egg parasitoid attacking H. halys sentinel egg masses deployed in cultivated peach, mulberry (Morus alba L.; Moraceae), and jujube (Ziziphus jujuba Mill.; Rhamnaceae) trees (Zhang et al. 2017). However, novel environments for parasitoid-host interactions, as with T. japonicus and H. halys in the US, open up an array of questions. For a given host species, its risk of parasitism may vary in different ecological contexts (Cronin & Reeve 2005).
Despite the high success of T. japonicus in its native range within agricultural crops (Zhang et al. 2017), the paucity of parasitism in US commercial agriculture had raised concerns. Our results suggest 2 important findings. First, T. japonicus can successfully forage and parasitize in US crops. Peach is a preferred host plant of H. halys (Acebes-Doria et al. 2016) and produces n-tridecane volatiles to which female T. japonicus also respond (Zhong et al. 2017), perhaps enhancing foraging behavior. Second, despite differences in management styles between Asia and the US, our results suggest that T. japonicus may be compatible with the IPM-CPR tactic in peaches, as all parasitism occurred within these reduced input blocks. The IPM-CPR tactic targets about 25% of the orchard with insecticide and integrates mating disruption for lepidopteran pests, significantly reducing insecticide applications throughout the growing season (Blaauw et al. 2015). Further research on the impact of insecticides on foraging behavior and survivorship of T. japonicus is needed to balance managing injury caused by H. halys in tree fruit with enhanced biological control.
We thank Ann Rucker, Meghin Rollins, and Marina Perez for their assistance in the laboratory and field. This project was supported in part by USDA NIFA 2015-70006-24282, USDA NIFA 2016-51181-25409, and the New Jersey Agricultural Experiment Station Multi-State Project NJ08225. We thank the Florida Department of Agriculture and Consumer Services, Division of Plant Industry for their support on this contribution.
- Acebes-Doria AL, Leskey TC, Bergh JC. 2016. Host plant effects on Halyomorpha halys (Hemiptera: Pentatomidae) nymphal development and survivorship.Environmental Entomology45: 663–670. Google Scholar
- Blaauw BR, Polk D, Nielsen AL. 2015. IPM-CPR for peaches: incorporating behaviorally-based methods to manage Halyomorpha halys and key pests in peach.Pest Management Science71: 1513–1522. Google Scholar
- Bon M-C, Hoelmer KA, Talamas EJ, Buffinton ML, Guermache F, Weber DC. 2017. Genetic diversity and origins of Halyomorpha halys in the U.S. and of its potential biological control agent unexpectedly recovered from the wild in the United States, pp. 240–242 In Mason PG, Gillespie DR, Vincent C [eds.], Proceedings of the 5th International Symposium on Biological Control of Arthropods, 11–15 Sep 2017, Langkawi, Malaysia.CAB International, Wallingford, United Kingdom. Google Scholar
- Cornelius ML, Dieckhoff C, Hoelmer KA, Olsen RT, Weber DC, Herlihy MV, Talamas EJ, Vinyard BT, Greenstone MH. 2016a. Biological control of sentinel egg masses of the exotic invasive stink bug Halyomorpha halys (Stål) in Mid- Atlantic USA ornamental landscapes.Biological Control103: 11–20. Google Scholar
- Cornelius ML, Dieckhoff C, Vinyard BT, Hoelmer KA. 2016b. Parasitism and predation on sentinel egg masses of the brown marmorated stink bug (Hemiptera: Pentatomidae) in three vegetable crops: importance of dissections for evaluating the impact of native parasitoids on an exotic pest.Environmental Entomology45: 1536–1542. Google Scholar
- Cronin JT, Reeve JD. 2005. Host-parasitoid spatial ecology: a plea for a landscape- level synthesis.Proceedings of the Royal Society B-Biological Sciences272: 2225–2235. Google Scholar
- Hedstrom C, Lowenstein D, Andrews H, Bai B, Wiman N. 2017. Pentatomid host suitability and the discovery of introduced populations of Trissolcus japonicus in Oregon.Journal of Pest Science90: 1169–1179. Google Scholar
- Herlihy MV, Talamas EJ, Weber DC. 2016. Attack and success of native and exotic parasitoids on eggs of Halyomorpha halys in three Maryland habitats.PLOS ONE11:e0150275. doi.org/10.1371/journal.pone.0150275 Google Scholar
- Hoebeke ER, Carter ME. 2003. Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America.Proceedings of the Entomological Society of Washington105: 225–237. Google Scholar
- Hufbauer RA. 2002. Evidence for nonadaptive evolution in parasitoid virulence following a biological control introduction.Ecological Applications12: 66–78. Google Scholar
- Lara J, Pickett C, Ingels C, Haviland DR, Grafton-Cardwell E, Doll D, Bethke J, Faber B, Dara SK, Hoddle M. 2016. Biological control program is being developed for brown marmorated stink bug.California Agriculture70: 15–23. Google Scholar
- Lee D-H, Leskey TC. 2015. Flight behavior of foraging and overwintering brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae).Bulletin of Entomological Research105: 566–573. Google Scholar
- Lee D-H, Nielsen AL, Leskey TC. 2014. Dispersal capacity and behavior of nymphal stages of Halyomorpha halys (Hemiptera: Pentatomidae) evaluated under laboratory and field conditions.Journal of Insect Behavior27: 639–651. Google Scholar
- Leskey TC, Nielsen AL. 2018. Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology, and management.Annual Review Entomology63: 433–452. Google Scholar
- Milnes JM, Wiman NG, Talamas EJ, Brunner JF, Hoelmer KA, Buffington ML, Beers EH. 2016. Discovery of an exotic egg parasitoid of the brown marmorated stink bug, Halyomorpha halys (Stål) in the Pacific Northwest.Proceedings of the Entomological Society of Washington118: 466–470. Google Scholar
- Morrison WR, Blaauw BR, Nielsen AL, Talamas E, Leskey TC. 2018. Predation and parasitism by native and exotic natural enemies of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) eggs augmented with semiochemicals and differing host stimuli.Biological Control121: 140–150. Google Scholar
- NJAES (New Jersey Agricultural Experiment Station).2017. New Jersey Commercial Tree Fruit Production Guide. Rutgers Cooperative Extension E002.Rutgers, The State University of New Jersey, New Brunswick, New Jersey, USA. Google Scholar
- Ogburn EC, Bessin R, Dieckhoff C, Dobson R, Grieshop M, Hoelmer KA, Mathews C, Moore J, Nielsen AL, Poley K, Pote JM, Rogers M, Welty C, Walgenbach JF. 2016. Natural enemy impact on eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in organic agroecosystems: a regional assessment.Biological Control101: 39–51. Google Scholar
- Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielsen AL, Pfeiffer DG, Raupp MJ, Rodriguez-Soana C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker JF. 2014. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae).Journal of Integrated Pest Management5: A1–A13. Google Scholar
- Short BD, Khrimian A, Leskey TC. 2016. Pheromone-based decision support tools for management of Halyomorpha halys in apple orchards: development of a trap-based treatment threshold.Journal of Pest Science90: 1191–1204. Google Scholar
- Sokal RR, Rohlf FJ. 1995. Biometry.W.H. Freeman and Company, New York, USA. Google Scholar
- Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer KA, Buffington M, Bon M-C, Weber DC. 2015. Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America.Journal of Hymenoptera Research43: 119–128. Google Scholar
- Yang Z-Q, Yao Y-X, Qiu L-F, Li Z-X. 2009. A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology.Annals of the Entomological Society of America102: 39–47. Google Scholar
- Zhang J, Zhang F, Gariepy T, Mason P, Gillespie D, Talamas E, Haye T. 2017. Seasonal parasitism and host specificity of Trissolcus japonicus in northern China.Journal of Pest Science1–15. Google Scholar
- Zhong Y-Z, Zhang J-P, Ren L-L, Tang R, Zhan H-X, Chen G-H, Zhang F. 2017. Behavioral responses of the egg parasitoid Trissolcus japonicus to volatiles from adults of its stink bug host, Halyomorpha halys.Journal of Pest Science90: 1097–1105. Google Scholar