The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a severe agricultural and urban nuisance pest that originates from southeast Asia (Hoebeke and Carter 2003) and has invaded numerous countries worldwide (Cesari et al. 2015, Gariepy et al. 2014, Haye et al. 2015b, Macavei et al. 2015, Milonas and Partsinevelos 2014, Vétek et al. 2014). As of 2020, it has been detected in 46 U.S. States and four Canadian Provinces, with 11 States reporting severe agricultural damage (StopBMSB.org). Halyomorpha halys was first detected in Utah in 2012 and has been considered a pest to fruit and vegetable crops since 2017. With the threat of increasing economic agricultural damage, development of proactive management tactics is imperative. In the U.S. Mid-Atlantic region, where H. halys has been a severe pest, effective control has relied on broad spectrum insecticides, leading to increased application frequency and disruption of integrated pest managment, including secondary pest outbreak (Lee et al. 2014, Leskey et al. 2014, Leskey et al. 2012a, Leskey et al. 2012b). Physical or cultural control (e.g. trap cropping and mass trapping) can offer some mitigation of plant damage, but may not be economically viable (Mathews et al. 2017). The most effective management tactics have paired cultural and chemical tactics (e.g. orchard perimeter insecticide applications and treatment of trap trees) (Blaauw et al. 2014).

Biological control by egg parasitoids has proven effective in suppressing H. halys populations in its native range (Yang et al. 2009, Zhang et al. 2017). Halyomorpha halys sentinel egg mass surveys in North America have identified parasitism by native parasitoids in the families Scelionidae, Encyrtidae and Eupelmidae (Abram et al. 2017, Cornelius et al. 2016a, Cornelius et al. 2016b, Balusu et al. 2019, Talamas et al. 2015a, Talamas et al. 2015b). However, parasitism rates are low, likely due to inability of native species to overcome healthy H. halys egg defences (Abram et al. 2017, Abram et al. 2014, Dieckhoff et al. 2017,Herlihy et al. 2016). Measuring native parasitoid effectiveness against H. halys eggs solely by wasp emergence may underestimate their impact, as partial development of a native wasp inside H. halys eggs can cause egg mortality (Abram et al. 2019a, Abram et al. 2014, Cornelius et al. 2016a, Schumm 2020). Therefore, evaluating native wasp parasitism rates, especially in novel landscapes where new behaviour or species may be observed, deserves critical analysis.

Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) is an egg parasitoid native to the home range of H. halys (Yang et al. 2009). Adventive T. japonicus have been discovered emerging from H. halys egg masses in North America (Milnes et al. 2016, Talamas et al. 2015b) and Europe (Stahl et al. 2019, Sabbatini Peverieri et al. 2018). Research has assessed the effectiveness of these adventive populations against H. halys and a recent study in Washington State revealed parasitoid emergence rates reaching 77% (Milnes and Beers 2019). Conversely, initial parasitism of H. halys eggs by T. japonicus in Europe has been as low as 2%. (Stahl et al. 2019).

Though adult wasp emergence has been documented on eggs of some native pentatomidae species, Trissolcus japonicus has shown superior adult emergence rates on H. halys eggs (Milnes and Beers 2019). Laboratory paired-host tests demonstrated significantly higher T. japonicus parasitism rates of H. halys over other stink bug species. However, no-choice tests documented T. japonicus readily parasitising Banasa dimidiata (Say) and Holcostethus abbreviatus Uhler (Hedstrom et al. 2017). Recent field tests in the Pacific Northwest found significantly lower T. japonicus parasitism rates of native stink bug egg masses (0.4–⁠8%) compared to H. halys (77%) (Milnes and Beers 2019). These findings suggest that, although non-target effects occur, natural settings may support more targeted control of H. halys by T. japonicus.

The primary objective of this study was to utilise H. halys egg mass surveys to identify potential parasitoid species for suppression of this invasive insect pest in northern Utah. Northern Utah provides novel geographic and environmental conditions for detection of H. halys parasitoids, most notably high elevation (>1200 m) and arid sites with a hot summer and cold winter climate (Utah Climate Center 2020), as compared to other regions where H. halys occurs (Herlihy et al. 2016, Jarrett et al. 2019, Milnes et al. 2016, Stahl et al. 2019). Secondly, we compared parasitism rates of wild (in situ) versus lab-reared egg masses to better understand effective survey approaches and projection of natural parasitism rates in the field (Abram et al. 2017).

Survey Sites

Surveys for native and exotic parasitoid wasps of H. halys eggs in northern Utah were conducted from June through September in each of 2017, 2018 and 2019. The surveys included a total of 17 field sites. Sites 1, 4, 5, 8 and 10–⁠17 were located in suburban landscapes containing mixed woody ornamental trees and shrubs. Sites 2, 3, 6, 7 and 9 were in conventionally-managed agricultural row crops and orchards (Fig. 1). Survey sites were chosen, based on areas of established H. halys populations and preferred host plant availability (Tables 1, 2).

Table 1.

Download as

CSV

XLSX

Number of deployed and parasitised fresh lab-reared H. halys egg masses by native wasps on multiple plant species in northern Utah from June through September, 2017 –⁠ 2019. Parasitism denotes adult wasp emergence.

Plant Species	Total Egg Masses (Eggs)	Parasitised Egg Masses (Eggs)
Acer negundo	13 (311)	0 (0)
Ailanthus altissima	7 (187)	0 (0)
Catalpa speciosa	62 (1503)	1 (5)
Cercis canadensis	19 (474)	0 (0)
Elaeagnus angustifolia	5 (137)	0 (0)
Helianthus annuus	1 (25)	0 (0)
Malus domestica	48 (1099)	1 (1)
Malus sp.	6 (122)	0 (0)
Prunus armeniaca	11 (277)	0 (0)
Prunus cerasus	12 (298)	0 (0)
Prunus domestica	3 (83)	0 (0)
Prunus persica	17 (453)	3 (7)
Robinia pseudoacacia	3 (73)	0 (0)
Sambucus sp.	6 (168)	0 (0)
Zea mays	22 (559)	0 (0)

Table 2.

Download as

CSV

XLSX

Number of deployed and parasitised wild H. halys egg masses by all wasps, native and exotic, on multiple plant species in northern Utah from June through September, 2017–⁠2019. Parasitism denotes adult wasp emergence.

Plant Species	Year	Total Egg Masses (Eggs)	All Parasitised Egg Masses (Eggs)	Egg Masses Parasitized by T. japonicus (Eggs)*
Acer grandidentatum	2018	1 (22)	1 (1)	0 (0)
Catalpa speciosa	2017	4 (108)	1 (4)	0 (0)
	2018	6 (164)	1 (7)	0 (0)
	2019	105 (2791)	43 (796)	21 (452)
Prunus cerasus	2018	1 (28)	0 (0)	0 (0)
	2019	1 (28)	0 (0)	0 (0)
Zea mays	2017	1 (28)	0 (0)	0 (0)

* Wasp identity confirmed upon adult emergence from H. halys eggs.

Figure 1.  

Blue dots indicate deployment and collection sites of lab-reared and wild egg masses in northern Utah, 2017-2019. Trissolcus japonicus was discovered at Sites 1 and 17. Geographical coordinates are as follows: Site 1: 40°46'14.8"N, 111°51'18.6"W; Site 2: 41°3'36.899"N, 112°0'46.944"W; Site 3: 41°45'48.39"N, 111°48'46.148"W; Site 4: 41°44'11.685"N, 111°49'14.446"W; Site 5: 41°43'41.968"N, 111°49'4.005"W; Site 6: 41°11'9.164"N, 112°2'25.368"W; Site 7: 41°1'18.787"N, 111°55'59.663"W; Site 8 40°16'07.6"N, 111°39'20.7"W; Site 9: 41°01'12.2"N, 111°55'49.4"W; Site 10: 40°59'44.2"N, 111°53'09.8"W; Site 11: 40°45'08.2"N, 111°52'25.2"W; Site 12: 41°44'32.9"N, 111°48'32.8"W; Site 13: 41°03'37.0"N, 111°58'13.8"W; Site 14: 40°46'03.3"N, 111°49'27.5"W; Site 15: 41°01'13.1"N, 111°56'12.9"W; Site 16: 40°46'23.0"N, 111°52'07.3"W; and Site 17: 40°46'49.3"N, 111°53'46.5"W.

Stink Bug Colony

Survey Methods

Statistical Methods

Voucher Specimens

Over the three year survey period, a total of 39 parasitoids from five native wasp species emerged from six wild and five lab-reared H. halys egg masses. Anastatus mirabilis (Walsh & Riley), A. pearsalli Ashmead, A. reduvii Ashmead, Trissolcus euschisti (Ashmead) and T. hullensis (Harrington) were documented from both guarding females and successful emergence from H. halys egg masses (Fig. 2). Trissolcus utahensis (Ashmead) and Telenomus podisi Ashmead were observed guarding H. halys eggs, but did not successfully emerge as adults. Catalpa speciosa (Warder), Malus domestica Borkh and Prunus persica (L.) Batsch were the only plant species on which lab-reared egg masses were parasitised and this parasitism was by native wasp species exclusively (Table 1). In June 2019, the Asian parasitoid T. japonicus was first discovered in Utah emerging from two wild H. halys egg masses at Site 1 in Salt Lake City (Figs 1, 2, 3) and was detected consistently from June through September. Further, a single egg mass with emergent T. japonicus was found at Site 17 in August 2019. Trissolcus japonicus was only detected at these two suburban landscape sites. A total of 452 T. japonicus emerged from 21 of the 106 wild egg masses found in 2019 (Fig. 2). Parasitised wild egg masses were collected on two tree species, C. speciosa and Acer grandidentatum Nutt, with attack by T. japonicus occurring only on C. speciosa (Table 2).

Figure 2.  

Percent parasitism (± SE) of eggs in wild and lab-reared egg masses with adult wasp emergence in northern Utah, 2017–⁠2019. Sample size (n) represents the number of egg masses parasitised by the indicated wasp species in each year. Bars without standard error lines represent single egg masses. The Unknown category represents egg masses in which parasitoid wasp emergence was confirmed, but no wasp specimens remained to confirm species identification.

Figure 3.  

Photo of female Trissolcus japonicus (FSCA 00090662), found in Salt Lake City, Site 1, on 17 June 2019. Key identifying characters include the episternal foveae occurring in a continuous line from the postacetabular sulcus to the mesopleural pit.

When native wasp species successfully emerged from H. halys eggs, the mean number of parasitised eggs per affected egg mass was low, 4–25%. When considering only those egg masses giving rise to adult T. japonicus in 2019, the mean egg parasitism rate per mass was 78.5%. Additionally in 2019, a group of 19 wild egg masses experienced a similarly high mean parasitism rate of 67.3%, though these egg masses did not have adult wasps present at the time of collection, only signs of chewing and emergence (Fig. 2).

Mean parasitism of lab-reared egg masses was 0.42% and 0.05% in 2017 and 2018, with no wasps emerging in 2019. Mean parasitism rates of wild-collected egg masses in 2017, 2018 and 2019 were 2.9%, 3.7% and 28.2%, respectively (Table 3). The generalised linear model did not reveal a significant two-way interaction between year and egg type (P = 0.196, F_2,348 = 1.63). Significantly more wasps emerged from wild than lab-reared egg masses (P = 0.002, F_1,348 = 9.50). There were no significant differences in mean wasp emergence amongst years (P > 0.797, F_2,348 = 0.23).

Surveys of wild and lab-reared H. halys eggs in northern Utah demonstrated relatively high diversity of native parasitoid wasps, but these native species all exhibited low rates of parasitism. These findings are congruent with other North American surveys of H. halys egg parasitoids (Dieckhoff et al. 2017, Abram et al. 2019b). Low native parasitism rates could be caused by deterrence from natural chemical defences on and within H. halys eggs or a lack of effective venom at the time of female oviposition needed for successful wasp development in the exotic host egg (Haye et al. 2015a, Tognon et al. 2016). Other research suggests that the use of parasitism emergence as a metric of parasitoid effectiveness underestimates native wasp effects on H. halys eggs since partially-developed wasps that do not complete emergence often kill the stink bug host (Abram et al. 2019a, Cornelius et al. 2016b, Schumm 2020). Although our egg dissections revealed many unhatched H. halys eggs with undifferentiated contents (Milnes and Beers 2019), the ultimate cause of egg death could not be ascertained.

Our results support those of Jones et al. (2014) and Abram et al. (2017) who found that wild (in situ) egg masses more accurately detect the presence and ability of parasitoid wasps to emerge from H. halys eggs than do field-deployed lab-reared egg masses. This difference may be due to a variety of factors, including the age of the egg mass upon deployment, length of egg mass exposure to field conditions and deployment height of egg masses in host trees. Hedstrom et al. (2017) noted the importance of semiochemical cues associated with the success of T. japonicus in finding and stinging H. halys egg masses. Research by Boyle et al. (2019) has also shown that kairomones, left by H. halys on host plant leaves, are detectable by T. japonicus and the wasp resides on these leaves longer than those lacking such kairomones. Therefore, lower parasitism rates of lab-reared egg masses could be due to reduced chemical cues.

Although current parasitism by the exotic T. japonicus in northern Utah is modest, relative to those in its native range (Yang et al. 2009, Zhang et al. 2017), our results indicate that T. japonicus has the potential to provide biological control of H. halys in the Intermountain West. Parasitism rates were not shown to be different amongst years, but our data clearly show higher parasitism in 2019, when T. japonicus was discovered, as compared to previous years. The dissonance of biological and statistical conclusions in our results is likely due to the variable and low sample size of egg masses. Trissolcus japonicus may have killed more H. halys eggs than we were able to document, based on identification of the causal wasp. Indeed, many egg masses were attacked by parasitoids that had already emerged from eggs before collection in 2019, with higher mean parasitism rates in affected egg masses than those observed for native wasp species, suggesting that at least some of the unidentified parasitoids were T. japonicus. It is also of interest to point out that T. japonicus was detected in two suburban landscape sites in Salt Lake County in 2019 and not in agricultural sites.

The northern Utah region differs in its climate and topography from most locations in which T. japonicus has been documented or predicted to become established in North America (Avila and Charles 2018). Given the arid, high elevation conditions of northern Utah that include cold winters and hot summers, detection of an adventive T. japonicus population implies potential for range expansion into other locations within the greater Intermountain West region. These results support the possibility of an eventual intersection of eastern and western T. japonicus populations in North America (Jarrett et al. 2019, Talamas et al. 2015b, Milnes et al. 2016). Further research should focus on the capacity of T. japonicus to persist in the Intermountain West, specifically focusing on overwintering behaviour where heavy snowfall accumulation and consistent sub-zero temperatures occur (Lowenstein et al. 2019, Nystrom Santacruz et al. 2017). In fact, follow-up surveys in 2020 have documented continued detection of T. japonicus in Salt Lake and expansion into Utah counties (K. Richardson, personal communication). Laboratory rearing and releases, in conjunction with conservation efforts, are critical next steps in supporting the future establishment of T. japonicus populations in Utah.

Our findings show that an adventive population of T. japonicus in northern Utah is causing higher levels of reproductive parasitism of H. halys eggs compared to native wasp species and wild (in situ) egg masses provide a more accurate measure of parasitoid activity compared to those deployed from lab colonies. This study reports the first detection of T. japonicus in the Intermountain West, a novel geographic location for this parasitoid in North America.

We thank Kate Richardson, Hanna Kirkland, Chelise Dever, Stephanie Hall, Erin Berdahl, Lily Bourett, James Withers, Loren Linford, Ben Steadman and Ryan West for their assistance with field research. In addition, we thank Susan Durham for statistical support and pre-submission review of the manuscript. Funding was provided by the National Institute of Food and Agriculture, U.S. Department of Agriculture, Specialty Crop Research Initiative under award number 2016-51181-25409; USDA Specialty Crop Block Grant; Utah Department of Agriculture and Food; Western Sustainable Agriculture Research and Education program under award number 2017-38640-26913 and subaward number [GW18-106]; USDA APHIS PPQ under cooperative agreements AP18PPQFO000C099 and AP19PPQFO000C343; and Utah State University Extension. This research was supported by the Utah Agricultural Experiment Station, Utah State University and approved as journal paper number 9313. Elijah Talamas was supported by the Florida Department of Agriculture and Consumer Services-Division of Plant Industry and the USDA Farm Bill: Identification, monitoring and redistribution of Trissolcus japonicus – Biological Control of Brown Marmorated Stink Bug (BMSB). USDA is an equal opportunity employer and service provider. Maps throughout this study were created using ArcGIS® software by Esri. ArcGIS® and ArcMap™ are the intellectual property of Esri and are used herein under licence. Copyright © Esri. All rights reserved. For more information about Esri® software, please visit www.esri.com.