Enhancement of Samurai Wasp [Trissolcus japonicus (Ashmead)] for Biocontrol of Invasive Brown Marmorated Stink Bug [Halyomorpha halys (Stål)] in Utah

Progress report for GW21-221

Project Type: Graduate Student
Funds awarded in 2021: $30,000.00
Projected End Date: 12/01/2022
Host Institution Award ID: G219-22-W8615
Grant Recipient: Utah State University
Region: Western
State: Utah
Graduate Student:
Major Professor:
Dr. Diane Alston
Utah State University
Major Professor:
Curtis Rowley
Cherry Hill Farms
Dr. Lori Spears
Utah State University
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Project Information

Summary:

The brown marmorated stink bug (BMSB, Halyomorpha halys Stål) is an invasive insect that feeds on specialty fruit and vegetable crops in North America. Current management of H. halys relies heavily on broad-spectrum insecticides which are only moderately effective and disrupt sustainable integrated pest management (IPM) programs by killing natural enemies and contributing to insecticide resistance and secondary pest outbreaks. The T. japonicus [Trissolcus japonicus (Ashmead)], a highly effective biocontrol agent native to the home range of H. halys, has shown strong promise in providing long-term and effective management of H. halys. While adventive populations of T. japonicus have been discovered in Utah, geographic distribution and climate models suggest this region is only marginally suitable. Utah’s high-elevation climate provides unique challenges to wasp establishment; therefore, conservation efforts are critical next steps to enhance T. japonicus populations. The objectives of this research are to answer: 1) What is the distribution of T. japonicus in northern Utah specialty crops and nearby urban areas, and how does the diversity of understory vegetation influence their abundance? 2) Which cover crops can increase wasp lifespan and fecundity? 3) How effective are stink bug host chemical cues (kairomones) in attracting the T. japonicus and increasing stink bug egg parasitism rates? Results will be disseminated to specialty crop producers and other stakeholders through multiple presentations (grower meetings and field days), two extension fact sheets, one newsletter article, and two research journal publications. This research will produce applicable information that supports improved sustainability of H. halys management and reduced economic losses to specialty crops.

Project Objectives:

My research will focus on the status, conservation, and enhancement of an effective egg parasitoid, the samurai wasp, [Trissolcus japonicus (Ashmead)] of the invasive insect pest, brown marmorated stink bug (BMSB) (Halyomorpha halys Stål) in northern Utah by pursuing the following objectives:

  • Objective 1- Determine the establishment and spread of the T. japonicus (e.g., overwinter survival) since its first detection in northern Utah in June, 2019, including assessment of the impacts of understory vegetation diversity on its occurrence and abundance.
  • Objective 2- Determine cover crop floral resource candidates to attract and sustain the T. japonicus, including impacts on wasp lifespan and reproduction.
  • Objective 3- Determine the viability of stink bug host chemical cues (kairomones) in attracting T. japonicus and increasing egg parasitism rates in both a field and mesocosm setting.

After reviewing preliminary results from Objective 2, research efforts were shifted towards a second experiment as a part of Objective 3 (mesocosm arena assessment of T. japonicus response to kairomones).

My educational objectives will focus on increasing the knowledge of specialty crop producers, research and extension colleagues, the general public, youth, and other interested stakeholders on conservation and enhancement of the T. japonicus for biological control of the invasive brown marmorated stink bug (BMSB; Halyomorpha halys).

  • Objective 1- Promote the T. japonicus for the sustainable management of BMSB to approximately 10,000 specialty crop producers and other relevant stakeholders.
  • Objective 2- Add to the national H. halys research knowledge base and share project results with professional colleagues through two journal publications and three scientific conference presentations.
  • Objective 3- Disseminate information on invasive species and sustainable pest management to the general public via varied outreach venues and formats.
Timeline:

Preliminary research and planning for this project began the summer of 2020 which resulted in the foundation of this proposal. Data collection for research objectives 1-3 will begin in May 2021 to take advantage of the active season for BMSB and samurai wasp and not exclude essential data collection. Student summer funding for 2021 is available to support this work from a USDA Utah Department of Agriculture and Food Specialty Crop Block Grant; however, this funding will be insufficient to achieve this project’s goals. The funds received from this grant will be used to support the completion of the research and outreach objectives as outlined above. Follow up will be focused on assessing the impacts and success of each objective, as outlined in the Evaluation and Producer Adoption section of the narrative, and preparing for grantee reporting.

[caption id="attachment_751035" align="alignnone" width="780"]Gantt chart showing timing of objectives *Data collection will begin May 2021 before the grant funding cycle begins.
**Data collection for the Y-tube olfactometer experiments portion of this objective are currently underway. Within the grant period follow up experiments will be completed as needed and data will be analyzed.[/caption]

Cooperators

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Research

Materials and methods:

Objective 1- Determine the establishment and spread of the T. japonicus (e.g., overwinter survival) since its first detection in northern Utah in June 2019, including assessment of the impacts of groundcover vegetation diversity on its occurrence and abundance.

Rationale

Preliminary research in 2020 found that the T. japonicus was primarily detected in urban landscapes, had successfully overwintered, and had expanded its distribution despite the unique climate challenges of northern Utah (Fig. 1). However, one year of overwinter survival is insufficient evidence of establishment; further study is necessary to fully understand the wasp’s overwintering ability, climate tolerance, and potential expansion, particularly within agricultural landscapes, in northern Utah. Comparing the effects of understory vegetation diversity on wasp abundance will provide further insight into foundational resource needs for the T. japonicus and methods to enhance its establishment in urban and agricultural landscapes.

Common methods of monitoring for parasitoid wasps are yellow sticky card deployments, collection of wild H. halys egg masses, and deployment of sentinel (lab-reared) H. halys egg masses. These methods proved effective in detecting the T. japonicus in 2019 and 2020 (Holthouse et al. 2020; K. Richardson, unpublished data), were used to compare the abundance of T. japonicus to native parasitoids in yellow sticky card surveys (Fig. 2), and to analyze parasitism success on wild egg masses (Fig. 3). Results from the following proposed methods will add to 2020 data on abundance and parasitism rates and will be used to build distribution and climate/habitat suitability maps.

 

Materials and Methods

Yellow sticky cards (YSC) (Alpha Scents, Inc 8 x 5.5 in) were placed at 24 sites in urban-agricultural interface and specialty crop landscapes in northern Utah. Orchard sites were selected based on understory vegetation diversity (bare soil, turf, or floral/broadleaf weed ground cover) with each understory type replicated 8 times (Table 1). A total of 10 deployments were conducted 19 May through 11 October 2021 in two-week intervals. Sticky cards were secured to a branch at 2 m height on peach, apple, and tart cherry orchard trees.

Upon retrieval, YSC were examined under a stereomicroscope (Leica Stereozoom S9E, Leica Microsystems Inc.) with 98–880x magnification for the presence of Trissolcus spp. Wasps were initially removed on a small piece of YSC, then soaked in Histo-Clear II histological clearing fluid (National Diagnostics, Atlanta, GA) for ~5–7 min to dissolve adhesive and mounted on a cardstock point via clear fingernail polish and insect pin to allow for species identification. Due to capture of large numbers of Trissolcus spp. on 23 August to 11 October of 2021, wasp specimens were directly identified on small pieces of YSC to reduce processing time, and only removed if required for species identification. All Trissolcus specimens were identified to species-level following the key to Nearctic Trissolcus (Talamas et al. 2015a). Some Trissolcus specimens were unidentifiable beyond genus level due to physical damage. Intact parasitoid wasps were either point mounted or pinned through YSC pieces, labeled, and stored in the Alston Lab, Department of Biology, Utah State University, Logan, UT. Voucher specimens were deposited in the Utah State University Insect Collection (https://biology.usu.edu/research/research_centers/insect-collection).

Abundance detection maps were built in ArcGIS Pro (version 2.9.0). The abundance of T. japonicus and native Trissolcus spp. found on YSC at Utah orchard sites was analyzed using a generalized linear mixed model (GLMM) assuming a negative binomial distribution.  Groundcover and time (deployment) were main fixed effects and sampling site was treated as a random effect. GLLM and subsequent pairwise comparisons using EMMs were run using R software (R version 3.6.1; R Core Team 2019).

Objective 2- Determine cover crop floral resource candidates to attract and sustain the T. japonicus, including impacts on wasp lifespan and reproduction.

Rationale

Research has shown that non-crop host plants can be critical in providing essential food and habitat resources to beneficial insects, such as predators and parasitoids (Baggen and Gurr 1998; Hickman and Wratten 1996). Effectiveness and longevity of parasitoid wasps can significantly benefit from floral resources such as nectar and pollen (Jervis et al. 1992; Lee et al. 2004). This study will focus on cover crops because of their benefits and appropriateness to agricultural production systems. Many growers already use cover crops for the benefits of soil conditioning, weed and erosion management, and attraction of beneficial insects.

Although McIntosh et al. (2020) explored the impact of eight flowering plant species on T. japonicus survival in the laboratory, only two of the previous plants will be tested in this study (buckwheat and sweet alyssum). The remaining flowers in their study (dill, cilantro, marigold, crimson clover, yellow mustard, and phacelia) are either more appropriate for small garden plantings than large commercial specialty crop production fields or are inappropriate for the Intermountain West region. No other studies have explored the use of cover crop floral resources, appropriate to intermountain regions, for enhancement of T. japonicus.

 Material and Methods

Here, the attractiveness of four cover crops: alfalfa [Medicago sativa (L.)], buckwheat [Fagopyrum esculentum (Moench)], red clover [Trifolium pratense (L.)], and sweet alyssum [Lobularia maritima (L.) Desv.] to T. japonicus females were assessed using a Y-tube olfactometer.  A single, mated, unfed female wasp (24-48 hr old) from the USU T. japonicus colony (originating from females collected in 2019 from Salt Lake City, Utah) was placed in a Y-tube olfactometer, made from a glass tube body (90 mm stem, 80 mm arms, 15 mm internal diameter), with approximately 0.5 g of floral material on one side of the Y and a blank control on the other (following similar methods outlined in Bertoldi et al. 2019; Salerno et al. 2002; Zhong et al. 2017). Flowers were grown from seed in the USU research greenhouse and charcoal filtered airflow was maintained at a rate of 90-110 cc/min. Wasps were carefully inserted into the Y-tube entrance of the central stem and observed for five minutes. Residence time in each arm of the olfactometer were recorded. The olfactometer was rotated after every fifth parasitoid to negate a possible left vs right side bias and cleaned with laboratory detergent and deionized water between each flower species.

Objective 3- Determine the viability of stink bug host chemical cues (kairomones) in attracting T. japonicuss and increasing egg parasitism rates in a field setting. 

Rationale

Though sentinel H. halys egg masses are a common way to assess wasp parasitism rates, studies have shown that lab-reared egg masses underestimate parasitism rates and attract fewer wasps than wild egg masses. This is thought to be because the T. japonicus uses volatile chemicals released by H. halys during host feeding and oviposition (Abram et al. 2017; Holthouse et al. 2020; Jones et al. 2014). Research by Malek et al. (in review) found that combining the H. halys host kairomones of n-tridecane and (E)-2-decenal at a ratio of 4:1 was highly attractive to T. japonicus adults in a Y-tube olfactometer experiment. However, another study found the ratio of 9:1 used in a field experiment demonstrated little success, possibly due method of delivery (filter paper) and rapid volatility of the chemicals (J. Kaser, personal communication). There is evidence of wasp attraction to these kairomones in a lab setting, but more research is needed to understand how they perform in agricultural field settings.

Materials and Methods

Experiment 1

To assess attractive chemicals in a field setting, custom rubber septa lures (loaded with 10 mg of test compounds) were developed by Trécé Inc., (Adair, OK). We tested four lure treatments in field trials with varying ratios of n-tridecane to (E)-2-decenal: 1:0, 9:1, 4:1, and hexane (control). Lab-reared H. halys sentinel egg masses were deployed adjacent to kairomone lures as hosts for parasitoid wasps.

Trials (n=6) were conducted from 24 June through 27 August 2021 in a strip of residential Catalpa speciosa trees in Salt Lake City, UT (40.77248026310703, -111.85497554923636). Catalpa trees were selected because they have been a consistent and highly suitable host plant for H. halys, composing 91% of H. halys detected in northern Utah in a recent host plant study (Holthouse et al. 2021). Treatments were replicated in four trees (three trees in the final deployment due to a lack of egg masses) with a blank buffer tree between each treatment tree. Each replicate tree contained four H. halys egg masses and one of each lure-treatment with one mass and lure placed approximately two meters laterally from the trunk of the tree at each cardinal direction. Halyomorpha halys eggs were attached to small rectangles of white cardstock (2 cm by 3 cm) and clipped with a lure to the underside of tree leaves (Fig. 5). Treatments were placed at approx. 2 m height above the ground with cardinal direction of treatments randomized for each tree in each deployment.

Egg masses (n=92) were ~48 hr old upon deployment and produced from an H. halys lab colony at the Oregon Department of Agriculture. Sentinel egg masses were deployed in the field for approximately 96 hr and returned to the lab for evaluation. Any wasps found guarding egg masses were collected into a 9-dram plastic vial (Thornton Plastics, Salt Lake City, UT) using an aspirator. After an incubation period of 14 days, eggs were evaluated for parasitism incidence and intensity, and emerged wasps were identified to species using the key to Nearctic Trissolcus (Talamas et al. 2015a). Egg masses were observed again four weeks after collection to identify late-emerging wasps or those with partially developed wasps or stink bugs within eggs. Individual egg fate was recorded as black goo (undeveloped egg and/or parasitoid), unhatched or hatched H. halys nymph, predated, sunken, empty, and missing. A generalized linear mixed model with a binomial distribution with observation-level random effects (OLRE) for overdispersion was used to analyze differences in egg fate by lure treatment, block (tree), and deployment date (trial).

Experiment 2

In order to mitigate many of the uncontrollable factors in a field setting, we are testing a mesocosm-scale lab-based experimental system in 2022. The goal of this experiment is to further explore the use and attraction of kairomone-loaded rubber septa lures in a controlled environment that supports parasitoid wasp moement and choice of H. halys egg masses for parasitism.

Experiment 2 will be set up in a 0.5 height x 0.5 depth x 1 m length mesh observation cage with quarter portions (15.25 X 15.25 cm) of a clear panel trap (Alpha Scents, Inc, 30.5 X 30.5 cm) and lure attached via a clothespin to the upper portion of the card piece hung at either end of the cage (1 m apart). Four to five naïve female Trissolcus japonicus will be introduced to the middle of the cage via a small access sleeve and allowed up to 30 min to select a treatment lure and card (2-way choice). In this experiment, different load rates of n-tridecane (1, 2.5, 5, and 10mg) be tested against a control as well as against each other and a higher number of replications can be performed. It will be valuable to test a range of lure load rates to determine if the high load rate of the 10 mg lures used in the previous experiment may have repelled adult parasitoids. We expect to run 10-15 replications conducted in a temperature controlled rearing room at 21–27°C and 30-50% RH. An additional experiment would use the same experimental setup but use H. halys egg masses instead of sticky cards so that parasitism rates can be assessed.

*Field research will begin before the start of the grant funding cycle.

Tables and Figures

Table 1. Objective 1 sites (n=24) in urban-agricultural interface and specialty crop landscapes in northern Utah

Groundcover

Site ID

County

Latitude

Longitude

Elevation (m)

Crop

Bare

B1

Box Elder

41.4475

-112.03740

1597

Peach

 

B2

Box Elder

41.4222

-112.03153

1597

Peach

 

B3

Box Elder

41.4128

-112.03087

1517

Peach

 

B4

Weber

41.3157

-111.95857

1347

Peach

 

B5

Davis

41.0361

-111.90632

1468

Peach

 

B6

Utah

40.3372

-111.71865

1417

Peach

 

B7

Utah

40.3131

-111.71038

1402

Apple

 

B8

Utah

40.0456

-111.86118

1458

Apple

Floral

F1

Cache

41.8138

-111.8096

1416

Apple

 

F2

Box Elder

41.4238

-112.03349

1597

Peach

 

F3

Weber

41.1855

-112.04066

1354

Peach

 

F4

Utah

40.0402

-111.85459

1375

Peach

 

F5

Utah

40.0291

-111.83839

1375

Tart Cherry

 

F6

Utah

40.0039

-111.82487

1476

Tart Cherry

 

F7

Utah

39.9969

-111.83255

1497

Tart Cherry

 

F8

Utah

39.9825

-111.82606

1497

Peach

Turf

T1

Cache

41.7254

-111.80753

1410

Apple

 

T2

Box Elder

41.6934

-112.30342

1431

Peach

 

T3

Cache

41.5817

-111.84779

1521

Apple

 

T4

Weber

41.3305

-112.00916

1303

Peach

 

T5

Davis

41.0214

-111.93194

1318

Peach

 

T6

Utah

40.0231

-111.70732

1534

Peach

 

T7

Utah

40.0127

-111.77738

1422

Tart Cherry

 

T8

Utah

39.9926

-111.76879

1520

Tart Cherry

 

Samurai wasp is found in Salt Lake City in 2019 and expanded locations north and south in 2020.
Figure 1. Trissolcus japonicus detections in northern Utah on yellow sticky cards between May and September, 2019-2020.
Samurai wasp is less abundant compared to native parasitoid wasps.
Figure 2. Proportion of parasitoid wasp species detected on yellow sticky cards in 2020. Trissolcus japonicus (samurai wasp) is the only introduced parasitoid, all others are native to Utah.
Samurai wasp showed high parasitism rates.
Figure 3. Proportion of target wasps found parasitizing BMSB wild egg masses in 2020. Trissolcus japonicus (samurai wasp) is the only introduced parasitoid, all others are native to Utah.
Y-tube glass piece
Figure 4. Y-tube olfactometer.

egg mass with lure

Figure 5. Deployed lab-reared H. halys egg mass (center) with adjacent kairomone lure.

 

Research results and discussion:

Objective 1:

Results

Trissolcus japonicus was detected at 17 out of the 24 orchard sites, of which 16 were new detection sites for the exotic species. It was detected in Box Elder and Cache cos. for the first time and showed continued detections in Davis, Utah, and Weber cos (Figure 1).

T. euschiti captures were the most abundant (79.8%) followed by T. utahensis (7.2%), T. japonicus (2.8%), T. hullensis (1.8%) and T. ruidus (<.1%)(Table 1). A little more than 8% of Trissolcus captures were unidentifiable beyond genus due to damaged specimens. Bare and floral sites had a similar number of detections (46% and 40%, respectively) while turf had 16% detections. Bare and floral sites had a similar proportion of total Trissolcus detections (46% and 40%, respectively) while turf had 16% of detections.

 For Trissolcus spp. as a whole, the effect of groundcover was not statistically significant (p>0.05). All groundcover types had increases in abundance beginning August 10 (Figure 2) and the effect of deployment (time) did show a significant effect on the number of detections (p<0.001). Detections were significantly higher in deployments 8-9 (24 August - 20 September) compared with the majority of the season (Table 2).

A total of 68 T. japonicus were captured on YSC; 34 (50%) were captured in bare orchards, 24 (35%) in floral, and 10 (15%) in turf. Similar peaks were seen as to the full complement of Trissolcus, though increases occurred one deployment sooner starting July 27 (Figure 3). There was no evidence of significant differences due to groundcover (p>0.05) or deployment (time) (p>0.05), likely due to low detections overall. The highest number of T. japonicus on any single YSC was 13 wasps and the average for cards with positive detections was 2.26 (±0.47).

Discussion

The analysis of this study is still underway. These data were analyzed with deployment as a categorical variable, but we are currently working on analyses using a degree day scale to better understand the effect of seasonality and timing of peak populations for both T. japonicus and our native parasitoids. We are also interested in looking at additional factors that may affect Trissolcus and T. japonicus abundance such as H. halys presence/abundance, surrounding habitat, and tree fruit type.

Objective 2:

Results

Preliminary results for this experiment were disappointing. When placed in the y-tube apparatus, T. japonicus individuals did not select an odor preference in most experimental runs. Many individuals remained within the insertion tube or in the main stem for the duration of the 5 min without making a choice. After adjusting air flow, the trial wasps would choose to move around the y-tube back and forth between the two arms with no distinct searching behaviors. Results for preliminary trials (Figure 4) show there was little difference between the control and floral odor arm residence times. ANOVA tests run on the pairs did not show statistical differences. As more trials were run, the average residence time became increasingly similar as seen in the buckwheat trials (n=46).

As part of the wasp longevity and fecundity trials we only ran a few trials to test experimental set up. The few preliminary trials that were run suggest that buckwheat, alyssum, alfalfa, and red clover may be life sustaining, while hairy vetch and birdsfoot trefoil show much less promise as wasps died within a 48 hr period.

Discussion

After reviewing preliminary results, numerous adjustments were made to the experimental equipment and design, including air flow, floral load, and pre-experiment feeding status of wasps. Eventually, the decision was made to not continue this study. Our experimental set up and/or equipment did not seem to be an appropriate means to measure T. japonicus attraction to floral resources.

The results for the y-tube experiment were to determine which flowers should be tested as part of the wasp longevity and fecundity trials. Without the initial results to verify which floral resources may be attractive, we chose to cancel the wasp longevity and reproduction trials. Resources that are life sustaining, but not attractive to T. japonicus, serve little benefit in an agricultural setting without attractive volatiles to guide the wasps to floral resources.  

At this point, the study of kairomones as part of objective 3 was showing great promise, but the results were inconclusive due to low parasitism rates. We decided to shift our research focus away from this objective 2 study in favor of being able to perform a more controlled kairomone experiment in a mesocosm arena as part of objective 3.

Objective 3:

Results

Overall, low levels of parasitism by two Trissolcus species were observed in this experiment. Out of 92 total egg masses deployed, 13 masses had evidence of parasitism (14.1%; guarding female or eclosed parasitoids) of which 6 masses supported successful emergence of adult parasitoids (6.5%). The lure treatments in order of highest proportion of eggs with successfully emerged parasitoids were 1:0 n-tridecane to (E)-2-decenal (10.6%), hexane control (4.7%), 4:1(1.3%), and 9:1 (0%) (Table 3, Fig. 5). Though the 1:0 lure showed double the parasitism of the control and more than eight times that of the 9:1 and 4:1, these results were not statistically different (p > 0.05) due to highly zero-inflated data.

Of the 129 H. halys individual eggs parasitized by Trissolcus japonicus, there was a high rate of successful wasp development and adult emergence (78.3%), while T. euschisti had low emergence (1.6%) from the 191 eggs it parasitized (Table 4). Trissolcus euschisti attempted to parasitize 6.5% of all egg masses deployed, and T. japonicus attempted to parasitize 5.4%. Two egg masses (2.2%) were parasitized by an unknown Trissolcus spp. (Table 4). In one instance, a T. euschisti female was found guarding an egg mass which later produced 26 T. japonicus individuals (92.9% emergence rate) and 2 inviable eggs.

Discussion

This study is the first to assess kairomone-infused rubber septa lures to attract T. japonicus and other potential H. halys parasitoids in a field setting. Though the kairomone chemicals tested herein have been previously evaluated in a lab setting, implementation in the field may provide different results due to the influence of numerous external factors on the shape, concentration, longevity, and spatial extent of the kairomone odor plume. In addition, mixing of the lure plume with nearby plant surfaces and volatiles may give rise to plume masking or plume amplification, of which little is known in a parasitoid searching context (Dicke et al. 2003). Our results contrast those of Malek et al. (2020) where the combination of the attractant and repellent was more attractive than the attractant alone. In our study, not only did the n-tridecane-only lure have a numerically (not statistically) higher parasitism rate than the control, the lures containing the previously identified repellant (E)-2-decenal had less parasitism than those without the repellant, including the hexane control. These results might suggest that under field conditions a combination of the attractant and repellant is not effective in attracting Trissolcus sp., at least with this specific load rate and placement adjacent to the target egg mass. However, given the low number of egg masses tested and lack of statistically significant results, the parameters of this study may have been unsuitable to discern differences in attractiveness of the different kairomone lure treatments.

The lures used in this study contained a load rate of 10 mg per lure, high in comparison to standard pheromone lures (1 mg), in the hopes of ensuring the attraction of parasitoids (Danielle Kirkpatrick, Trece Inc., personal communication); however, this relatively high load rate may have been counterproductive to enhancing parasitism of adjacent H. halys egg masses. In studies of pheromone lure load rates, it has been found that attraction often plateaus and can even become repellant to the insect at high release rates (Charles et al. 2015; Knight et al. 2005; Stelinski et al. 2021). In addition, our lures were placed directly adjacent to the H. halys egg masses (Fig. 5), which might be a deterrent to parasitoid attraction as the host female stink bug does not typically remain near the eggs following oviposition.

The results observed in this study further verify the preliminary research in Utah on the effectiveness of the exotic T. japonicus and the common native T. euschisti. In this study as in others (Holthouse et al. 2020, K. Richardson, unpublished data), T. euschisti has the ability to parasitize H. halys and attempts to at an almost equal proportion to the natural parasitoid of H. halys, T. japonicus. However, T. euschisti is an inviable option for successful biological control due to low adult emergence success, additionally posing an evolutionary trap for this native species.

We observed low parasitism rates across all egg mass deployment periods in this study. The site we chose for this experiment has previously had the highest abundance of T. japonicus observed in Utah with concomitant high parasitism rates of H. halys. However, compared to T. japonicus populations in its native geographic regions and other adventive populations in the US, the abundance of T. japonicus in Utah is relatively low (Quinn et al. 2021; Talamas et al. 2015b).  In addition, Utah has suffered from significant drought over the time frame of this study with 99.9% of the state in “extreme” or “exceptional” drought categories (Utah DNR 2021) which may have had a negative effect on host abundance, parasitoid wasp populations, and H. halys egg parasitism rates (Zhu et al. 2012).

 Other researchers have observed that lab-reared egg masses perform inferiorly to wild egg masses in terms of their attractiveness to parasitoids (Abram et al. 2017; Holthouse et al. 2020; Jones et al. 2014). The lures tested here were an initial attempt to solve this issue and increase the accuracy of parasitism rates detected in deployed egg masses. Parasitism was observed in wild egg masses near deployed, unparasitized egg masses during the study. This may suggest the lures were attracting parasitoids to the general area, but were ineffective, or even repellant as a close-range chemical cue. These observations may have been the result of dispersion and/or absorption of the kairomone lure plume and greater attractiveness of wild egg masses with their natural kairomones intact. Without an in-depth analysis on the release rate of these lures, it is unknown if the plumes for each lure treatment may have overlapped within the tree block, and potentially interfered with one another. It is also possible that the chemicals were absorbed and retained in the plant material adjacent to the deployed lures. An attempt to mitigate this possibility was to remove the leaf to which the lure was directly attached post-experiment, but nearby leaves and bark may have absorbed kairomone chemicals.  In either case, the repellant effect of the (E)-2-decenal or high load rate may have reduced parasitism for all deployed egg masses. This research provides preliminary results and a basis for planning of future work with experimental lures in a field environment.

The addition of experiment two under this objective will mitigate many of the unknown and unpredictable factors of experiment one. Running these trials in a mesocosm in a controlled lab setting will remove the variability of weather, including storms that may cause lost egg masses and data, as well as drought which may affect wasp populations and/or searching behavior. In the mesocosm environment, it is also possible to control the number of T. japonicus allowed to respond to the lures and parasitize egg masses. Research in Utah has demonstrated the ability of T. japonicus to parasitize more egg masses than native wasps (Holthouse et al. 2020), but was not upheld in experiment one results for unknown reasons. Supplying a larger number of wasps to experiment two will allow us to discern if the lack of parasitism in our study was due to overall population sizes at the field site or due to some aspect of the lures themselves. Additionally, testing different load rates will shed light on the sensitivity of T. japonicus to kairomone chemicals tested, and determine where lures should be placed in a field setting to optimize parasitoid response and H. halys suppression.

Tables and Figures

Table 1. The number of Trissolcus spp. identified on yellow sticky cards in orchards with bare, floral, and turf landscapes. Proportional abundance of each species by groundcover type is provided in parentheses. Data was collected 19 May through 11 October 2021 in northern Utah.

Groundcover

T. japonicus

T. euschisti

T. utahensis

T. hullensis

T. ruidus

Trissolcus spp.*

Total

Bare

34 (0.03)

905 (0.80)

80 (0.07)

12 (0.01)

1 (0.00)

105 (0.09)

1137

Floral

24 (0.03)

746 (0.80)

78 (0.05)

19 (0.02)

0 (0.00)

68 (0.08)

935

Turf

10 (0.03)

317 (0.80)

20 (0.05)

14 (0.04)

1 (0.00)

32 (0.08)

394

Total

68 (0.03)

1968 (0.80)

178 (0.07)

45 (0.02)

2 (0.00)

205 (0.08)

2466

*Trissolcus wasps that were unidentifiable below the genus level due to damage are presented as Trissolcus spp.

Table 2. Pairwise comparisons of deployment as a categorical variable. P-values with * are considered significant.

 

1

2

3

4

5

6

7

8

9

10

1

 

0.05*

0.12

0.71

0.77

1.00

0.15

<.01*

<.01*

<.01*

2

0.05*

 

1.00

0.90

0.84

<.01*

1.00

0.11

0.15

0.25

3

0.12

1.00

 

0.98

0.96

0.03*

1.00

0.04*

0.05

0.10

4

0.71

0.90

0.98

 

1.00

0.36

0.99

<.01*

<.01*

<.01*

5

0.77

0.84

0.96

1.00

 

0.41

0.97

<.01*

<.01*

0.97

6

1.00

<.01*

0.03*

0.36

0.41

 

0.03*

<.01*

<.01*

<.01*

7

0.15

1.00

1.00

0.99

0.97

0.0288*

 

0.02*

0.03*

0.06

8

<.01*

0.11

0.04*

<.01*

<.01*

<.01*

0.02*

 

1.00

1.00

9

<.01*

0.15

0.05

<.01*

<.01*

<.01*

0.03*

1.00

 

1.00

10

<.01*

0.25

0.10

<.01*

0.97

<.01*

0.06

1.00

1.00

 

Table 3.Percentage of H. halys eggs (n=2,427) in each fate category based on the total number of eggs deployed for each kairomone lure treatment. Data are from 6 H. halys egg mass deployments in Salt Lake City, UT, from 24 June through 27 August 2021. Lure treatments are n-tridecane to (E)-2-decenal; hexane (control), 1:0, 4:1, and 9:1.

 H. halys Egg Fate (%)

Control

(n=598)

1:0 (n=615)

4:1

(n=597)

9:1

(n=617)

Trissolcus japonicus emergence

4.7

10.6

1.3

0.0

Trissolcus euschisti emergence

0.5

0.0

0.0

0.0

Black goo

5.0

1.6

5.9

3.9

Unhatched H. halys

26.4

13.2

19.8

25.5

Predated

3.5

2.1

3.9

3.2

Sunken

25.9

24.6

25.1

17.7

Empty

1.7

0.5

1.2

0.7

Missing

9.0

7.6

6.5

8.1

Hatched H. halys

23.2

39.8

36.4

41.0

 

Table 4. Parasitism rates of H. halys egg masses and eggs, and emergence rates by parasitoid species. Data in the center column are number and percentage of egg masses parasitized out of the total 92 egg masses deployed followed by parasitoid emergence from egg masses. Egg masses were deployed in Salt Lake City, UT, from 24 June through 27 August 2021. The right column is the total number of individual eggs within masses that showed signs of parasitism (determined by presence of a guarding female and/or parasitoid emergence) followed by the number of successfully emerged parasitoid species.

 

Egg Masses (n=92)

Parasitized Eggs

Parasitoid Species

Parasitized

Emergence

Total

Emergence

Trissolcus euschisti

7 (7.6%)

1 (1.1%)

191

3 (1.6%)

Trissolcus japonicus

5 (5.4%)

5 (5.4%)

129

101 (78.3%)

Unknown

2 (2.2%)

0 (0%)

52

0 (0%)

Total

13 (14.1%)*

6 (6.5%)

372

104 (28.0%)

               *One egg mass had evidence of parasitism by both T. euschisti and T. japonicus.

TJ map

Figure 1. Trissolcus japonicus detections in northern Utah represented by first year of detection at that site. Results are from yellow sticky card surveys between May and September, 2019-2021.

  line graph TR

Figure 2. Mean number of Trissolcus spp. detected on yellow sticky cards May-September 2021. Each card was deployed for 2 weeks at a unique site (n=24). Counts were averaged by groundcover designations of Bare, Floral, and Turf with 8 of each designation.

 

line graph TJ

Figure 3. Mean number of T. japonicus detected on yellow sticky cards May-September 2021. Each card was deployed for 2 weeks at a unique site (n=24). Counts were averaged by groundcover designations of Bare, Floral, and Turf with 8 of each designation.

y tube bar graph

Figure 4. Residence time in the treatment vs. control arm of the Y-tube olfactometer out of 5 minutes.

bar graph

Figure 5. Fate of field deployed H. halys eggs (n=2,472) categorized by the percentage in each lure kairomone treatment. Lure treatments are n-tridecane to (E)-2-decenal; hexane (control, n=598), 1:0 (n=615), 4:1 (n=597), and 9:1 (n=617). A total of 6 deployments were made in Salt Lake City, UT, from 24 June through 27 August 2021.

Participation Summary
22 Farmers participating in research

Educational & Outreach Activities

1 Published press articles, newsletters
4 Webinars / talks / presentations
3 Workshop field days
1 Other educational activities: Announcement of Idaho State Record of the exotic Trissolcus japonicus.

Participation Summary:

133 Farmers
46 Ag professionals participated
Education/outreach description:

Fact Sheets:

  • Schumm, Zachary R.; Richardson, Kate V.; Holthouse, Mark Cody; Mizuno, Yota; Alston, Diane G.; and Spears, Lori R. (2019).  "Parasitoid Wasps of the Invasive Brown Marmorated Stink Bug in Utah" Utah State University Extension – Fact Sheet ENT-198-19. (revision in progress)
  • Conservation of Samurai Wasp for the Management of the Invasive Brown Marmorated Stink Bug (Future outcome)

Published press articles, newsletters:

  • Richardson, K.V. Bee Assassin Bug Predating on BMSB. Utah Pests News, Utah State University Extension. Vol 15: Summer edition. https://extension.usu.edu/pests/files/up-newsletter/2021/UtahPestsNews-summer21.pdf
    • 11,090 Subscribers
  • Field efficacy of host kairomones to increase biological control of Halyomorpha halys by parasitoid Trissolcus japonicus (in progress)
  • Range Expansion of Trissolcus japonicus (Ashmead) in Utah and Effects of Floral Resources on its Prevalence (in progress)

Webinars, talks and presentations:

  • Richardson, K.V. Beneficial Insects: Wasps and Flies. Utah Pests Extension, June 29 Vegetable IPM Twilight Meetings.
    • 61 live attendees
    • 653 YouTube views
    • 222 Facebook views
  • Richardson, K.V., D. Alston, and L. Spears. 2021. Kairomone Lures to attract parasitoids of the invasive Halyomorpha halys (Stål). Entomological Society of America, October 31- November 3 National Annual Meeting– Student 10 min paper competition.
  • Richardson, K.V., D. Alston, and L. Spears. 2022. Brown Marmorated Stink Bug Biological Control. Utah State Horticultural Association Annual Convention, January 20.
    • 28 live attendees
  • Richardson, K.V., D. Alston, and L. Spears. 2022. Biological Control of Brown Marmorated Stink Bug. 10th Annual Utah Urban and Small Farms Conference, February 24.
    • 82 live attendees
    • 351 YouTube views

Workshop/field days:

  • Richardson, K.V. Insect Basics Class. Freckle Farm, June 17 Little Farmers Camp.
    • 20 live attendees
  • Richardson, K.V. Biological control of BMSB by samurai wasp (Trissolcus japonicus). Utah Pests Extension, September 30 First Detector Workshop.
    • 22 live attendees
  • Richardson, K.V. Utah Tree Fruit Field Day, July 5.
    • ~25 live attendees

Other:

  • Richardson, K.V. Samurai Wasp (Trissolcus japonicus Ashmead) Discovered in Idaho by Utah State University. Idaho State record announcement.

Project Outcomes

46 Farmers reporting change in knowledge, attitudes, skills and/or awareness
34 Farmers intend/plan to change their practice(s)
2 Grants received that built upon this project
Did this project contribute to a larger project?:
Yes
26 New working collaborations
Project outcomes:

Utah’s tree fruit growers were surveyed in 2018 about their highest priority needs for H. halys research. Greatest interest was in biological control (31%), followed by insecticides (25%), monitoring/thresholds (24%), cultural control (15%), and phenology models (5%) (L. Spears, personal communication). This project supports follow-up on Utah tree fruit industry priorities by producing applied research results on enhancement of biological control. Successful engagement of natural enemies will save growers an estimated $200 per acre in insecticide and application costs on approximately 15,034 acres of specialty crops affected by H. halys in northern Utah, for a total of $155,000 in annual savings for tart cherry producers, and $60,000 in annual savings for each peach and apple producers (USDA NASS, 2017).

Utah is a unique climate for T. japonicus and the location presents obstacles to establishment due to its extreme climate and high elevation. Current geographic distribution and climate modeling shows parts of Utah as marginally suitable for T. japonicus to persist as a permanent population (Avila and Charles 2018), yet the T. japonicus has successfully overwintered and expanded its distribution in Utah (K. Richardson, personal observation). Therefore, promoting and conserving the presence of T. japonicus populations already established is a highly viable option for sustainable management of H. halys.

This proposed research supports sustainable approaches through cultural practices that 'naturalize' crop habitats and facilitate recruitment and persistence of the T. japonicus (Michaud 2018). One such approach is to enhance habitat diversity by providing supplementary resources (e.g., alternative hosts, supplemental food sources, and/or overwintering sites) to natural enemies (English-Loeb et al. 2003; Perez-Alvarez et al. 2019). Since parasitoids rely on nectar and pollen sources to survive and reproduce, identifying flowering plants that increase parasitoid fitness in agricultural landscapes is essential to their establishment (Foti et al. 2016; McIntosh et al. 2020; Rahat et al. 2005; Winkler et al. 2009).  This project will also study the effectiveness of a synthetic kairomone (an interspecific chemical cue) to attract and retain T. japonicus. This strategy is based on the premise that chemical residues left by host insects can attract parasitoid wasps, elicit parasitoid arrestment, stimulate parasitoid search behavior, and result in increased parasitism (Mansour et al. 2010; Murali-Baskaran et al. 2018; Peri et al. 2006). These approaches support the need for further research on T. japonicus in northern Utah, and key strategies for its conservation and enhancement. 

Success stories:

 “As an Extension educator with topic specialty, I am often asked to serve as source for information requests for Southeastern Utah (~ 55k population) and teaching Master Gardeners and other gardening/agriculture workshops especially in pest management. Research updates like those shared increase my capacity to provide current research-based information.”

“Let us know of any further developments. This was cutting edge and needed research.”

“I will pass information from this along to others in entomology to improve habitat for the wasp”

Recommendations:

I greatly appreciate receiving this grant and all the benefits it has brought to my research. One thing I would like to share with SARE is the difficulty of tuition costs not being allowed in the budget. I understand that the grant's purpose is to be used for research rather than to take courses, but as a graduate student, I have a number of "Thesis Research Credits" that I pay tuition for and are designed to give me time to conduct my research funded by this grant.  Without a way to cover these required credits' tuition costs, I can not be enrolled as a graduate student or conduct my research. We have managed to find other funding through a local horticulture association to help with these tuition costs, but I know this is a common problem with many grants and graduate students. It would lessen the financial burden and help better facilitate research if "Thesis Research Credits" were allowable under the budget of the SARE Graduate Student Grant. 

Information Products

    Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.