Brown Marmorated Stink Bug (BMSB), native to eastern Asia, was first detected
in the U.S. in Allentown, PA in 1996, and by 2010 populations increased significantly
in the mid-Atlantic region. Multiple high value fruit and vegetable crops experienced
extreme damage, stone fruit losses being particularly severe, many times sustaining
100% crop loss (Hoebeke and Carter 2003, Leskey et al. 2012). Following range
expansion and multiple introductions, BMSB was first found in Utah in Salt Lake City
in 2012 (Gariepy et al. 2014, Haye et al. 2015, Dr. L. Spears, personal
communication). BMSB adults are strong fliers, immature and adult life stages feed
on over 100 plant species often resulting in economic damage, the insect is tolerant
of many insecticides, and it is well adapted to overwintering in human structures
(Wiman et al. 2015, Rice et al. 2014). All of these characteristics make BMSB a
significant threat to U.S. agriculture, especially specialty crops like fruits and
vegetables. Little research has addressed BMSB status and management in the high
elevation, arid environments of the Intermountain West. I propose to conduct
critical research and outreach education on BMSB through host plant use surveys,
development of life stage degree models (for egg, nymph and adult activity),
assessment of native and introduced biological controls through sentinel egg mass
deployment and field surveys, grower and public presentations on study findings,
and publication of results in an extension factsheet, news articles, and pest
advisories. In 2017, BMSB economic crop damage was reported for the first time in
Utah on peach, apple, squash, and corn. My project will provide valuable insight for
better understanding and managing BMSB in the urban-agricultural landscapes of
northern Utah. I will help train the public sector on prevention, monitoring, and
management of BMSB. I will coordinate my outreach education efforts with the USU
Extension Invasive Pest Program.
1. Host Plant Surveys (2018-2019)
Purpose: Host plant surveys will be conducted May through October of 2018 and 2019 to
determine BMSB plant use for spring emergence/acclimation, feeding (adult and nymph
stages), and reproduction. Surveys will be in suburban and rural locations of the Wasatch
Front. Surveys in 2017 were focused in suburban areas near human structures that
support overwintering. These results showed that BMSB is expanding into the suburbanagricultural/rural
a. Host plant surveys of residential areas will be conducted in Provo, Salt Lake City,
Kaysville, Layton, Roy, and Ogden for 2018 (surveys were conducted in similar
locations in 2017) to compile a list of common plants associated with BMSB.
b. In 2019, host plant survey sites will be positioned next to commercial farms and
community gardens producing fruits and vegetables. The results from these
surveys will expand the Utah host plant list to include agriculturally significant
plants, especially those in close proximity to residential neighborhoods.
c. With the assistance of several undergraduate student research technicians, I will
document which BMSB developmental life stages (egg, nymph, adult) are
present, and an estimate of their abundance.
2. Phenology (2018-2019)
Purpose: A seasonal timeline of BMSB development in Utah is imperative to empower
producers to manage BMSB. I intend to employ traps and host plant surveys described in
Objective 1 to characterize BMSB phenology in northern Utah.
a. Seasonal development of BMSB will be documented from late April to October in
both 2018 and 2019. Host plant surveys and trap deployment at each of the survey
sites will support observation of life stage occurrences and population abundance
patterns during the growing season.
*Reference figures and tables can be found in addenda document 5
b. Based on observed phenological activity and temperature, a BMSB degree-day
model will be developed for Utah. With this information, growers and the private
sector will be able to better anticipate optimal timings in the BMSB seasonal
cycle to interrupt population growth.
c. It has been speculated that BMSB is univoltine (one generation per season) in
Utah, but one year of data collection in 2017 indicated that a small second adult
generation may occur in the late fall (Fig. 7-8). During 2018 surveys, a subset of
first generation adults will be marked and confined on host plants with mesh
netting; their progeny will be marked to determine if a second adult generation is
produced before the onset of winter.
3. Biological Control (2018-2019)
Purpose: My focus for this objective is to discover natural enemies of BMSB present in
Utah. Parasitoid wasps are of specific interest, along with documentation of generalist
predators and microsporidia (Nosema spp.) in the gut of wild caught BMSB. It is
important that growers in Utah gain a better understanding of the potential for natural
control, and which organisms contribute the most to BMSB population suppression.
a. In the spring/summer of each 2018 and 2019 season, I will survey for parasitoid
wasps that specifically target BMSB eggs. Sentinel egg mass deployments
(BMSB egg masses reared in a lab colony that are deployed on host plants and
collected 2-3 days later) will survey for parasitoid wasps in suburban and
rural/agricultural environments, and determine if native (or introduced) wasps can
successfully kill and parasitize BMSB eggs.
b. Preliminary sentinel egg mass deployments in 2017 found several native egg
parasitoids. Parasitoid surveys in 2018 and 2019 will target native and exotic
wasps, such as the samurai wasp (Trissolcus japonicus), which can provide high
egg parasitism rates in the native range of BMSB and in laboratory studies (and
has now been detected in 9 U.S. states).
c. Generalist insect predators (e.g. praying mantis, assassin bugs, robber flies,
spiders, etc.) will be documented as observed in host plant surveys and sentinel
egg mass assessments.
d. Microsporidia have been identified as a potential population control agent of
BMSB in the eastern U.S. Microsporidia live in the intestinal tract of BMSB.
Wild caught BMSB will be dissected in the lab and evaluated for the presence of
microsporidia (Nosema spp.) spores.
Host Plant Surveys
Due to the fact that BMSB was originally discovered in Salt Lake City, UT on the University of Utah campus, host plant survey locations were concentrated within Salt Lake county (eight sites). The remaining seven sites were selected in adjacent counties like Utah (three sites), Davis (three sites), and Weber (one site). Selecting 15 total sites was based on time needed to survey each site every other week from May to September. Our crew of three to four people were usually able to survey an average of four sites a day, twice a week. Each site was selected based on homeowner reports from previous years provided by Dr. Lori Spears. Of the approximately 52 mapped/documented homeowner reports (as of spring 2017) of BMSB, 15 of these sites were selected based on access to an adequate number of plants (>20), along with homeowner permission to conduct surveys on plants that may have been on/over their property lines. The 20 plants randomly selected of those that were available at each site were within our 40×200 m long transect. Each plant was inspected using a beat sheet technique (a padded dowel/stick and canvas beating sheet by BioQuip) and visual observation by at least two people for three minutes, less time if a full plant inspection could be completed in under 3 minutes (e.g. plants with little foliage present). Access to higher branches with the beat sheet technique was enabled by a 1.5 m tall step ladder. Plants that were observed with at least one BMSB life stage (egg, nymph, or adult) present were allotted another seven minutes of inspection. The number of BMSB from each life stage was recorded for every plant. Every plant surveyed was identified to species level. A foliage sample from each species was pressed and mounted in accordance to protocols set forth by the Intermountain Herbarium.
In documenting BMSB phenology and seasonal developmental patterns, host plant surveys, trapping, and controlled voltinism field experiments have been employed.
Three traps were deployed at each of the host plant survey sites from approximately May 8 through October 25, 2018. Trap types included: 1) Dead-Inn 1.2 m tall black corrugated plastic pyramid trap (AgBio Inc., Westminster, CO), 2) Trece STKY dual panel adhesive trap (Trece Inc., Adair, OK) mounted on a wooden stake 1.2 m above ground height, and 3) Trece dual funnel tube trap (Trece Inc., Adair, OK) attached to a tree trunk 2-3 m above ground height. All traps were baited with the Trece BMSB dual lure (murganitol + aggregation pheromone MDT) and replaced every 12 weeks. The sticky panels were replaced at 6-week intervals or when 50% of trap surface was covered by debris or insects. Traps were positioned in the urban landscape sites to avoid conflict with human activity as much as possible. All traps were serviced weekly, and specimens recorded by number of adults (by males or female) and nymphs (by 2nd-3rd or 4th-5th instars).
The number of full and partial generations each season in Utah has not yet been confirmed. Current knowledge asserts that BMSB is univoltine (one adult generation per season) in the Intermountain West based on latitude and elevation; however, late season occurrence of nymphs in 2017 trapping trials and host plant surveys suggest that there may be a partial second generation occurring. To determine generation times for northern Utah, overwintering adults were collected (n=70) in May 2018, and confined within mesh fabric sleeve cages (made from 30×80 cm piece of mosquito netting, MosquitoCurtains.com, Alpharetta, GA) on two preferential hosts (host plants that offer season long nutrition, shelter, and substrate for oviposition), catalpa and tart cherry. A total of seven mesh bags each containing 10 overwintered adult BMSB (five males and five females) were placed on individual tree branches (three on catalpa and four on tart cherry) in the USU Kaysville Farm/Arboretum. Each mesh bag was marked and monitored once weekly to assess survival status and longevity of captive BMSB. Every bag was sealed with both a plastic zip tie and a metal twisty tie. Leaves with new egg masses produced by adults were removed, pinned to a new leaf (on a new branch) and enclosed in a new cage on the same host tree for continued monitoring. Nymphs that hatched from these eggs (F1 generation) were counted weekly by nymphal instar (Instars 1-5). Adults that developed from these F1 nymphs were again recorded and monitored for survival and longevity. Overwintering behaviors, such as aggregation, were also monitored for. Any new egg masses produced by these F1 adults were transferred to a new cage as before. Nymphs from these egg masses marked the beginning of the F2 generation, which were then monitored weekly into mid-October in a similar fashion to the F1 generation. Counting the number of individuals still alive each week was done by hand. Our lab group found that counting was easiest when all counted insects were placed into a temporary holding container (e.g. plastic container with a funnel for a lid as to allow for easy bug transfer into the container) and then placed back into the bag after the count was finished. Relative humidity and temperature were logged with a HOBO data logger (UX100, Onset Computer Co., Bourne, MA), one to represent the tart cherry and another for the catalpa.
Sentinel egg deployment, along with collection of wild BMSB egg masses started on June 6 and continued throughout (as egg masses were made available) the summer, ending September 20. Only fresh eggs taken from the BMSB lab colony at USU were used in sentinel egg deployments, all of which were less than 72 hours old. Deployed lab eggs were placed on double sided sticky tape and applied to a small circular piece of thick wax paper or water resistant card stock with a circumference of approximately 16 cm. These circular cards each containing an egg mass were then safety pinned to the underside of tree leaves at approximately 2-3 m above the ground. Cards were collected two days after deployment. Information on egg count, appearance, and signs of feeding were recorded before and after deployment. When deployed/wild egg masses were collected an initial onsite assessment for guarding parasitoid wasps was conducted, any present were caught with an aspirator. All egg masses were kept in tight seal petrie dishes and taken back to the lab where they were placed into an insect incubator. Conditions in the incubator were sustained at 25°C, approximate relative humidity 30%, and light to dark exposure set to 16:8 hours. All egg masses were then assessed visually 7-14 days after collection and then a final time 6 weeks later. Assessments included a description of unhatched egg color/shape or the presence of hatched BMSB nymphs or parasitoids wasps. Trees used for deployments and wild egg mass collections included pluot, tart cherry, catalpa, Norway maple, black locust, eastern redbud, bigtooth maple, apple, green ash, purple leaf plum, and tree of heaven.
Natural Enemy Surveys and the Search for Microsporidia
Host plant surveys previously described were also used to document the occurrence of natural enemies considered capable of feeding on BMSB eggs and other life stages as defined by Morrison et al. 2016* and observations by our lab in Utah. Each plant was given a total number of each insect family or order in cases in which family was too difficult to discern in the field.
Another major portion of our biological control research was focused on documenting the percentage of BMSB infected with the microsporidia species Nosema maddoxi. This microsporidian has only recently been discovered to infect BMSB by Dr. Ann Hajek, her research** gives hope to future possibilities of biological control of BMSB. All urban trap specimens of BMSB were taken from traps once a week, put into bags and labeled with date and location information, and finally stored in the freezer at -15°C. Stink bug specimen were then prepared for dissection according to procedures set for by Dr. Ann Hajek’s lab. Each stink was crushed with dissection probes/pestles inside of a 2 mL micro centrifuge tube. Crushed stink bugs were then mixed with 500, 200, 140, 60, 50, and 50 µL of deionized water for each life stage (adult, 5th, 4th, 3rd, 2nd, and 1st instar nymph) respectively. A 12 µL sample of the crushed stink bug solution was then placed on a microscope slide and covered with 22×22 mm cover slip. The slide was then viewed under a phase contrast microscope at 400x magnification. Visual confirmation of microsporidia infection was confirmed by the presence of spores (see the many pill shaped objects in view in figure 1). After viewing each sample under the microscope, the original micro centrifuge samples were then frozen at -80°C.
*Morrison, W. R., Mathews, C. R., & Leskey, T. C. (2016). Frequency, efficiency, and physical characteristics of predation by generalist predators of brown marmorated stink bug (Hemiptera: Pentatomidae) eggs. Biological Control, 97, 120–130. https://doi.org/10.1016/j.biocontrol.2016.03.008
**Hajek, A. E., Solter, L. F., Maddox, J. V., Huang, W. F., Estep, A. S., Krawczyk, G., … Becnel, J. J. (2017). Nosema maddoxi sp. nov. (Microsporidia, Nosematidae), a Widespread Pathogen of the Green Stink Bug Chinavia hilaris (Say) and the Brown Marmorated Stink Bug Halyomorpha halys (Stål). Journal of Eukaryotic Microbiology. https://doi.org/10.1111/jeu.12475
Urban host plant surveys conducted in 2018 documented 2552 BMSB, this total being made of up egg masses (37), nymphs (2170), and adults (345). The occurrences of each life stage over time is shown in figure 2. Plants observed were made up of 37 plant species (Figure 3), 13 of which were novel BMSB host plants to the state of Utah (Figure 4). These 2018 BMSB plant data also contributed to the total list of 63 known Utah BMSB host plants (Figure 5), which is currently published on the Utah Pests website through Utah State University Extension.
Host plant data from 2018 surveys were compared to identical surveys conducted by our lab in 2017 and the findings shed some light on the most commonly encountered host plants (Figure 6) and numbers of BMSB found at each survey site in both years (Figure 7).
Trap data collected in 2018 trapping trials brought in a total of 818 BMSB (sum of all three trap types). The pyramid trap performed the best in overall trap catch (584), followed by the dual panel adhesive trap (168), and the dual funnel tube trap with the least (66). Trap data was recorded for each of the three trap types at all 15 host plant survey locations every week. Peak numbers of BMSB adults occurred in late May and early June, along with mid-July through early August, and once again in late September (Figure 8). Nymph numbers peaked most notably in early July (Figure 9).
The four sites dispersed within Weber and Davis counties (Ogden Valley) recorded 72 BMSB by the end of the season, the eight sites in Salt Lake county (Salt Lake Valley) accumulated 591 BMSB, and the three sites in Utah county (Utah Valley) had 155 BMSB (Figure 10). The overall trap catch of BMSB decreased dramatically in 2018 when compared to the overall total catch in 2017 (Figure 10).
After season long observations of BMSB on both catalpa and tart cherry, tart cherry was found to be the only plant successful in harboring a partial F2 generation(Figure 11). Catalpa supported only the F1 generation and these adults produced no eggs (Figure 12). These results are not entirely surprising, as it was previously understood that northern Utah would most likely only support a single adult generation given historical weather and other environmental factors. In light of these results, our lab is still not convinced that this experiment has fully exposed the truth behind BMSB voltinism in Utah. A major problem with our design was the initiation date of the experiment. Originally the start date was set for mid-May, but the tart cherry plot wasn’t started until June 4, 2018 and catalpa not until June 18, 2018 (with only 30 total F0 adults instead of 40 as in tart cherry). This delayed and disjoint start was a product of low numbers of collected wild adults in May. We started the experiment as fast as we could with the population supply that was available us, but it was too late. The plan for this coming 2019 field season is to dedicate the first two weeks of May to full time collection of spring emerged wild adults for this experiment. The latter part of May is a critical point in F0 adult egg oviposition. It was noted that some of the F0 adults collected in May 2018 were laying eggs on or near the date they were recovered. Because these eggs were laid on artificial substrate and not in a natural environment, these egg masses were not considered in the experiment. Even with a delayed start on tart cherry, BMSB did experience a partial second generation. It is thought that an earlier start date may enable better observation of a full second generation in September. A new start date of May 15, 2019 has been set to try and account for this earlier F0 egg oviposition and allow adequate time to collect wild BMSB in April and early May.
In total, 47 fresh lab reared BMSB egg masses were deployed and 15 wild stink bug egg masses were collected, seven of which were BMSB and eight of which other species. Out of the 54 total BMSB egg masses analyzed/dissected in the lab, 5.5% were found to have at least one emerging parasitoid. These emerged parasitoids included Anastatus pearsali (Figure 13), Anastatus reduvii, and a Trissolcus sp. (confirmed not T. japonicus). Identification of these wasps is to be confirmed by specialist Dr. Elijah Talamus from University of Florida Gainesville. The search for native and exotic parasitoids will continue in 2019.
Natural Enemies and the Search for Microsporidia
Currently the raw data for all natural enemies included in the orders/families (Anthocoridae, Asilidae, Cantharidae, Carabidae, Chrysopidae, Coccinellidae, Dermaptera, Dolichopodidae, Formicidae, Gryllidae, Mantodea, Nabidae, Pentatomidae, Reduviidae, Salticidae, Tettigonidae, Thomisidae, Eutichuridae, Araneidae, and Hemerobiidae) have been recorded alongside host plant survey data and are waiting to be analyzed for possible correlation of occurrence with BMSB.
Whole body BMSB dissections looking for microsporidial infections began in October 2018. Undergraduate student research assistant James Withers has been trained in visual inspection and microscope techniques in searching for microsporidia, specifically Nosema maddoxi (Figure 1). Due to a slow learning curve by our lab group (myself included) in determining absence or presence of spores visually, only a small fraction of the trap catch specimen from the 2018 field season have been dissected and visually inspected. But our ability to process each sample has steadily increased in the last few weeks. Of the 89 total BMSB dissected and inspected under phase contrast microscopy, only 4 have been found with spores, indicating a microsporidial infection by N. maddoxi. These 89 specimen are but a small fraction of the specimens in cold storage yet to be dissected. Two other undergraduate research assistants will be joining James this spring semester and our group should be able to process more specimen visually this way. Also, we are hoping to try and start confirming positive visual detection samples with PCR techniques by this March or April.
Educational & Outreach Activities
- I created a poster that was displayed at the Entomological Society of America Annual Meeting in Vancouver, Canada, displaying current brown marmorated stink bug host plants, voltinism, and trapping data for urban-agricultural landscapes in Utah. My poster received a cash prize for first place in its category and is now displayed in the Utah State University biology department. (Poster PDF file is available on other report page)
- Utah State University Entomology Club Insect Tours: September 26, 2018 Cedar Ridge Elementary (15 participants)
- Utah State University Entomology Club Insect Tours: October 16, 2018 Edith Bowen Laboratory School (20 participants)
Insect tours at USU are a great platform for sharing basic insect facts and information with young people from the Cache county community. When I am in charge of giving a presentation in front of these young people, I include information on the brown marmorated stink bug (BMSB) and why it is significant to all of us here in Utah. I show students live BMSB specimens, help them understand its impact on agriculture and food production, and explain tactics used by my lab to better understand and manage BMSB as a pest.
- Weber State University October 4, 2018 (25 participants; 45 minutes)
I was invited to share a lecture with students at Weber State University in Odgen, Utah by Dr. John Mull. The presentation explained basic BMSB identification, ecology, and why it is currently considered a major pest in many parts of the world, including Utah. I was able to share findings on some of the most common host plants observed in my surveys, which trap type of the three I compared was most successful in the urban landscape, how many generations of BMSB were observed in controlled outdoor trials, and parasitoid wasps discovered stinging BMSB egg masses. Students were able to ask me questions after the presentation as well.
- Kaysville Fruit and Vegetable Field Day June 20, 2018 (24 participants)
Utah farmers and growers were able to listen to a variety of presentations given at the USU research farm in Kaysville. Dr. Lori Spears, Zach Schumm, and myself shared general information on BMSB. This included traps, fruit feeding damage, and what research was being conducted onsite. I was able to show growers where I would be conducting my voltinism experimentation and display BMSB egg masses deployed in trees in an effort to document local parasitoid wasps. I also had handouts for participants containing data on urban trapping data from 2017 and 2018 summer trials.
2. Kaysville First Detector Workshop September 21, 2018 (47 participants)
Dr. Lori Spears invited me to give a presentation on the current pest status of BMSB at the USU Kaysville Education Center. I presented data on host plants, trapping trials, and biological control agents documented in the summers of 2017 and 2018. The audience was made up of master gardeners and local extension agents. I facilitated a verbal quiz at the end of my talk in which the audience was given two stink bug photos on individual PowerPoint slides and made to select which one was the native look alike species, and which one was BMSB. The audience was receptive to this exercise and I received verbal appreciation after the talk for photos of insects that might commonly be mistaken for BMSB in Utah.
(Other Educational Activities)
1. Farmers market attendance and presentations: Wheeler Historic Farm in Murray, UT on July 29 (38 participants)
2. Farmers market attendance and presentations: Wheeler Historic Farm in Murray, UT on August 19, 2018 (42 participants)
Utah State University sponsors a tent for master gardeners at many Utah farmer’s markets, I happened to volunteer two different Sundays at their Wheeler Historic Farm tent. I was alongside three master gardeners and each of us stood on the ready for any questions the market goers might have about horticultural practices or insect pest problem. When I introduced myself to someone asking about pests I always started by saying that I studied the invasive brown marmorated stink bug. Most of the time I was asked what BMSB looked like, and it was a great way for me to share basic identification information and why BMSB is of such importance in Utah. Many times these people would say that they had seen this insect in their home or yard and I took the time to explain good exclusion practices for their home and how to avoid future problems with BMSB by preventative measures.
(Documents in Progress)
- Utah Pests Fact Sheet through Utah State University Extension: Common Stink Bugs of Utah
I am in the process of writing a fact sheet on some of the common stink bug species found in Utah. The document begins by introducing basic stink bug characteristics and ecology, and later progressing into single species descriptions of 12 different plant feeding stink bugs. This first part of the fact sheet has been completed, what remains is a new section including descriptions of some of Utah’s beneficial predatory stink bugs (e.g. stink bugs of Podisus sp.) that home owners and producers should try and preserve.
2. Journal Article: Brown Marmorated Stink Bug Host Plants
I have begun writing a manuscript rough draft on the data collected from BMSB host plant surveys conducted in 2017-2018. This document will provide insight into which host plants were particularly beneficial two one or more BMSB life stages and when this kind of interaction occurred. The current list of all known plants to harbor BMSB will be provided, along with a list of non-host species.
- Utah State Horticultural Association: Urban Habitats as Sources of BMSB on Agricultural Lands January 25, 2019
This presentation will be aimed at producers/growers in Utah, informing them of current data on which plants harbor BMSB, effective trapping techniques, and other developments of the BMSB invasion within the urban landscapes of Utah. This presentation will emphasize that data on urban settings is extremely applicable to agricultural production because of the close proximity of urban and agricultural lands in northern Utah.
Right now our research contributes mostly to preventative foresight and knowledge to producers (those involved with USU Extension outreach events), master gardeners, and lay people within academia and beyond. By introducing which plants are most susceptible to BMSB, what time of the year BMSB seems to be present as a pest in northern Utah, and describing which beneficial insects can possibly limit BMSB population expansion in Utah, people are more prepared for better management of BMSB in the future.
Most of the knowledge gained has been in refining and perfecting host plant survey, trapping, and biological control survey techniques and how such raw data can be shared with the public through workshops, markets, and educational platforms in schools.