Biological control of Halyomorpha halys (Stål) (Hempitera: Pentatomidae)

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an invasive pest of American agriculture. The native range of H. halys includes China, Korea and Japan, where it is considered a sporadic pest of tree fruit and soybeans. Halyomorpha halys was first detected in the U.S. near Allentown, PA in the late 1990s and has subsequently spread to over 40 states and several Canadian provinces. Due to its highly polyphagous feeding habits, H. halys is considered a serious agricultural pest throughout the mid-Atlantic region known to damage tree fruit, berry crops, grapes, vegetables, field crops and ornamentals. Currently, H. halys is being managed by repeated applications of broad spectrum insecticides, derailing IPM practices in many crops. However, little is known about the effects of native natural enemies on the population dynamics of H. halys. The purpose of this doctoral dissertation was to identify natural enemies which effect H. halys in New Jersey agro-ecosystems and evaluate their effectiveness in laboratory, greenhouse and field settings. The effect of natural enemies was first studied on sentinel H. halys egg masses deployed at agricultural sites across southern New Jersey. After 48 h in the field, egg masses were assessed for signs of predation and incubated for 6 weeks to allow for parasitoid emergence and development. Utilization of H. halys eggs was generally low: 5.84% of eggs were consumed by predators while 1.43% of eggs were parasitized. A subset of sentinel H. halys egg masses were recorded with closed circuit security cameras to further identify those organisms effecting egg masses in the field. Video recordings revealed 688 visits by organisms in 31 taxa. Muscoid flies were the most common visiting taxa but these visits did not include observable damage to the eggs. Orthopteran visitors consumed H. halys eggs on at least 3 occasions, and in two of these cases the Orthopteran consumed the egg mass entirely leaving no signs of eggs or predation. Sentinel egg masses do not provide information about the identity of predators of H. halys nymph stages so I developed a set of H. halys-specific molecular primers for use in gut content analysis. HhalysCO1Spec primers amplify an 89-bp region of the CO1 mtDNA gene and have been verified specific to H. halys by BLASTn query and by cross-amplification tests on non-target Pentatomidae present in the Eastern U.S. Timed digestion trials were used to determine the half-life of degradation for the sequence amplified by the HhalysCO1Spec primers in laboratory-fed C. carnea (Stephens) larvae. These laboratory-fed predators were also used to determine the DNA detectability half-life for the qPCR assay BMITS1 which amplifies a sequence of H. halys DNA of similar length to HhalysCO1Spec. Both primer sets successfully amplified target DNA from laboratory-fed predators, but further analysis revealed significant differences in the duration of DNA detectability between the two methods. The half-life of detectability for the BMITS1 assay (T50 = 48.87 h) was approximately 4 times longer than that of the HhalysCO1Spec method (T50 = 12.12 h). Due to the higher sensitivity of the BMITS1 assay, this amplification method was selected to screen field-collected predators for the presence of H. halys DNA. Throughout the summer months of 2014 through 2016, potential predators were collected from soy, peaches, peppers and sunflower plantings in southern New Jersey. These predators were assayed for H. halys DNA with the BMITS1 qPCR system. In total, 850 predators were collected and of these, 13.6% of samples assayed positive for H. halys DNA. Taxa with the highest proportion of positive assay results included Nabidae (29.4% ± 6.4%), Tettigoniidae (26.3% ± 7.2%), Acrididae (14.7% ± 6.2%), Dermaptera (12.8% ± 4.0%) and Coccinellidae (11.7% ± 1.6%). Although the sample size varied between crops, predators collected in sunflowers, peppers and raspberry displayed significantly higher rates of H. halys DNA detection than those collected in soybeans and peaches. Despite the observed low rates of predation on H. halys egg masses, a greater diversity of predator taxa were found to contain H. halys DNA indicating that predators can consume other stages of H. halys. To identify generalist predator taxa which consume H. halys nymphs, I conducted no-choice predator feeding trials in laboratory-based microcosms. Field collected predators were exposed to 1) one H. halys egg mass, 2) 20-30 1st instar H. halys nymphs or 3) five H. halys 2nd instar nymphs. Prey were deposited on a sunflower seedling within a plastic predation arenas, while predator-protected control prey of identical stage and age were kept in cups within the arena. After 48 h of exposure, nymph survivorship was assessed while predation on eggs was measured by assessing hatch rate. Predation was determined statistically by comparing the survivorship of treatment prey which were exposed to predators to that of protected prey. Egg predation occurred from predators in the following taxa: Acrididae, Coccinella septempunctata (L.), Podisus maculiventris (Say), and Tettigoniidae. Predators in the families Nabidae and Reduviidae caused significant reduction in the survivorship of 1st instar nymphs while Nabidae and P. maculiventris nymphs reduced the survivorship of 2nd instar nymphs. Several taxa of predator showed stage-specific differences in their consumption of H. halys immatures, with Acrididae and Tettigoniidae preying upon eggs but not nymphs, while Hemipteran predators of the taxa Nabidae, Reduviidae and Pentatomidae attacked nymphs but not eggs. Based on the aforementioned results, it is clear that H. halys is attacked by predators in laboratory and field settings. However, the utility of this predation as a means of preventing H. halys damage to agricultural crops is unclear. It is also unclear if observed rates of H. halys predation in laboratory settings would be affected by the presence of alternate prey. To study the effect of H. halys predation on plant yield, H. halys nymphs were exposed to predators on potted soybean plants in greenhouse mesocosms. Aphis glycines (Matsumura), an important aphid pest of soybean, were introduced into a subset of mesocosms as alternate prey. Two commercially available predators were introduced into the soybean mesocosms: Hippodamia convergens (Guerin-Meneville), a predator of A. glycines, and P. maculiventris, a predator of H. halys. After 21 days, prey abundance was assessed, as were metrics of plant health including vertical growth, lateral bud development and dry mass. Prey treatments significantly affected plant vertical growth, lateral bud development and final dry mass but in most cases, predator treatments did not significantly reduce the negative effects of herbivory. Plant health metrics were negatively affected by the presence of A. glycines, but these did not differ significantly from treatments which included both A. glycines and H. halys. Halyomorpha halys nymphal survival was unexpectedly higher in treatments which included A. glycines as alternate prey; the cause of this result is unknown. The results of this dissertation indicate that H. halys is affected by a relatively broad community of generalist predators in New Jersey agro-ecosystems. However, the abundance and efficacy of these predators varies widely by crop, growing season, and H. halys life stage. In greenhouse mesocosms, moderate predation on H. halys nymphs did not prevent measurable declines in soybean plant health, leading to the conclusion that natural control by endemic predators and parasitoids may impact annual H. halys populations but are insufficient to prevent economic injury.

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