Field phenology of emerald ash borer (Coleoptera: Buprestidae) parasitoids in New York State.

Emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), has caused extensive mortality of ash across North America. Biological control offers a potential long-term management option, allowing for long-term survival of ash. Careful monitoring of populations of biocontrol agents is necessary to understand their relative impacts. Understanding the emergence and flight phenology of these species allows for the optimization of monitoring schemes and improves our understanding of host-parasitoid interactions. We used yellow pan trapping data to assess the adult phenology of both EAB and its associated native and introduced parasitoids in 3 New York counties. We monitored 2 introduced larval biocontrol agents, Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius galinae Belokobylskij & Strazanac (Braconidae), for 3-4 years post-release, as well as the native parasitoid Phasgonophora sulcata Westword (Chalcididae). Results indicate a single discrete emergence event for both EAB and P. sulcata in all monitored counties, which is consistent with previously reported results. Our results also suggest there are 4 generations per year of T. planipennisi and 3 generations of S. galinae in the monitored counties. We recorded an additional generation of T. planipennisi that had not previously been reported in New York, and both T. planipennisi and S. galinae appeared to emerge earlier than previously documented.

Establishment and impacts of emerald ash borer (Coleoptera: Buprestidae) parasitoids released at early- and post-invasion sites.

Forest stands infested by emerald ash borer (EAB), Agrilus planipennis Fairmaire, experience extensive mortality of mature ash trees. Post-invasion woodlands commonly have a small contingent of mature lingering ash, an orphaned cohort of seedlings/saplings, and low EAB densities. To protect regenerating ash against rebounding EAB populations, a suite of biocontrol agents are being reared and released. USDA APHIS guidelines currently recommend the release of parasitoids into forests prior to overstory ash mortality at sites containing a variety of ash size classes and low to moderate but building EAB densities. To understand if biocontrol establishment and control of EAB is feasible in post-invasion sites, we assessed the establishment of parasitoids in 6 post-invasion forest stands in 2 regions of NY and compared EAB mortality in these stands to 2 regions where releases were conducted during the early-invasion phase. Results of parasitoid trapping indicates Tetrastichus planipennisi Yang established under both release strategies. Spathius galinae Belokobylskij & Strazanac was only released in post-invasion stands, where it was established successfully. Artificial EAB cohorts were established and life tables were constructed at 3 sites per region. EAB mortality due to T. planipennisi parasitism was similar under both release strategies 2 yr after release in post-invasion stands versus 8 yr after release in early-invasion stands. Combined mortality from T. planipennisi and woodpecker predation resulted in consistently low EAB reproductive rates. Future biocontrol releases could target forests identified as economically or ecologically important, regardless of whether EAB populations are increasing or have collapsed following initial invasion.

Mortality of Emerald Ash Borer Larvae in Small Regenerating Ash in New York Forests.

Despite a robust biocontrol program against emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), parasitoid populations cannot build quickly enough to save mature ash trees. The future of ash as a viable component of North American forests depends on survival of immature ash that were too small to be attacked during the initial outbreak. This study was designed to quantify impacts of established introduced parasitoids and native woodpeckers on the population growth of emerald ash borer infesting regenerating ash saplings in white ash forests. Most emerald ash borer larvae were killed by Tetrastichus planipennisi Yang and woodpeckers in the fourth instar. Life-table analyses revealed that the estimated net reproductive rate of emerald ash borer was R0 = 4.2 in eastern New York and R0 = 0.0 in western New York. Without mortality from parasitoids and woodpeckers, R0 values would have been 16.4 and 7.9 in eastern and western New York, respectively. We monitored the health of mature and sapling ash trees from 2012 to 2017 and found that large trees were significantly more likely to be infested with emerald ash borer and to die than smaller trees. Fifty-four percent to 81% of ash saplings contained no living emerald ash borer, and the density of emerald ash borer at all sites was very low (< 4/m2). This study adds to the growing body of evidence that emerald ash borer biocontrol is contributing to population control and can help promote survival of young ash trees as forests recover from emerald ash borer outbreaks.

Phenology of Emerald Ash Borer (Coleoptera: Buprestidae) and Its Introduced Larval Parasitoids in the Northeastern United States.

Biological control offers a long-term and sustainable option for controlling the destructive forest pest emerald ash borer (EAB), Agrilus planipennis Fairmaire, in North America. Three larval parasitoids, Spathius agrili Yang (Hymenoptera: Braconidae), Tetrastichus planipennisi Yang (Eulophidae), and Spathius galinae Belokobylskij & Strazanac, have been introduced to North America from the native range of EAB (northeastern Asia). While T. planipennisi appears to be persisting where it has been introduced in northern United States, S. agrili failed to establish in northeastern states. The more recently identified parasitoid S. galinae was recovered from the Russian Far East and climate matching suggests it should be suited for release in colder climates. We collected data on the phenology of EAB and its introduced larval parasitoids from colonies established in an insectary, growth chambers, and field-caged trees in Syracuse, New York to determine whether asynchrony between parasitoids and EAB or climate could impact establishment and persistence. Phenological data indicated EAB has one and 2-yr life cycles in New York, with parasitoid-susceptible EAB larvae available spring to fall for parasitism. Insectary and growth chamber studies indicated S. galinae and T. planipennisi were synchronous with EAB phenology, and field studies suggested both species could overwinter in northeastern climates. Spathius agrili was asynchronous with EAB phenology and climate, emerging when fewer parasitoid-susceptible EAB larvae were available and temperatures were not optimal for survival. Our results suggest S. galinae and T. planipennisi are suited for biological control of EAB at the northern limits of its range in North America.

Landscape Features Associated With Blacklegged Tick (Acari: Ixodidae) Density and Tick-Borne Pathogen Prevalence at Multiple Spatial Scales in Central New York State.

Blacklegged ticks (Ixodes scapularis Say, Acari: Ixodidae) are the most commonly encountered and medically relevant tick species in New York State (NY) and have exhibited recent geographic range expansion. Forests and adjacent habitat are important determinants of I. scapularis density and may influence tick-borne pathogen prevalence. We examined how percent forest cover, dominant land cover type, and habitat type influenced I. scapularis nymph and adult density, and associated tick-borne pathogen prevalence, in an inland Lyme-emergent region of NY. I. scapularis nymphs and adults were collected from edge and wooded habitats using tick drags at 16 sites in Onondaga County, NY in 2015 and 2016. A subsample of ticks from each site was tested for the presence of Borrelia burgdorferi, Borrelia miyamotoi, Anaplasma phagocytophilum, and Babesia microti using a novel multiplex real-time polymerase chain reaction (PCR) assay, and deer tick virus using reverse transcription-PCR. Habitat type (wooded versus edge) was an important determinant of tick density; however, percent forest cover had little effect. B. burgdorferi was the most commonly detected pathogen and was present in ticks from all sites. Ba. microti and deer tick virus were not detected. Habitat type and dominant land cover type were not significantly related to B. burgdorferi presence or prevalence; however, ticks infected with A. phagocytophilum and B. miyamotoi were collected more often in urban environments. Similarity between B. burgdorferi prevalence in Onondaga County and hyperendemic areas of southeastern NY indicates a more rapid emergence than expected in a relatively naive region. Possible mechanistic processes underlying these observations are discussed.

Identifying Possible Pheromones of Cerambycid Beetles by Field Testing Known Pheromone Components in Four Widely Separated Regions of the United States.

The pheromone components of many cerambycid beetles appear to be broadly shared among related species, including species native to different regions of the world. This apparent conservation of pheromone structures within the family suggests that field trials of common pheromone components could be used as a means of attracting multiple species, which then could be targeted for full identification of their pheromones. Here, we describe the results of such field trials that were conducted in nine states in the northeastern, midwestern, southern, and western United States. Traps captured 12,742 cerambycid beetles of 153 species and subspecies. Species attracted in significant numbers to a particular treatment (some in multiple regions) included 19 species in the subfamily Cerambycinae, 15 species in the Lamiinae, one species in the Prioninae, and two species in the Spondylidinae. Pheromones or likely pheromones for many of these species, such as 3-hydroxyhexan-2-one and syn- and anti-2,3-hexanediols for cerambycine species, and fuscumol and/or fuscumol acetate for lamiine species, had already been identified. New information about attractants (in most cases likely pheromone components) was found for five cerambycine species (Ancylocera bicolor [Olivier], Elaphidion mucronatum [Say], Knulliana cincta cincta [Drury], Phymatodes aeneus LeConte, and Rusticoclytus annosus emotus [Brown]), and five lamiine species (Ecyrus dasycerus dasycerus [Say], Lepturges symmetricus [Haldeman], Sternidius misellus [LeConte], Styloleptus biustus biustus [LeConte], and Urgleptes signatus [LeConte]). Consistent attraction of some species to the same compounds in independent bioassays demonstrated the utility and reliability of pheromone-based methods for sampling cerambycid populations across broad spatial scales.

Evaluating buprestid preference and sampling efficiency of the digger wasp, Cerceris fumipennis, using morphometric predictors.

In-ground colonies of the native digger wasp, Cerceris fumipennis Say (Hymenoptera: Crabronidae), were sampled over two years in four New York State counties to characterize prey range, primarily their preying on beetles in the metallic wood-boring family, Buprestidae. These records were also used to evaluate beetle sampling efficiency by comparing collected beetles to historic county records and to identify limitations of wasp-mediated sampling in study areas. Overall, 1,530 beetles representing three families and 44 beetle species were collected from C. fumipennis. Five of these species (Agrilus cuprescens (Ménétriés) (Coleoptera: Buprestidae), A. pensus Horn, Buprestis nutalli Kirby, Chrysobothris scabripennis Gory and Laporte, Dicerca pugionata (Germar)) were new prey records for C. fumipennis. The wasps exhibited a strong preference for larger beetle genera (e.g., Dicerca, Buprestis), which accounted for 68% of beetles caught. Agrilus and Chrysobothris were the next dominant genera, accounting for 16% and 11%, respectively. A 4-19 mm prey size range is proposed, as all beetles collected were within this range despite the availability of prey outside of this range. Cerceris fumipennis caught 43% of the 42 buprestids species present in museum records from the four census counties as well as an additional 23 buprestid species that were not represented in museum records. Of the 22 buprestid species identified in museum collections that were not caught by C. fumipennis in the census counties, only one was within the proposed size range and active during the C. fumipennis flight season (late June through August). Overall, sampling C. fumipennis colonies over two summers at five sites resulted in 32% of the recorded buprestid species in New York State being caught, indicating that monitoring colonies is an efficient and viable means of quantifying buprestid assemblages.

Susceptibility of two hymenopteran parasitoids of Agrilus planipennis (Coleoptera: Buprestidae) to the entomopathogenic fungus Beauveria bassiana (Ascomycota: Hypocreales).

Emerald ash borer (EAB), Agrilus planipennis Fairmaire, native to Asia, is killing ash trees (Fraxinus spp.) across 15 states and southeastern Canada. Integrated pest management using biological control is the only viable long-term approach for controlling the spread of EAB outside of host resistance. Three hymenopteran parasitoids, Spathius agrili Yang, Tetrastichus planipennisi Yang, and Oobius agrili Zhang and Huang were discovered attacking EAB in China and were approved for release in the United States in 2007. The objective of this study was to assess susceptibility of the larval parasitoid species S. agrili and T. planipennisi, relative to that of EAB, to Beauveria bassiana, an entomopathogenic fungus that infects and kills EAB adults when sprayed on ash bark or foliage. Adult EAB and parasitoids were exposed to B. bassiana inoculated ash twigs for 2 h and then monitored daily for death and signs of infection for up to 10 days. All EAB adults exposed to B. bassiana were fatally infected while mean survival for control EAB was 77%. Average survival in the treatment groups for T. planipennisi and S. agrili were 99% and 83%, respectively, indicating these parasitoids are relatively unaffected by exposure to B. bassiana. This research elucidates interactions between a fungal pathogen and two parasitoids of EAB, and provides data necessary to developing a successful multi-stage integrated management approach to control of EAB.

Partial life tables from three generations of Enaphalodes rufulus (Coleoptera: Cerambycidae).

We used life table analyses to investigate age specific mortality and to better understand the population dynamics of the red oak borer, Enaphalodes rufulus (Haldeman) (Coleoptera: Cerambycidae). We continually sampled populations within 177 trees at primarily two sites in the Ozark National Forest in Arkansas throughout three (2-yr) generations. The first cohort (adults emerged in 2003) was sampled during a severe population outbreak, whereas the second and third (2005 and 2007) were sampled during the population crash that followed. Generation mortality was 94% in 2003 and 99% in both 2005 and 2007. Estimates of apparent mortality indicated that the E. rufulus population crash likely occurred during or before the first overwintering period (2003-2004) of the generation that emerged as adults in 2005. We found limited evidence for density dependent mortality, which suggest that intraspecific competition after the first active feeding period was apparently not an important mortality factor during E. rufulus development. Life tables revealed that E. rufulus larvae generally experienced the greatest apparent mortality during the second summer of active feeding (80-94%) when larvae were feeding in, and moving between phloem and sapwood. The least apparent mortality was incurred during the following spring and early summer (26-67%) when late stage larvae and pupae were deepest and most protected within sapwood or heartwood tunnels. We found very little evidence for mortality from associated species. Scarring of vascular tissue in response to E. rufulus feeding occurred during early life stages and may be an important tree resistance mechanism and E. rufulus mortality factor.