The subapical labial sensory organ of spotted lanternfly Lycorma delicatula.

Deciphering how spotted lanternfly (SLF), an invasive polyphagous planthopper in North America, engages with its environment is a pressing issue with fundamental biological significance and economic importance. This interaction primarily depends on olfaction. However, the cellular basis of olfaction in SLF remains elusive. Here we investigate the neuronal and functional organization of the subapical labial sensory organ using scanning electron microscopy and electrophysiological recordings. This organ is believed to supply planthoppers with crucial sensory information that influences their subsequent feeding behaviour. We find in SLF that this organ comprises two identical placoid sensilla, each housing two distinct neurons. The A neuron displays a remarkable sensitivity to changes in airflow speed. Importantly, the same neuron also exhibits robust excitatory responses exclusively to three aldehydes out of a diverse pool of 85 tested odorants and inhibitory responses to 62 other odorants. By contrast, the B neuron solely serves as an olfactory detector, showing strong excitatory responses to 17 odorants and inhibitory responses to only three. The results provide a potential cellular basis for the behavioural responses of SLF to its ecologically relevant stimuli. Our study also identifies new odorants that may be useful for managing this serious pest.

Temporal and spatial dynamics of the emerald ash borer invasion in Connecticut as shown by the native digging wasp Cerceris fumipennis (Hymenoptera: Crabronidae).

Detecting and monitoring populations of the invasive emerald ash borer (EAB) is crucial to successful management of the pest and evaluation of its ecological impacts. However, the beetle's cryptic habit makes accurate monitoring costly and time-consuming. Biosurveillance takes advantage of the foraging effort of a predatory wasp Cerceris fumipennis (Hymenoptera: Crabronidae). This native, solitary, ground-nesting hunting wasp hunts adult buprestid beetles to provision its brood cells. By intercepting the hunting wasps, we can learn which species of buprestids are in the surrounding forest. The resulting data provides information on the presence and relative abundance of invasive buprestids like EAB which can supplement other monitoring efforts. In this paper we share results of ten years of biosurveillance surveys of the EAB in Connecticut. Among 112 sites, we observed EAB populations; from first detection, through the population peak and then through to the population crash, matching patterns observed in other regions of the United States. We also observed the spread of the EAB relative abundance as it moved through the state following an invasion front starting in New Haven, Co. The average time from first detection to population crash was nine years. On average, populations peaked three years after first detection, and remained at peak levels for three to four years. Population decline was gradual and took another three to four years. Notably, no evidence of a second introduction to Connecticut was seen with proportional abundance increasing over time after expanding outward from the introduction point. These results corroborate other traditional monitoring efforts in the eastern U.S. and provide independent validation of predicted population dynamics in ash stands.

Mating Behavior and Reproductive Biology of Emerald Ash Borer (Coleoptera: Buprestidae) and Two of Its Native Congeners, the Twolined Chestnut Borer and the Bronze Birch Borer.

We studied the mating behavior and reproductive biology of three members of the genus Agrilus: the bronze birch borer, Agrilus anxius Gory; the twolined chestnut borer, Agrilus bilineatus (Weber); and the emerald ash borer, Agrilus planipennis Fairmaire. All three species share a highly stereotyped mating behavior. However, the copulation duration of A. planipennis was 90% longer than that of its two congeners. Female reproductive tracts of the three species were anatomically similar, as were the spermatophores. Within the spermatophores, sperm were single in A. anxius and A. bilineatus, while in A. planipennis, sperm were bundled in groups of approximately 20 in a hyaline sheath. We found that field-caught A. anxius and A. bilineatus had higher rates of female insemination than A. planipennis. In additional studies with A. planipennis and A. anxius, we found that mating duration was related to mating success, and fecundity for A. planipennis, but not for A. anxius. For both A. planipennis and A. anxius, the spermatophore was passed to the female toward the end of the copulatory period. Sperm were found in the spermatheca immediately after copulation ended in A. planipennis and 30 min after copulation ended in A. anxius. We present possible explanations for these differences.

Establishment and Early Impact of Spathius galinae (Hymenoptera: Braconidae) on Emerald Ash Borer (Coleoptera: Buprestidae) in the Northeastern United States.

The emerald ash borer (EAB), Agrilus planipennis Fairmaire, a buprestid beetle native to Asia, has become a serious pest of ash trees (Fraxinus spp.) in North America since the early 2000s. Due to the impracticality of applying insecticides in natural forests, biocontrol is the most viable method to manage EAB in natural ecosystems. Here, we report the first evidence for the establishment and impact of Spathius galinae Belokobylskij & Strazenac, a larval parasitoid first released in North America in 2016 and 2017 at six mixed-hardwood forest sites, in Connecticut, New York, and Massachusetts. We also report current levels of abundance and parasitism of another introduced larval EAB parasitoid, Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae), released in 2015 and 2016 in these same sites. Spathius galinae was recovered at all release sites in 2018, and its density in sampled trees had increased 1.5- to 20-fold (relative to the first postrelease sample year), reaching a final density of 2.3-14.3 broods/m2 of phloem area and causing 13.1-49.2% marginal rate of parasitism at four of the six sites. In contrast, T. planipennisi was only recovered in 2018 at four of the six release sites, and both its density (0.1-2.3 broods/m2 of phloem area) and parasitism (0.1-5.6%) were lower than that of S. galinae throughout the study at the four sites where recoveries were made. Our data fill a critical gap in the development of a biocontrol-based EAB management plan to protect surviving ash trees capable of reaching maturity and producing replacement trees.

Larval Survival and Growth of Emerald Ash Borer (Coleoptera: Buprestidae) on White Ash and White Fringetree Saplings Under Well-Watered and Water-Deficit Conditions.

Emerald ash borer (Agrilus planipennis Fairmaire) was recently found on a novel host in North America, white fringetree (Chionanthus virginicus L.) (Oleaceae). In this study, we artificially infested 4-yr-old, naïve white fringetree and white ash (Fraxinus americana L.) saplings under well-watered and water-deficit conditions with emerald ash borer eggs. We used physiological and phenotypical approaches to investigate both plant response to emerald ash borer and insect development at 21, 36, and 61 d postinfestation. Photosynthesis was reduced in both tree species by larval feeding, but not by water deficits. Emerald ash borer larvae established and survived successfully on white ash. Both establishment and survival were lower on white fringetree than on white ash. Larvae were larger, and had reached higher instars at all three time points on white ash than on white fringetrees. Larvae grew faster in white ash under water-deficit conditions; however, water-deficit conditions negatively impacted survival of larvae at 61 d postinfestation in white fringetrees, although head size did not differ among surviving larvae. White ash showed higher callus formation in well-watered trees, but no impact on larval survival was observed. In white fringetree, callus formation was not affected by water treatment, and was inversely related to larval survival. The higher rate of mortality and slow growth rate of larvae in white fringetree as compared to white ash suggest that populations of emerald ash borer may be sustained by white fringetree, but may grow more slowly than in white ash.

Identification of a Pheromone Component and a Critical Synergist for the Invasive Beetle Callidiellum rufipenne (Coleoptera: Cerambycidae).

The invasive Asian cerambycid beetle Callidiellum rufipenne (Motschulsky), informally known as the Japanese cedar longhorned beetle, was first detected in North America in North Carolina in 1997. The beetle has since been detected in neighboring states and is expected to further expand its range. However, delineating the current distribution of C. rufipenne has been hindered by the lack of efficient sampling methods. Here, we present the results of research on the chemistry of volatile pheromones of C. rufipenne. Analyses of headspace odors revealed that males produce (R)-3-hydroxyhexan-2-one, with lesser amounts of (S)-3-hydroxyhexan-2-one, and (R)- and (S)-2-hydroxyhexan-3-one. In field bioassays conducted over several years in Connecticut, where populations of the beetle were well established, no reconstructed blend of these compounds was significantly attractive to beetles of either sex. However, during field trials in Japan that targeted another species, we discovered that adult male and female C. rufipenne were attracted to a blend of racemic 3-hydroxyhexan-2-one and a novel natural product, 1-(1H-pyrrol-2-yl)-1,2-propanedione. Attraction to (R)-3-hydroxyhexan-2-one and the pyrrole subsequently was confirmed in field trials in Connecticut. Although it is unclear why the pyrrole acts as a synergist for a species that apparently does not produce it, the serendipitous discovery that adult C. rufipenne are attracted by the blend of ketone and pyrrole provides a badly needed method for monitoring its ongoing range expansion within North America, and for detecting new introductions in other parts of the world.

Identification of an important component of the contact sex pheromone of Callidiellum rufipenne (Coleoptera: Cerambycidae).

Adult male and female Callidiellum rufipenne (Motschulsky) (Coleoptera: Cerambycidae) aggregate on severely stressed or fallen trees and cut logs of cypress species (Cupressaceae) that are the hosts of their larvae. Our studies showed that male C. rufipenne actively search for females on these trees and only respond to females after contacting them with their antennae. Removing cuticular hydrocarbons from fresh carcasses of females with solvent rendered the carcasses unattractive to males, but activity was restored when the solvent extract was reapplied. These findings suggest that contact pheromones mediate mate recognition in this species. Bioassays of fractions of the extracts determined that the branched chain hydrocarbon fraction was primarily responsible for activity. 5,17-Dimethylnonacosane was a key sex-specific component in extracts of females, and synthetic 5,17-dimethylnonacosane elicited a strong mating response from males. We conclude that this compound is an important component of the contact sex pheromone of C. rufipenne if not the sole component. Solvent extracts of both sexes also contained 9-pentacosyne and 9-heptacosyne. To our knowledge, this is only the second report of alkynes in the cuticular lipids of insects.

First report of an attractant for a tumbling flower beetle (Coleoptera: Mordellidae).

In 2004 and 2005, large numbers of the tumbling flower beetle, Falsomordellistena bihamata (Melsheimer), were found on traps baited with sweet birch oil, whereas significantly fewer individuals were found on control traps. In both years, peak captures were at 680 DD10 degrees C. Trapping was conducted in Naugatuck State Forest in Naugatuck, CT. Little is known about the ecology and biology of the tumbling flower beetles (Coleoptera: Mordellidae), and the larval food plant for this species is not known. Thus, we cannot say why the beetle is attracted to sweet birch oil. Sweet birch oil is approximately 99.8% methyl salicylate (MeSA). MeSA is found constitutively in large quantities in some plants, but it is also an important signal in, and product of, plant stress-response pathways. MeSA has been found to attract both herbivores that need stressed plants as food and natural enemies of herbivores in stressed plants. To our knowledge, this is the first report of mass trapping of a tumbling flower beetle. Fuller understanding of the phenomenon awaits further study.

Soybean plant stage and population growth of soybean aphid.

The soybean aphid, Aphis glycines Matsumura, is a newly invasive species of aphid in North America. Previous studies disagree as to whether soybean, Glycine max (L.) Merr., plant stage has an impact on aphid intrinsic rate of increase. Therefore, the growth rate of soybean aphids on soybean plants of different stages was examined at two different scales in the field. A planting date experiment was used to measure the population growth of soybean aphids on plants of different stages. Clip-cages were used to measure life history characteristics of individual aphids on plants of different stages. No differences were found in the population growth or dynamics of soybean aphids in the planting date experiment. The life history characteristics of individual aphids also showed no significant difference when feeding on different growth stages of soybean plants. The impact of these findings on soybean aphid management is discussed and the possible reasons why the results differ from previous estimates of the aphid growth-plant stage relationship are considered.

Arthropod diversity in peas with normal or reduced waxy bloom.

Crop traits can alter economically important interactions between plants, pests, and biological control agents. For example, a reduced waxy bloom on the surface of pea plants alters interactions between pea aphids and their natural enemies. In this study, we assess whether the effect of wax reduction extends beyond the 2 or 3 arthropod species closely associated with the plants and into the structure of the broader arthropod community of over 200 taxa at our site. We sampled arthropods on lines of peas with normal and reduced wax in Latah Co., Idaho using pitfall traps within randomly assigned pairs of 5 x 5 meter plots. During the 1998 and 1999 growing seasons, we collected 12,113 individual arthropods from 221 unambiguously identified morphospecies. The number of individuals collected from each morphospecies responded idiosyncratically to the reduced wax peas. To test whether arthropod community structure differed between the collections from plots having peas with normal or reduced wax, we performed a randomization test. The collection from peas with reduced wax had higher species evenness and thus higher community diversity despite having lower species richness. Our results demonstrate the potential of a single plant trait, epicuticular wax, to affect a community of arthropods. Two pests of peas had opposite responses to peas with reduced wax. The number of pea aphids collected was greater from peas with normal wax peas than those with reduced wax. In contrast, the number of pea leaf weevils collected was greater from peas with reduced wax.

Effects of a simple plant morphological mutation on the arthropod community and the impacts of predators on a principal insect herbivore.

Plant features that enhance predator effectiveness can be considered extrinsic-resistance factors because they result in reduced insect herbivory. In this paper we test the hypothesis that reduced epicuticular wax (EW) in Pisum sativum L. is an extrinsic-resistance factor contributing to field resistance to Acyrthosiphon pisum (Harris). We monitored pea aphid populations in the field on reduced EW and normal EW near isolines of peas for two seasons and confirmed that aphid populations are lower on reduced EW peas than on normal EW peas. We also monitored predators within the canopies of the two pea lines to discover community level patterns in response to differences in EW. We found that while predator numbers were similar between the two lines, there were more syrphids on the normal EW peas, and a trend towards more coccinellids on reduced EW peas. We tested the impact of predators on pea aphids on the two EW lines by monitoring their population levels in cages that excluded predators, and in cages that allowed predators to enter. We found that pea aphid populations were similar on the two EW lines when predators were excluded. When predators were allowed access to the plants, pea aphid populations were reduced more on reduced EW peas than on normal EW peas. We also examined the intrinsic resistance to aphids in reduced EW peas with laboratory dual-choice tests comparing aphid response to reduced EW and normal EW peas, and found that walking, apterous aphids displayed no preference for one pea line over the other. Bioassays to measure growth and fecundity of the pea aphid on the two EW types in the greenhouse and in the field showed that intrinsic rate of increase, and other life table parameters, were not different for aphids on the two lines. Together these results support the hypothesis that reduced EW in peas is a predator-dependent extrinsic resistance factor. Genetically reducing EW bloom in peas and other waxy crop plants might improve the effectiveness of arthropod natural enemies of insect pests. More generally, the results show that a subtle change in plant morphology can substantially influence the impact of predators on insect herbivore populations. The benefit of extrinsic resistance to herbivory conferred by reduced EW may balance any benefits of a prominent EW bloom, thereby sustaining EW polymorphisms in some natural plant populations.