Do adult Magicicada (Hemiptera: Cicadidae) feed? Historical perspectives and evidence from molecular gut content analysis.

The periodical cicadas in the genus Magicicada are remarkable for their unusual life histories and dramatic synchronized emergences every 13 or 17 years. While aspects of their evolution, mating behaviors, and general biology have been well-characterized, there is surprising uncertainty surrounding the feeding habits of the short-lived adult stage. Despite a tentative scientific consensus to the contrary, the perception that adult Magicicada do not feed has persisted among the general public, and recent studies are lacking. We directly investigated the feeding behavior of Magicicada spp. through high-throughput sequencing (HTS)-based dietary analysis of nymphs, freshly molted (teneral) adults, and fully sclerotized adults collected from orchard and wooded habitats during the 2021 emergence of Brood X. Identifiable plant DNA (trnF, ITS amplicons) was successfully recovered from nymphs and adults. No plant DNA was recovered from teneral adults, suggesting that all DNA recovered from sclerotized adults was ingested during the post-teneral adult stage. Both nymphs and adults were found to have ingested a range of woody and herbaceous plants across 17 genera and 14 families. Significantly more plant genera per individual were recovered from adults than from nymphs, likely reflecting the greater mobility of the adult stage. We hypothesize that the demonstrated ingestion of plant sap by Magicicada adults is driven by a need to replace lost water and support specialized bacteriome-dwelling endosymbionts that cicadas depend upon for growth and development, which constitutes true feeding behavior.

Gut microbiome insights from 16S rRNA analysis of 17-year periodical cicadas (Hemiptera: Magicicada spp.) Broods II, VI, and X.

Periodical cicadas (Hemiptera: Magicicada) have coevolved with obligate bacteriome-inhabiting microbial symbionts, yet little is known about gut microbial symbiont composition or differences in composition among allochronic Magicicada broods (year classes) which emerge parapatrically or allopatrically in the eastern United States. Here, 16S rRNA amplicon sequencing was performed to determine gut bacterial community profiles of three periodical broods, including II (Connecticut and Virginia, 2013), VI (North Carolina, 2017), and X (Maryland, 2021, and an early emerging nymph collected in Ohio, 2017). Results showed similarities among all nymphal gut microbiomes and between morphologically distinct 17-year Magicicada, namely Magicicada septendecim (Broods II and VI) and 17-year Magicicada cassini (Brood X) providing evidence of a core microbiome, distinct from the microbiome of burrow soil inhabited by the nymphs. Generally, phyla Bacteroidetes [Bacteroidota] (> 50% relative abundance), Actinobacteria [Actinomycetota], or Proteobacteria [Pseudomonadota] represented the core. Acidobacteria and genera Cupriavidus, Mesorhizobium, and Delftia were prevalent in nymphs but less frequent in adults. The primary obligate endosymbiont, Sulcia (Bacteroidetes), was dominant amongst core genera detected. Chryseobacterium were common in Broods VI and X. Chitinophaga, Arthrobacter, and Renibacterium were common in Brood X, and Pedobacter were common to nymphs of Broods II and VI. Further taxonomic assignment of unclassified Alphaproteobacteria sequencing reads allowed for detection of multiple copies of the Hodgkinia 16S rRNA gene, distinguishable as separate operational taxonomic units present simultaneously. As major emergences of the broods examined here occur at 17-year intervals, this study will provide a valuable comparative baseline in this era of a changing climate.

Influence of Landscape Factors and Abiotic Conditions on Dispersal Behavior and Overwintering Site Selection by Halyomorpha halys (Hemiptera: Pentatomidae).

Since the initial detection of the invasive Halyomorpha halys (Stål) in the United States in the late 1990s, this insect has emerged as a severe agricultural and nuisance pest. Nuisance problems are due to adult dispersal to overwintering sites in the fall at which time they alight onto and eventually settle within human-made structures in addition to natural harborage. This study examined how three factors, elevation, light, and moisture affected overwintering site selection by H. halys in the mid-Atlantic. Observational counts performed along elevational transects revealed elevation was significant predictor of H. halys abundance during both years of the study in 2014 and 2015 with more adults observed at higher elevations. Choice tests examining effects of moisture and light on settling behavior demonstrated H. halys settled within overwintering shelter boxes in significantly greater numbers when shelters were dry compared with those having moist conditions, and in darkened shelters compared with those augmented with LED lights. Our findings indicate that H. halys use cues at both landscape and very localized levels when seeking and selecting overwintering sites.

Invasive stink bug favors naïve plants: Testing the role of plant geographic origin in diverse, managed environments.

With the introduction and establishment of exotic species, most ecosystems now contain both native and exotic plants and herbivores. Recent research identifies several factors that govern how specialist herbivores switch host plants upon introduction. Predicting the feeding ecology and impacts of introduced generalist species, however, remains difficult. Here, we examine how plant geographic origin, an indicator of shared co-evolutionary history, influences patterns of host use by a generalist, invasive herbivore, while accounting for variation in plant availability. The brown marmorated stink bug, Halyomorpha halys, is a highly polyphagous Asian herbivore and an economically important invasive pest in North America and Europe. In visual surveys of 220 plant taxa in commercial nurseries in Maryland, USA, H. halys was more abundant on non-Asian plants and selected these over Asian plants. The relationship between the relative use of plants and their availability was strongly positive but depended also on plant origin at two of our three sites, where the higher relative use of non-Asian plants was greatest for highly abundant taxa. These results highlight the importance of considering both plant origin and relative abundance in understanding the selection of host plants by invasive generalist herbivores in diverse, natural and urban forests.

Host Plant Use by the Invasive Halyomorpha halys (Stål) on Woody Ornamental Trees and Shrubs.

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an invasive plant-feeding insect native to eastern Asia. This herbivore is highly polyphagous, feeding on and damaging diverse plants, including field crops, vegetables, tree fruits, and ornamentals. Woody ornamental plants provide early- and late-season resources for adults emerging from and returning to overwintering sites, as well as feeding and breeding sites for H. halys throughout the growing season. In this study, we quantify the use of diverse plants by H. halys in two commercial nurseries in Maryland, recording data on the abundance of egg masses, early and late instar nymphs, and adults over a three-year study period. Our specific goals were to provide a quantitative comparison of the use of diverse plant species and cultivated varieties, identify non-hosts that could be used to create landscapes refractory to H. halys, and determine whether the use of plants varied across life stages of H. halys or the taxonomic status of plants. We found broad use of diverse plants in this study, identifying 88 host plants used by all life stages of H. halys. We also highlight the 43 plant taxa that did not support any life stage of H. halys and are thus classified as non-hosts. Interestingly, some of these plants were congeners of highly-used plants, underscoring high intrageneric and intraspecific variation in the use of plants by this polyphagous herbivore. We discuss how the selective planting of non-hosts, especially gymnosperms, may aid in reducing the agricultural and nuisance pest status of this invasive insect.

Edge Effects Influence the Abundance of the Invasive Halyomorpha halys (Hemiptera: Pentatomidae) in Woody Plant Nurseries.

The invasive brown marmorated stink bug, Halyomorpha halys (Stål), has caused severe economic losses in the United States and is also a major nuisance pest invading homes. In diverse woody plant nurseries, favored host plants may be attacked at different times of the season and in different locations in the field. Knowledge of factors influencing H. halys abundance and simple methods to predict where H. halys are found and cause damage are needed to develop effective management strategies. In this study, we examined H. halys abundance on plants in tree nurseries as a function of distance from field edges (edge and core samples) and documented the abundance in tree nurseries adjoining different habitat types (corn, soybean, residential areas, and production sod). We conducted timed counts for H. halys on 2,016 individual trees belonging to 146 unique woody plant cultivars at two commercial tree nurseries in Maryland. Across three years of sampling, we found that H. halys nymphs and adults were more abundant at field edges (0-5 m from edges) than in the core of fields (15-20 m from edges). Proximity of soybean fields was associated with high nymph and adult abundance. Results indicate that monitoring efforts and intervention tactics for this invasive pest could be restricted to field edges, especially those close to soybean fields. We show clearly that spatial factors, especially distance from edge, strongly influence H. halys abundance in nurseries. This information may greatly simplify the development of any future management strategies.

Traps and trap placement may affect location of brown marmorated stink bug (Hemiptera: Pentatomidae) and increase injury to tomato fruits in home gardens.

The invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is an important pest of field crops, fruit orchards, commercial vegetables, ornamental plants, and home vegetable gardens. Pheromone-baited traps designed to attract, trap, and kill H. halys are marketed for use in home gardens to reduce damage to plants. To test this assertion, we conducted the following experiment: One group of 15 gardeners placed stink bug traps at the end of a row of tomatoes, Solanum lycopersicum (L.), in their vegetable garden and another group of 14 placed no traps in their garden and served as controls. Gardeners with traps were no more or less likely to have H. halys on tomato plants than those without traps, but the abundance of H. halys on tomato fruits was marginally greater in gardens with traps. However, tomato fruits grown in gardens with traps sustained significantly more injury than tomato fruits grown in gardens without traps. Furthermore, tomato fruits on plants near the trap housed more H. halys than tomato fruits on plants at the end of a row away from the trap. Traps may be useful in identifying gardens where H. halys is likely to be found and ones in which stink bug injury to tomatoes is likely. We found no evidence that stink bug traps protected tomatoes from H. halys, and it appears that the addition of traps to gardens may increase injury to tomato fruits.

Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants.

BACKGROUND: Chemical suppression of arthropod herbivores is the most common approach to plant protection. Insecticides, however, can cause unintended, adverse consequences for non-target organisms. Previous studies focused on the effects of pesticides on target and non-target pests, predatory arthropods, and concomitant ecological disruptions. Little research, however, has focused on the direct effects of insecticides on plants. Here we demonstrate that applications of neonicotinoid insecticides, one of the most important insecticide classes worldwide, suppress expression of important plant defense genes, alter levels of phytohormones involved in plant defense, and decrease plant resistance to unsusceptible herbivores, spider mites Tetranychus urticae (Acari: Tetranychidae), in multiple, distantly related crop plants. METHODOLOGY/PRINCIPAL FINDINGS: Using cotton (Gossypium hirsutum), corn (Zea mays) and tomato (Solanum lycopersicum) plants, we show that transcription of phenylalanine ammonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase are suppressed and concentrations of the phytohormone OPDA and salicylic acid were altered by neonicotinoid insecticides. Consequently, the population growth of spider mites increased from 30% to over 100% on neonicotinoid-treated plants in the greenhouse and by nearly 200% in the field experiment. CONCLUSIONS/SIGNIFICANCE: Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species. More importantly, this is the first study to document insecticide-mediated disruption of plant defenses and link it to increased population growth of a non-target herbivore. This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

Direct and indirect effects of imidacloprid on fecundity and abundance of Eurytetranychus buxi (Acari: Tetranychidae) on boxwoods.

Populations of spider mites often reach high levels on urban plants. In many cases, insecticide applications targeting other herbivores trigger outbreaks of spider mites. Recently, elevated populations of spider mites on a diversity of plants in urban landscapes have been associated with applications of imidacloprid, a neonicotinoid insecticide. Imidacloprid has also been linked to increased fecundity in two species of spider mites. In this study, we evaluated the indirect (plant-mediated) and direct impact of imidacloprid on fecundity and longevity of Eurytetranychus buxi Garman (Acari: Tetranychidae), feeding on boxwoods, Buxus sempervirens L. Moreover, we compared the abundance of E. buxi on imidacloprid-treated and untreated boxwoods in the landscape and a greenhouse to determine if changes in the fecundity of mites exposed to imidacloprid were linked to outbreaks of E. buxi. We found that females consuming imidacloprid-treated plants laid more eggs than females feeding on untreated boxwoods, while their longevity remained unchanged. Fecundity was not affected, however, when spider mites were directly sprayed with imidacloprid and consumed foliage of untreated boxwoods. Furthermore, populations of E. buxi were greater on boxwoods treated with imidacloprid in the landscape and greenhouse. On landscape boxwoods, elevated populations of E. buxi persisted into a second year. We also observed general lack of predators of spider mites on treated and untreated boxwoods in the field suggesting that imidacloprid's eruptive effect on E. buxi stems more from indirect changes in plant quality than from a loss of top-down regulation from E. buxi's natural enemies.

Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes.

BACKGROUND: Attempts to eradicate alien arthropods often require pesticide applications. An effort to remove an alien beetle from Central Park in New York City, USA, resulted in widespread treatments of trees with the neonicotinoid insecticide imidacloprid. Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues. However, unexpected outbreaks of a formerly innocuous herbivore, Tetranychus schoenei (Acari: Tetranychidae), followed imidacloprid applications to elms in Central Park. This undesirable outcome necessitated an assessment of imidacloprid's impact on communities of arthropods, its effects on predators, and enhancement of the performance of T. schoenei. METHODOLOGY/PRINCIPAL FINDINGS: By sampling arthropods in elm canopies over three years in two locations, we document changes in the structure of communities following applications of imidacloprid. Differences in community structure were mostly attributable to increases in the abundance of T. schoenei on elms treated with imidacloprid. In laboratory experiments, predators of T. schoenei were poisoned through ingestion of prey exposed to imidacloprid. Imidacloprid's proclivity to elevate fecundity of T. schoenei also contributed to their elevated densities on treated elms. CONCLUSIONS/SIGNIFICANCE: This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism. Laboratory experiments provide evidence that imidacloprid debilitates insect predators of spider mites suggesting that relaxation of top-down regulation combined with enhanced reproduction promoted a non-target herbivore to pest status. With global commerce accelerating the incidence of arthropod invasions, prophylactic applications of pesticides play a major role in eradication attempts. Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

Robert F. Denno (1945-2008): insect ecologist extraordinaire.

Robert F. Denno was widely recognized as one of the leading insect ecologists in the world. He made major contributions to the study of plant-insect interactions, dispersal, interspecific competition, predator-prey interactions, and food web dynamics. He was especially well known for his detailed and comprehensive study of the arthropods that inhabit salt marshes. Denno promoted a research approach that included detailed knowledge of the natural history of the study system, meticulous experiments that often pushed logistical possibilities, and a focus on important ecological questions of the day. He was an enthusiastic collaborator and excellent mentor who invested incredible amounts of time and energy in the training and placement of graduate students and postdoctoral associates. As a result, Denno's legacy will continue to shape the field of insect ecology for generations to come.

Ecology of herbivorous arthropods in urban landscapes.

Urbanization affects communities of herbivorous arthropods and provides opportunities for dramatic changes in their abundance and richness. Underlying these changes are creation of impervious surfaces; variation in the density, diversity, and complexity of vegetation; and maintenance practices including pulsed inputs of fertilizers, water, and pesticides. A rich body of knowledge provides theoretical underpinnings for predicting and understanding impacts of urbanization on arthropods. However, relatively few studies have elucidated mechanisms that explain patterns of insect and mite abundance and diversity across urbanization gradients. Published accounts suggest that responses to urbanization are often taxon specific, highly variable, and linked to properties of urbanization that weaken top-down and/or bottom-up processes, thereby destabilizing populations of herbivores and their natural enemies. In addition to revealing patterns in diversity and abundance of herbivores across urbanization gradients, a primary objective of this review is to examine mechanisms underlying these patterns and to identify potential hypotheses for future testing.

Phylogeography of a specialist insect, Adelges cooleyi: historical and contemporary processes shape the distribution of population genetic variation.

Adelges cooleyi is a host-alternating, gall-making insect native to the Rocky Mountains and Cascade Mountains in western North America. The insect's primary hosts are Picea (spruce) species, and its secondary host is Pseudotsuga menziesii, Douglas fir. To determine whether there are large-scale patterns of genetic variation in this specialist insect, we created molecular phylogenies of geographically separate samples of A. cooleyi using sequence data from two mitochondrial (mtDNA) genes and amplified fragment length polymorphisms (AFLPs). Three divergent mtDNA lineages were identified. Analysis of mtDNA and AFLP genetic variation revealed that samples from southeastern Arizona are genetically isolated from all other samples. AFLP data identified possible gene flow between individuals from divergent mtDNA lineages in an area in the central Rocky Mountains. Factors that likely affected divergence within A. cooleyi were identified by comparing our conclusions with well-known changes in the distribution of vegetation in response to glaciations and previous phylogeographical work conducted on this specialist insect's host-plants. In addition to documenting previously unknown patterns of genetic variation in A. cooleyi, our work provides the basis for a testable hypothesis regarding the extent to which the distribution of variation in Picea and Pseudotsuga hosts mediates the distribution of genetic variation for this specialist insect.

Do top-down or bottom-up forces determine Stephanitis pyrioides abundance in urban landscapes?

This study examined the influence of habitat structural complexity on the collective effects of top-down and bottom-up forces on herbivore abundance in urban landscapes. The persistence and varying complexity of urban landscapes set them apart from ephemeral agroecosystems and natural habitats where the majority of studies have been conducted. Using surveys and manipulative experiments. We explicitly tested the effect of natural enemies (enemies hypothesis), host plant quality, and herbivore movement on the abundance of the specialist insect herbivore, Stephanitis pyrioides, in landscapes of varying structural complexity. This herbivore was extremely abundant in simple landscapes and rare in complex ones. Natural enemies were the major force influencing abundance of S. pyrioides across habitat types. Generalist predators, particularly the spider Anyphaena celer, were more abundant in complex landscapes. Predator abundance was related to greater abundance of alternative prey in those landscapes. Stephanitis pyrioides survival was lower in complex habitats when exposed to endemic natural enemy populations. Laboratory feeding trials confirmed the more abundant predators consumed S. pyrioides. Host plant quality was not a strong force influencing patterns of S. pyrioides abundance. When predators were excluded, adult S. pyrioides survival was greater on azaleas grown in complex habitats, in opposition to the observed pattern of abundance. Similarly, complexity did not affect S. pyrioides immigration and emigration rates. The complexity of urban landscapes affects the strength of top-down forces on herbivorous insect populations by influencing alternative prey and generalist predator abundance. It is possible that habitats can be manipulated to promote the suppressive effects of generalist predators.

Comparison of exclusion and imidacloprid for reduction of oviposition damage to young trees by periodical cicadas (Hemiptera: Cicadidae).

Insecticides are traditionally used to control periodical cicadas (Homoptera: Cicadidae) and to reduce associated injury caused by oviposition. However, research has shown that conventional insecticides have low or variable season-long efficacy in reducing injury caused by cicadas. New systemic neonicotinoid insecticides provide excellent levels of control against a variety of sucking insects. We compared the efficacy of a neonicotinoid insecticide, imidacloprid, and a nonchemical control measure, netting, to reduce cicada injury. Netted trees sustained very little injury, whereas unprotected trees were heavily damaged. Fewer eggnests, scars, and flags were observed on trees treated with imidacloprid compared with unprotected trees; however, the hatching of cicada eggs was unaffected by imidacloprid.

Behavioral responses of a leaf beetle to injury-related changes in its salicaceous host.

Adults of the leaf beetle Plagiodera versicolora Laich, avoided previously injured shoots of Salix alba 'Tristis' in favor of nearby uninjured ones. The response was rapid and persisted for five days of study. During brief periods of observation, the vast majority of beetles engaged in behaviors other than locomotion such as feeding and resting. Furthermore, the proportions of beetles walking were similar on injured and uninjured shoots. It appears that under these experimental conditions previous injury did not greatly increase searching behavior of the beetles. Leaves on previously injured shoots received less subsequent herbivory than uninjured ones. Findings of these experiments are consistent with patterns of herbivory observed in the field and known reproductive responses of beetles to diets of injured leaves. These results provide new information toward understanding relatively low levels of herbivory on individual willow leaves associated with the feeding of P. versicolora.