Zsofia Szendrei

A meta-analysis of insect pest behavioral manipulation with plant volatiles

Many insect pests utilize plant volatiles for host location and untangling the mechanisms of this process can provide tools for pest management. Numerous experimental results have been published on the effect of plant volatiles on insect pests. We used a meta‐analysis to summarize this knowledge and to look for patterns. Our goal was to identify herbivore and plant traits that might explain the herbivores’ behavioral response to plant volatiles in field applications. We scored a total of 374 unique plant volatile‐insect herbivore interactions obtained from 34 published studies investigating 50 herbivore pest species. Attractants had a significant effect on insect herbivore abundance but repellents did not; this latter result could be a result of the comparatively small number of field studies that tested plant volatiles as repellents (3%). Females were significantly more attracted to plant volatile baits than males. The diet breadth of herbivores was independent of a behavioral response to plant volatiles, but more case studies show effects of volatiles on chewers, followed by wood‐borers and sap‐feeders. There are more demonstrations of attraction to plant volatiles in Lepidoptera than in Thysanoptera. The method of plant volatile application had a significant effect on herbivore abundance and increasing the number of chemicals in individual baits attracted more herbivores. The magnitude of the response of herbivores to plant volatiles in forest and agricultural habitats was similar. We explore consistent patterns and highlight areas needing research in using plant volatiles to manage insect pests.

Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences

The process of selecting certain desirable traits for plant breeding may compromise other potentially important traits, such as defences against pests; however, specific phenotypic changes occurring over the course of domestication are unknown for most domesticated plants. Cranberry (Vaccinium macrocarpon) offers a unique opportunity to study such changes: its domestication occurred recently, and we have access to the wild ancestors and intermediate varieties used in past crosses. In order to investigate whether breeding for increased yield and fruit quality traits may indirectly affect anti-herbivore defences, the chemical defences have been examined of five related cranberry varieties that span the history of domestication against a common folivore, the gypsy moth (Lymantria dispar). Direct defences were assessed by measuring the performance of gypsy moth caterpillars and levels of phenolic compounds in leaves, and indirect defences by assaying induced leaf volatile emissions. Our results suggest that breeding in cranberry has compromised plant defences: caterpillars performed best on the derived NJS98-23 (the highest-yielding variety) and its parent Ben Lear. Moreover, NJS98-23 showed reduced induction of volatile sesquiterpenes, and had lower concentrations of the defence-related hormone cis-jasmonic acid (JA) than ancestral varieties. However, induced direct defences were not obviously affected by breeding, as exogenous JA applications reduced caterpillar growth and increased the amounts of phenolics independent of variety. Our results suggest that compromised chemical defences in high-yielding cranberry varieties may lead to greater herbivore damage which, in turn, may require more intensive pesticide control measures. This finding should inform the direction of future breeding programmes.

Choosing natural enemies for conservation biological control: use of the prey detectability half-life to rank key predators of Colorado potato beetle

Determining relative strengths of trophic links is critical for ranking predators for conservation biological control. Molecular gut‐content analysis enables ranking by incidence of prey remains in the gut, but differential digestive rates bias such rankings toward predators with slower rates. This bias can be reduced by indexing each predator’s half‐life to that of the middle‐most half‐life in a predator complex. We demonstrate this with data from key species in the predator complex of Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), comprising adults and immatures of four taxonomically diverse species. These animals display order‐of‐magnitude variation in detectability half‐life for the cytochrome oxidase I DNA sequence of a single CPB egg: from 7.0 h in larval Coleomegilla maculata (DeGeer) (Coleoptera: Coccinellidae) to 84.4 h in nymphal Perillus bioculatus (Fabricius) (Hemiptera: Pentatomidae). The raw species‐specific incidence of L. decemlineata DNA in the guts of 351 field‐collected predators ranged from 11 to 95%, ranking them as follows: C. maculata adults < Lebia grandis Hentz (Coleoptera: Carabidae) adults < Podisus maculiventris (Say) (Hemiptera: Pentatomidae) adults < P. maculiventris nymphs < P. bioculatus adults < P. bioculatus nymphs. Half‐life adjustment reorders the rankings: C. maculata adults < P. bioculatus adults < P. bioculatus nymphs < P. maculiventris nymphs < L. grandis adults < P. maculiventris adults. These changes in status demonstrate the value of half‐life‐adjusted molecular gut‐content data for ranking predators. This is the first study to measure prey detectability half‐lives for the key arthropod predators of a major insect pest, and to use them to evaluate the relative impact of all adults and immatures in this predator complex.

Resistance to neonicotinoid insecticides in field populations of the Colorado potato beetle (Coleoptera: Chrysomelidae)

BACKGROUND Neonicotinoid insecticides were first used commercially for Colorado potato beetle [Leptinotarsa decemlineata (Say), Coleoptera: Chrysomelidae] control in the United States in 1995, and since then have been critical for management of this pest. Field populations from the northeastern and midwestern United States were tested from 1998 to 2010 for susceptibility to imidacloprid and thiamethoxam using standard topical dose assays with adults. RESULTS From 1998 to 2001, imidacloprid resistance was present in only a few locations in the eastern United States. By 2003, imidacloprid resistance was common in the northeastern Unites States. In 2004, imidacloprid resistance in Colorado potato beetle was detected for the first time in the midwestern United States. In 2003, the first case of resistance to thiamethoxam was found in a population from Massachusetts. Neonicotinoid resistance in summer-generation adults was higher than in overwintered adults from the same locations. By 2009, 95% of the populations tested from the northeastern and midwestern United States had significantly higher LD(50) values for imidacloprid than the susceptible population. CONCLUSIONS The increasing resistance to neonicotinoid insecticides raises concerns for the continued effective management of Colorado potato beetles in potatoes and highlights the need for more rigorous practice of integrated pest management methods.

Response of Cranberry Weevil (Coleoptera: Curculionidae) to Host Plant Volatiles

ABSTRACT The oligophagous cranberry weevil, Anthonomus musculus Say, causes economic losses to blueberry growers in New Jersey because females deposit eggs into developing flower buds and subsequent larval feeding damages buds, which fail to produce fruit. A cost-effective and reliable method is needed for monitoring this pest to correctly time insecticide applications. We studied the behavioral and antennal responses of adult A. musculus to its host plant volatiles to determine their potential for monitoring this pest. We evaluated A. musculus response to intact and damaged host plant parts, such as buds and flowers in Y-tube bioassays. We also collected and identified host plant volatiles from blueberry buds and open flowers and performed electroantennograms with identified compounds to determine the specific chemicals eliciting antennal responses. Male weevils were more attracted to blueberry flower buds and were repelled by conspecific-damaged buds compared with clean air. In contrast, females were more attracted to open flowers compared with flower buds. Nineteen volatiles were identified from blueberry buds; 10 of these were also emitted from blueberry flowers. Four of the volatiles emitted from both blueberry buds and flowers [hexanol, (Z)-S-hexenyl acetate, hexyl acetate, and (Z)-3-hexenyl butyrate] elicited strong antennal responses from A. musculus. Future laboratory and field testing of the identified compounds in combination with various trap designs is planned to develop a reliable monitoring trap for A. musculus.

Ground predator abundance affects prey removal in highbush blueberry (Vaccinium corymbosum) fields and can be altered by aisle ground covers

Habitat management to conserve natural enemies has increased biological control of insect pests in various cropping systems [Annu. Rev. Entomol. 45: 175–201, 2000]. We wanted to determine if insect predation in highbush blueberry, Vaccinium corymbosum L. (Ericales: Ericaceae), is influenced by manipulation of edaphic arthropod community and whether management of ground cover in aisles between blueberry rows enhances this community. The first question was studied in blueberry plots bounded by trenches permitting selective movement into plots (ingress) or out of plots (egress), as well as unbounded control plots. We observed a significant effect of boundary type on the arthropod communities’ relative abundance as measured with pitfall traps, with relative abundance highest in ingress plots, intermediate in control plots and lowest in egress plots. Effects of ground arthropod abundance on predation rates were assessed with onion fly, Delia antiqua (Meigen) (Diptera: Anthomyiidae), pupae as sentinel prey. Pupa recovery was greatest in egress boundary plots, intermediate in control plots and lowest in ingress boundary plots. Regression analyses indicate pupal recovery rate decreased as a function of carabid abundance as well as the abundance of non-insect ground predators. To determine if ground cover management influenced natural enemy abundance, aisles were clean cultivated or planted with three ground covers (clover, ryegrass, or buckwheat). Increasing ground cover had a significant effect on the relative abundance of Harpalus pensylvanicus De Geer (Coleoptera: Carabidae). In addition to conserving natural enemies for control of blueberry insect pests, we discuss additional benefits of ground covers that may increase their utility for blueberry production.

Cover Crop Mulch and Weed Management Influence Arthropod Communities in Strip-Tilled Cabbage

ABSTRACT Cover crop mulch and weeds create habitat complexity in agricultural fields that may influence arthropods. Under strip-tillage systems, planting rows are tilled and preestablished cover crops can remain between rows. In field experiments conducted in Michigan in 2010 and 2011, a preestablished oat (Avena sativa L.) cover crop was allowed to grow between rows of strip-tilled cabbage and killed at 0, 9–14, or 21–27 d after transplanting (DAT). The effects of herbicide intensity and oat kill date on arthropods, weeds, and crop yield were examined. Two levels of herbicide intensity (low or high) were used to manipulate habitat vegetational complexity, with low weed management intensity resulting in more weeds, particularly in 2010. Oat kill date manipulated the amount of cover crop mulch on the soil surface. Later oat kill dates were associated with higher natural enemy abundance. Reduced herbicide intensity was associated with 1) lower abundance of several key cabbage (Brassica oleraceae L.) pests, and 2) greater abundance of important natural enemy species. Habitats with both later oat kill dates and reduced herbicide intensity contained 1) fewer herbivores with chewing feeding guilds and more specialized diet breadths, and 2) greater abundance of active hunting natural enemies. Oats reduced cabbage yield when oat kill was delayed past 9–14 DAT. Yields were reduced under low herbicide intensity treatments in 2010 when weed pressure was greatest. We suspect that increased habitat complexity associated with oat mulches and reduced herbicide intensity enhances biological control in cabbage, although caution should be taken to avoid reducing yields or enhancing hyperparasitism.

Ground Covers Influence the Abundance and Behavior of Japanese Beetles

Abstract Ground covers were tested for 3 consecutive yr for their effect on Japanese beetle, Popillia japonica Newman (Coleoptera: Scarabaeidae), abundance and behavior in a blueberry planting. Alsike clover (Trifolium hybridum L.), buckwheat (Fagopyrum esculentum Moench), perennial ryegrass (Lolium perenne L.), and bare ground were compared within row-middles for their effect on abundance of adult female beetles, female beetle behavior after landing, density of larvae in the soil, and survival of larvae. Adult beetles were consistently most abundant on buckwheat, followed by clover and ryegrass, while they were generally absent from bare ground plots. Larval density was three times greater in ryegrass and clover than in buckwheat, with the fewest found in bare ground. There was high variability in larval survival within treatments, but overall survival was highest in plots with ryegrass. Observations of adult beetles revealed that the proportion of time spent feeding and the frequency of feeding were higher on buckwheat and clover than on ryegrass, and the average duration of digging bouts lasted longer on ryegrass than on the other two plant treatments. These results reveal that adult P. japonica behavior is affected by cover crops and that this behavior translates into variation in larval density of this pest.

Habitat manipulation in potato affects Colorado potato beetle dispersal

Increased habitat complexity in agricultural fields can alter the movement of pests into or within a field. Using a mark–release–recapture method with Colorado potato beetle [Leptinotarsa decemlineata (Say)], we compared the tenure time and dispersal of marked insects released within experimental potato fields to those released at the field borders in three trials in summer 2006. Plots within fields had rye, vetch or no plant residues. Movement of marked Colorado potato beetles into the tilled plots was significantly higher than into vetch or rye cover treatments. The abundance of naturally occurring beetles in the three cover treatments followed the general patterns of the number of marked immigrants over all releases. Marked beetles released inside the potato field tended to move along the release row rather than across rows; this pattern was stronger for the tilled treatment than for the two mulch cover treatments. Marked beetles disappeared from within the potato fields differently, depending on the cover crop treatment, but the patterns were not consistent over the season. Incorporation of dispersal patterns into pest management strategies should improve methods of pest population regulation, especially for the initial colonization of fields.

Behavioral and Electrophysiological Responses of Listronotus maculicollis (Coleoptera: Curculionidae) to Volatiles from Intact and Mechanically Damaged Annual Bluegrass

ABSTRACT Listronotus maculicollis Kirby is a highly destructive pest of low mown, cool-season turfgrasses in the northeastern United States and Canada. Behavioral and electrophysiological assays were conducted to identify compounds that may be useful in developing novel monitoring techniques. In Y-tube assays, males and females responded differently to volatiles from intact and clipped annual bluegrass (Poa annua L.). Females were significantly attracted to intact P. annua but repelled from clippings; males did not respond significantly to either treatment. Electroantennogram (EAG) recordings from both sexes showed a significant response to volatiles from both treatments. Gas chromatography mass spectrometry (GC-MS) identified 12 volatile compounds from P. annua of which nine were common to both intact plants and clippings. On average, seven-fold higher quantities of volatiles were collected from clippings than from intact plants (24.3 versus 3.4 ng/g of tissue/h). Eight compounds were released in significantly greater quantities from clippings of which 50% were the n-C6 compounds hexanal, (E)-2-hexenal, and (Z)-3-hexenyl acetate, commonly referred to as “green leaf volatiles” (GLVs). Only octanal was emitted in greater amounts from intact plants than clippings. These nine compounds were tested individually against male and female antennae. Both sexes displayed greatest sensitivity to nonanal, octanal, and (E)-2-hexenal, but a significant doseresponse relationship was observed with all compounds tested. These studies indicate that both sexes respond physiologically and that L. maculicollis females exhibit behavioral responses to host-plant volatiles. Future studies will need to assess the effects of individual compounds and component mixtures on L. maculicollis behavior in the field.