Peter Witzgall

Sex pheromones and their impact on pest management.

The idea of using species-specific behavior-modifying chemicals for the management of noxious insects in agriculture, horticulture, forestry, stored products, and for insect vectors of diseases has been a driving ambition through five decades of pheromone research. Hundreds of pheromones and other semiochemicals have been discovered that are used to monitor the presence and abundance of insects and to protect plants and animals against insects. The estimated annual production of lures for monitoring and mass trapping is on the order of tens of millions, covering at least 10 million hectares. Insect populations are controlled by air permeation and attract-and-kill techniques on at least 1 million hectares. Here, we review the most important and widespread practical applications. Pheromones are increasingly efficient at low population densities, they do not adversely affect natural enemies, and they can, therefore, bring about a long-term reduction in insect populations that cannot be accomplished with conventional insecticides. A changing climate with higher growing season temperatures and altered rainfall patterns makes control of native and invasive insects an increasingly urgent challenge. Intensified insecticide use will not provide a solution, but pheromones and other semiochemicals instead can be implemented for sustainable area-wide management and will thus improve food security for a growing population. Given the scale of the challenges we face to mitigate the impacts of climate change, the time is right to intensify goal-oriented interdisciplinary research on semiochemicals, involving chemists, entomologists, and plant protection experts, in order to provide the urgently needed, and cost-effective technical solutions for sustainable insect management worldwide.

Host plant volatiles synergize response to sex pheromone in codling moth, Cydia pomonella

Plant volatile compounds synergize attraction of codling moth males Cydia pomonella to sex pheromone (E,E)-8,10-dodecadien-1-ol (codlemone). Several apple volatiles, known to elicit a strong antennal response, were tested in a wind tunnel. Two-component blends of 1 pg/min codlemone and 100 pg/min of either racemic linalool, (E)-β-farnesene, or (Z)-3-hexen-1-ol attracted significantly more males to the source than codlemone alone (60, 58, 56, and 37%, respectively). In comparison, a blend of codlemone and a known pheromone synergist, dodecanol, attracted 56% of the males tested. Blends of pheromone and plant volatiles in a 1:100 ratio attracted more males than 1:1 or 1:10,000 blends. Adding two or four of the most active plant compounds to codlemone did not enhance attraction over blends of codlemone plus single-plant compounds. Of the test compounds, only farnesol was attractive by itself; at a release rate of 10,000 pg/min, 16% of the males arrived at the source. However, attraction to a 1:10,000 blend of codlemone and farnesol (42%) was not significantly different from attraction to codlemone alone (37%). In contrast, a codlemone mimic, (E)-10-dodecadien-1-ol, which attracted 2% males by itself, had a strong antagonistic effect when blended in a 1:10,000 ratio with codlemone.

Attraction of codling moth males to apple volatiles

The attraction of the codling moth, Cydia pomonella, to apple volatile compounds known to elicit an antennal response was tested both in the field and in a wind tunnel. In the field, (E)‐β‐farnesene captured male moths. The addition of other apple volatiles, including (E,E)‐α‐farnesene, linalool, or (E,E)‐farnesol to (E)‐β‐farnesene did not significantly augment trap catch. Few females were caught in traps which also caught male moths, but female captures were not significantly different from blank traps. In the wind tunnel, males were attracted to (E,E)‐farnesol, but not to (E)‐β‐farnesene. The addition of (E,E)‐α‐farnesene to (E)‐β‐farnesene had a synergistic effect on male attraction. The male behavioural sequence elicited by plant volatiles, including upwind flight behaviour, was indistinguishable from the behaviour elicited by sex pheromone.

Putative Chemosensory Receptors of the Codling Moth, Cydia pomonella, Identified by Antennal Transcriptome Analysis

The codling moth, Cydia pomonella, is an important fruit pest worldwide. As nocturnal animals, adults depend to a large extent on olfactory cues for detection of food and mates, and, for females, oviposition sites. In insects, odor detection is mediated by odorant receptors (ORs) and ionotropic receptors (IRs), which ensure the specificity of the olfactory sensory neuron responses. In this study, our aim was to identify chemosensory receptors in the codling moth as a means to uncover new targets for behavioral interference. Using next-generation sequencing techniques, we identified a total of 43 candidate ORs, one gustatory receptor and 15 IRs in the antennal transcriptome. Through Blast and sequence similarity analyses we annotated the insect obligatory co-receptor ORco, five genes clustering in a conserved clade containing sex pheromone receptors, one homolog of the Bombyx mori female-enriched receptor BmorOR30 (but no homologs of the other B. mori female-enriched receptors) and one gene clustering in the sugar receptor family. Among the candidate IRs, we identified homologs of the two highly conserved co-receptors IR8a and IR25a, and one homolog of an IR involved in phenylethyl amine detection in Drosophila. Our results open for functional characterization of the chemosensory receptors of C. pomonella, with potential for new or refined applications of semiochemicals for control of this pest insect.

Flying the Fly: Long-range Flight Behavior of Drosophila melanogaster to Attractive Odors

The fruit fly, Drosophila melanogaster Meigen (Diptera: Drosophilidae), is a model for how animals sense, discriminate, and respond to chemical signals. However, with D. melanogaster our knowledge of the behavioral activity of olfactory receptor ligands has relied largely on close-range attraction, rather than on long-range orientation behavior. We developed a flight assay to relate chemosensory perception to behavior. Headspace volatiles from vinegar attracted 62% of assayed flies during a 15-min experimental period. Flies responded irrespective of age, sex, and mating state, provided they had been starved. To identify behaviorally relevant chemicals from vinegar, we compared the responses to vinegar and synthetic chemicals. Stimuli were applied by a piezoelectric sprayer at known and constant release rates. Re-vaporized methanol extracts of Super Q-trapped vinegar volatiles attracted as many flies as vinegar. The main volatile component of vinegar, acetic acid, elicited significant attraction as a single compound. Two other vinegar volatiles, 2-phenyl ethanol and acetoin, produced a synergistic effect when added to acetic acid. Geosmin, a microbiological off-flavor, diminished attraction to vinegar. This wind tunnel assay based on a conspicuous and unambiguous behavioral response provides the necessary resolution for the investigation of physiologically and ecologically relevant odors and will become an essential tool for the functional analysis of the D. melanogaster olfactory system.

Floral to green: mating switches moth olfactory coding and preference

Mating induces profound physiological changes in a wide range of insects, leading to behavioural adjustments to match the internal state of the animal. Here, we show for the first time, to our knowledge, that a noctuid moth switches its olfactory response from food to egg-laying cues following mating. Unmated females of the cotton leafworm (Spodoptera littoralis) are strongly attracted to lilac flowers (Syringa vulgaris). After mating, attraction to floral odour is abolished and the females fly instead to green-leaf odour of the larval host plant cotton, Gossypium hirsutum. This behavioural switch is owing to a marked change in the olfactory representation of floral and green odours in the primary olfactory centre, the antennal lobe (AL). Calcium imaging, using authentic and synthetic odours, shows that the ensemble of AL glomeruli dedicated to either lilac or cotton odour is selectively up- and downregulated in response to mating. A clear-cut behavioural modulation as a function of mating is a useful substrate for studies of the neural mechanisms underlying behavioural decisions. Modulation of odour-driven behaviour through concerted regulation of odour maps contributes to our understanding of state-dependent choice and host shifts in insect herbivores.

ANTENNAL AND BEHAVIORAL RESPONSES OF GRAPEVINE MOTH Lobesia botrana FEMALES TO VOLATILES FROM GRAPEVINE

Grapevine moth Lobesia botrana is the economically most important insect of grapevine Vitis vinifera in Europe. Flower buds, flowers, and green berries of Chardonnay grapevine are known to attract L. botrana for oviposition. The volatile compounds collected from these phenological stages were studied by gas chromatography—mass spectrometry, and the antennal response of L. botrana females to these headspace collections was recorded by gas chromatography—electroantennography. The compounds found in all phenological stages, which consistently elicited a strong antennal response, were pentadecane, nonanal, and α -farnesene. In a wind tunnel, gravid L. botrana females flew upwind to green grapes, as well as to headspace collections from these berries released by a piezoelectric sprayer release device. However, no females landed at the source of headspace volatiles, possibly due to inappropriate concentrations or biased ratios of compounds in the headspace extracts.

Antennal and behavioural response of codling moth Cydia pomonella to plant volatiles

Identification of host volatile compounds attractive to codling moth Cydia pomonella, a most important insect of apple, will contribute to the development of safe control techniques. Synthetic apple volatiles in two doses were tested for antennal and behavioural activity in codling moth. Female antennae strongly responded to (Z)3‐hexenol, (Z)3‐hexenyl benzoate, (Z)3‐hexenyl hexanoate, (±)‐linalool and E,E‐α‐farnesene. Two other compounds eliciting a strong antennal response were the pear ester, ethyl (E,Z)‐2,4‐decadienoate, and its corresponding aldehyde, E,E‐2,4‐decadienal, which is a component of the larval defence secretion of the European apple sawfly. Attraction of codling moth to compounds eliciting a strong antennal response was tested in a wind tunnel. Male moths were best attracted to a blend of (E,E)‐α‐farnesene, (E)‐beta‐farnesene and ethyl (E,Z)‐2,4‐decadienoate. The aldehyde E,E‐2,4‐decadienal had an antagonistic effect when added to the above mixture.

Chemical Ecology and Management of Lobesia botrana (Lepidoptera: Tortricidae)

ABSTRACT The moth Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae) feeds on grapes (Vitis vinifera L.), reducing yield and increasing susceptibility to fungal infections. L. botrana is among the most economically important insects in Europe and has recently been found in vineyards in Chile, Argentina, and California. Here, we review L. botrana biology and behavior in relation to its larval host (the grapevine) and its natural enemies. We also discuss current and future control strategies in light of our knowledge of chemical ecology, with an emphasis on the use of the sex pheromone-based strategies as an environmentally safe management approach. Pheromone-mediated mating disruption is the most promising technique available on grapes and is currently implemented on ≈140,000 ha in Europe. Experience from several growing areas confirms the importance of collaboration between research, extension, growers, and pheromone-supply companies for the successful implementation of the mating disruption technique. In the vineyards where mating disruption has been successfully applied as an areawide strategy, the reduction in insecticide use has improved the quality of life for growers, consumers, as well as the public living near wine-growing areas and has thereby reduced the conflict between agricultural and urban communities.

Plant volatiles mediate attraction to host and non-host plant in apple fruit moth, Argyresthia conjugella

Plant volatiles mediate host finding in insect herbivores and lead to host fidelity and habitat‐specific mating, generating premating reproductive isolation and facilitating sympatric divergence. The apple fruit moth, Argyresthia conjugella Zeller (Lepidoptera: Argyresthiidae), is a particularly suitable species to study the cues and behavioural mechanisms leading to colonization of a new host: it recurrently oviposits on the non‐host plant, apple Malus domestica Borkh. (Rosaceae), where the larvae cannot complete their development. The larval host of the apple fruit moth (Lepidoptera, Argyresthiidae), is rowan Sorbus aucuparia L. (Rosaceae). Fruit setting in rowan, however, fluctuates strongly over large areas in Scandinavia. Every 2–4 years, when too few rowanberries are available for egg laying in forests, apple fruit moth females oviposit instead on apple in nearby orchards, but not on other fruits, such as pear or plum. This poses the question of which cues mediate attraction to rowan and apple, and how apple fruit moth discriminates rowan from apple. Chemical analysis and antennal recordings showed that 11 out of 15 rowan volatiles eliciting an antennal response in A. conjugella females co‐occur in rowan and apple headspace, in a different proportion. In the field, A. conjugella was attracted to several of these plant volatiles, especially to 2‐phenyl ethanol, methyl salicylate, and decanal. Addition of anethole to 2‐phenyl ethanol had a strong synergistic effect, the 1 : 1 blend is a powerful attractant for A. conjugella males and females. These results confirm that volatiles common to both plants may account for a host switch in A. conjugella from rowan to apple. Some of the most attractive compounds, including 2‐phenyl ethanol, anethole, and decanal, which have been found in several apple cultivars, were not present in the headspace of the apple cultivar, Aroma, which is also susceptible to attack by A. conjugella. This supports the idea that the odour signal from apple is suboptimal for attraction of A. conjugella, but is nonetheless sufficient for attraction, during times when rowan is not available for egg laying.