The Scent of Individual Foraging Bees.

Honey bees (Apis mellifera) forage by using their sense of smell and returning to floral odours that they have previously learned to associate with high-quality food rewards. Foraging bees communicate with other bees in the hive about food sources by exchanging chemical and locational information. It is well established that bees transfer non-volatile information regarding taste and quality of nectar via trophallaxis and communicate location information via directional dances. But to our knowledge, volatiles carried by returning forager bees on their bodies has not been explored as another source of chemical information. We investigated the cuticular-adsorbed odours of bees when foraging on three different crops and compared their odours with the crops' flower headspace. We found that cuticular extracts were in majority correlated with the flower headspace where bees were foraging, specific to the crop and field. Our results support the hypothesis that the scent of returning forager bees can be communicated to hivemates and is associated with information about current floral resources. Some of the floral volatiles that we identified in bee extracts had been previously found to be key compounds learned from the crop, thus supporting a mechanism for the selection of decisive compounds.

Electrophysiological and Behavioral Responses of Queensland Fruit Fly Females to Fruit Odors.

Females of the Queensland fruit fly (QFF), Bactrocera tryoni, are amongst the most damaging pests of horticulture in Australia and neighboring countries. Females can lay eggs into more than a hundred species of fruits and vegetables, resulting in large crop losses. Sexually mature males can be managed sustainably with traps baited with long-lasting synthetic lures, and sexually immature males and females can be attracted and killed by short-lived protein baits applied directly on surfaces, with a low success rate (< 20%). No long-lasting attractants for virgin or mated females exist. With the aim of developing a female attractant for surveillance, we collected and analyzed the odors of four ripe host fruits: orange, cherry guava, banana and feijoa. Virgin and mated female QFF were tested with gas-chromatography coupled with electro-antennographic detection to identify electrophysiologically (EAD)-active compounds. We detected 41 EAD-active compounds, with seven found common for more than one fruit. Overall, mated females responded more often and with higher intensity than virgin females. In particular, five compounds present either in cherry guava or feijoa triggered a significantly higher EAD response from mated females than from virgins. Twenty-six EAD-active compounds were selected and tested individually in a Y-tube olfactometer to measure attraction of both virgin and mated females. Behavioral responses differed significantly amongst the compounds, but not strongly between virgin and mated females. We did not find any correlation between electrophysiological and behavioral responses. Further field testing with behaviorally-active compounds is needed for the development of a new QFF female lure.

Past, Present, and Future of Integrated Control of Apple Pests: The New Zealand Experience.

This review describes the New Zealand apple industry's progression from 1960s integrated pest control research to today's comprehensive integrated pest management system. With the exception of integrated mite control implemented during the 1980s, pest control on apple crops was dominated by intensive organophosphate insecticide regimes to control tortricid leafrollers. Multiple pest resistances to these insecticides by the 1990s, and increasing consumer demand for lower pesticide residues on fruit, led to the implementation of integrated fruit production. This substantially eliminated organophosphate insecticide use by 2001, replacing it with pest monitoring systems, threshold-based selective insecticides, and biological control. More recently, new demands for ultralow-residue fruit have increased the adoption of mating disruption and use of biological insecticides. Widespread adoption of selective pest management has substantially reduced the status of previously important pests, including leafrollers, mealybugs, leafhoppers, and mites for improved phytosanitary performance, and contributed to major reductions in total insecticide use.

Regulatory Innovation, Mating Disruption and 4-Play(TM) in New Zealand.

Straight-chained lepidopteran pheromones are now regulated under a group standard in New Zealand, which is generic for moth pheromone products of similar low risk, under the Hazardous Substances and New Organisms Act (1996). This means that compliant new pheromone products can be developed and commercialized with low regulatory requirements. This encourages innovation and supports fruit industries interested in meeting export phytosanitary standards, while targeting low or nil residues of pesticides. Changes to pheromone blends for reasons such as technical improvements or variations in pest species composition in different crops can be made with minimal regulatory involvement. We illustrate how this system now operates with a four species mating disruption product commercialized in 2012. The odors involved in "4-Play™" consist of a range of components used by codling moth (Cydia pomonella), lightbrown apple moth (Epiphyas postvittana), green-headed leafroller (Planotortrix octo), and brown-headed leafroller (Ctenopseustis obliquana). The development of 4-Play™ illustrates how mating disruption of insects can support industry goals.

Feasibility of Mating Disruption for Agricultural Pest Eradication in an Urban Environment: Light Brown Apple Moth (Lepidoptera: Tortricidae) in Perth.

Eradication technologies are needed for urban and suburban situations, but may require different technologies from pest management in agriculture. We investigated mating disruption of a model moth species recently targeted for eradication in Californian cities, by applying dollops of SPLAT releasing a two-component sex pheromone of the light brown apple moth in 2-ha plots in low-density residential Perth, Australia. The pheromone technology was applied manually at ∼1.5 m height to street and garden trees, scrubs, and walls at 500 dollops per hectare of 0.8 g containing ∼80 mg active two-component pheromone. Catches of male moths were similar among all plots before treatment, but in treated areas (six replicates) pheromone trap catches were substantially reduced for up to 29 wk posttreatment, compared with untreated control plot catches (three replicates). The treatment with pheromone reduced catch to virgin females by 86% (P < 0.001) and reduced the occurrence of mating by 93%, compared with three equivalent untreated control plot catches (P < 0.001). Eradication programs are following an upward trend with globalization and the spread of invasive arthropods, which are often first detected in urban areas. Eradication requires a major increase in the communication distance between individuals, but this can be achieved using sex pheromone-based mating disruption technology, which is very benign and suitable for sensitive environments. The need for new socially acceptable tools for eradication in urban environments is likely to increase because of increasing need for eradications.

Combining Irradiation and Biological Control against Brown Marmorated Stink Bug: Are Sterile Eggs a Suitable Substrate for the Egg Parasitoid Trissolcus japonicus?

The brown marmorated stink bug (BMSB), Halyomorpha halys, is a phytophagous invasive pest native to south-eastern Asia, and it is now distributed worldwide. This species is considered to be one of the most damaging insect pests in North America and in Europe. In agriculture, the predominant approach to managing BMSB is based on the use of insecticides, specifically pyrethroids and neonicotinoids. Unfortunately, the biology of the species and its facility to develop mechanisms of resistance to available pesticides has induced farmers and scientists to develop different, least-toxic, and more effective strategies of control. In a territorial area-wide approach, the use of a classical biological control program in combination with other least-toxic strategies has been given prominent consideration. Following exploratory surveys in the native range, attention has focused on Trissolcus japonicus, a small scelionid egg parasitoid wasp that is able to oviposit and complete its larval development in a single egg of H. halys. A common method for detecting egg parasitoids in the native range involves the placement of so-called 'sentinel' egg masses of the pest in the environment for a short period, which are then returned to the laboratory to determine if any of them are parasitized. Outside of the area of origin, the use of fertile sentinel eggs of the alien species may lead to the further release of the pest species; an alternative is to use sterile sentinel eggs to record the presence of new indigenous egg parasitoids or to detect the dispersal of alien species (in this case, T. japonicus) released in a new environment to control the target insect pest species. This study evaluated the performance of three types of sterile sentinel eggs as a suitable substrate for the oviposition and larval development of the egg parasitoid T. japonicus in a context of combining classical biological control with a Sterile Insect Technique (SIT) approach.

Effects of Irradiation on Biology and Mating Behaviour of Wild Males of Brown Marmorated Stink Bug Using a 6 MV Medical Linear Accelerator.

The brown marmorated stink bug, Halyomorpha halys, is a pentatomid bug of Eastern Asian origin that became an economically relevant pest in the Eurasian and American continents. Management of this species is limited to use of chemical insecticides: an inefficient method due to the strong adaptability of the target pest. The sterile insect technique (SIT) is potentially a valid tactic in the search for nontoxic alternatives. In this work, we investigated the suitability of mass-trapped overwintering males, collected during the aggregation phase before the winter diapause, for their release as competitive sterile males in an SIT programme. Differently from previous studies, irradiation was applied with a linear accelerator device that produced high-energy photons. Following a similar scientific protocol with newly emerged irradiated males, the effects of X-ray irradiation on physiological parameters (longevity, fecundity and fertility) were assessed. In addition, behavioural bioassays were carried out in no-choice conditions to evaluate if irradiation interferes with mating processes. The results are very encouraging; the effects of the irradiation at 32 Gy did not differ from the controls in the longevity or fecundity of the exposed overwintering adults. The hatching rate of the eggs laid by the fertile females that had mated with the irradiated males was less than 5%. The results of behavioural bioassays showed that the irradiation did not cause a significant impact on the quality of the sterile males. More research is warranted to evaluate the mating competitiveness of sterile males in semi-field and field conditions.

Combining tactics to exploit Allee effects for eradication of alien insect populations.

Invasive species increasingly threaten ecosystems, food production, and human welfare worldwide. Hundreds of eradication programs have targeted a wide range of nonnative insect species to mitigate the economic and ecological impacts of biological invasions. Many such programs used multiple tactics to achieve this goal, but interactions between tactics have received little formal consideration, specifically as they interact with Allee dynamics. If a population can be driven below an Allee threshold, extinction becomes more probable because of factors such as the failure to find mates, satiate natural enemies, or successfully exploit food resources, as well as demographic and environmental stochasticity. A key implication of an Allee threshold is that the population can be eradicated without the need and expense of killing the last individuals. Some combinations of control tactics could interact with Allee dynamics to increase the probability of successful eradication. Combinations of tactics can be considered to have synergistic (greater efficiency in achieving extinction from the combination), additive (no improvement over single tactics alone), or antagonistic (reduced efficiency from the combination) effects on Allee dynamics. We highlight examples of combinations of tactics likely to act synergistically, additively, or antagonistically on pest populations. By exploiting the interacting effects of multiple tactics on Allee dynamics, the success and cost-effectiveness of eradication programs can be enhanced.

Argentine ant trail pheromone disruption is mediated by trail concentration.

Argentine ant trail pheromone disruption, using continuous release of the trail pheromone compound (Z)-9-hexadecanal, reduces the incidence of trails and foraging rates of field populations. However, little is known about the concentrations of pheromone required for successful disruption. We hypothesized that higher pheromone quantities would be necessary to disrupt larger ant populations. To test this, we laid a 30-cm long base trail of (Z)-9-hexadecanal on a glass surface at low and high rates (1 and 100 pg/cm) (Trail 1), and laid a second, shorter trail (Trail 2, 10 cm long, located 1.5 cm upwind) near the middle of Trail 1 at six rates (1, 10, 100, 1,000, 10,000, and 100,000 pg/cm). We then recorded and digitized movements of individual ants following Trail 1, and derived a regression statistic, r (2), as an index of trail integrity, and also recorded arrival success at the other end of the trail (30 cm) near a food supply. Disruption of trails required 100 fold more pheromone upwind, independent of base-trail concentration. This implies that in the field, trail disruption is likely to be less successful against high ant-trail densities (greater concentration of trail pheromone), and more successful against newly formed or weak trails, as could be expected along invasion fronts.

Modeling the sterile insect technique for suppression of light brown apple moth (Lepidoptera: Tortricidae).

A population model was derived for light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), subject to the sterile insect technique (SIT). The model was parameterized from the literature and from recent laboratory studies conducted in New Zealand and Australia. Relationships were fitted for several model parameters that vary with irradiation dose, allowing the model to simulate effectively complete sterility at 300 Gy through inherited sterility occurring from lower doses. At 300 Gy, the model suggests that eventual population extinction is 95% probable when the ratio of released to wild males in monitoring traps exceeds 6.4. Higher overflooding rates would be required to achieve eradication more rapidly. The optimal release interval, in terms of minimizing the required rate of production of factory moths, is approximately weekly. There is little advantage in releasing males only compared with releasing both sexes. Female-only releases are unlikely to be a useful tool for inherited sterility eradication because there is no reduction in the fertility of F1 offspring. The critical release rate required to halt population increase declines with decreasing irradiation dose, but at doses of < 171 Gy there is a risk that irradiated-lineage moths may form a self-sustaining population, making eradication by SIT alone impossible. The model suggests that a dose of around 200 Gy may be optimal because the resulting inherited sterility would reduce by a third the number of factory moths required compared with 300 Gy.

Irradiation-induced sterility in an egg parasitoid and possible implications for the use of biological control in insect eradication.

Classical biological control is a pest control tool involving the release of imported natural enemies. The Sterile Insect Technique (SIT) comprises releasing sexually sterile insects of a pest into the wild population for suppression or eradication. Both these approaches are environmentally friendly and their combination can result in a synergistic impact on pest populations and improve eradication. However, stringent regulation surrounding the introduction of biological control agents limits their use in eradication owing to the perceived risk of effects on non-target organisms. We investigated the irradiation biology of the egg parasitoid Trissolcus basalis to ascertain whether sterile parasitoids could mitigate the risk of potential sustained non-target impacts. Mated female T. basalis were gamma-irradiated at doses between 120 and 150 Gy and exposed to egg masses of their host Nezara viridula throughout their lifespans. This resulted in host mortality, despite a substantial reduction in developing parasitoid offspring, which followed a negative dose-response. There was no emergence of parasitoid offspring at 140 Gy and above. Irradiation did not affect oviposition behaviour but caused an increase in longevity. Consequently, sterile parasitoids could possibly alleviate concerns regarding the irreversibility of biological control release, which promotes further investigation of their potential role in eradication.

Invasive potential of tropical fruit flies in temperate regions under climate change.

Tropical fruit flies are considered among the most economically important invasive species detected in temperate areas of the United States and the European Union. Detections often trigger quarantine and eradication programs that are conducted without a holistic understanding of the threat posed. Weather-driven physiologically-based demographic models are used to estimate the geographic range, relative abundance, and threat posed by four tropical tephritid fruit flies (Mediterranean fruit fly, melon fly, oriental fruit fly, and Mexican fruit fly) in North and Central America, and the European-Mediterranean region under extant and climate change weather (RCP8.5 and A1B scenarios). Most temperate areas under tropical fruit fly propagule pressure have not been suitable for establishment, but suitability is predicted to increase in some areas with climate change. To meet this ongoing challenge, investments are needed to collect sound biological data to develop mechanistic models to predict the geographic range and relative abundance of these and other invasive species, and to put eradication policies on a scientific basis.

Operational Parameters for the Aerial Release of Sterile Codling Moths Using an Uncrewed Aircraft System.

The codling moth is a serious pest of apples in most regions of the world where this fruit is produced. The sterile insect technique is one strategy used to control this pest and is employed as part of an area-wide integrated pest management program for the codling moth in British Columbia, Canada. Modified fixed wing aircraft are the most common method for the release of sterile insects in large area-wide pest management programs. However, aerial release with a full-size aircraft can be prohibitively expensive. We evaluated the use of small, uncrewed aircraft systems (UASs) for the release of sterile codling moths. Sterile codling moths released from greater altitudes were more broadly distributed and drifted more in strong winds, compared to those released from lower altitudes. Most of the released insects were recaptured in a 50 m wide swath under the release route. Recapture rates for aerially released insects were 40-70% higher compared to those released from the ground. UASs provide a promising alternative to ground release and conventional aircraft for the release of sterile codling moths.

Trail pheromone disruption of Argentine ant trail formation and foraging.

Trail pheromone disruption of invasive ants is a novel tactic that builds on the development of pheromone-based pest management in other insects. Argentine ant trail pheromone, (Z)-9-hexadecenal, was formulated as a micro-encapsulated sprayable particle and applied against Argentine ant populations in 400 m2 field plots in Hawai'i Volcanoes National Park. A widely dispersed point source strategy for trail pheromone disruption was used. Traffic rates of ants in bioassays of treated filter paper, protected from rainfall and sunlight, indicated the presence of behaviorally significant quantities of pheromone being released from the formulation for up to 59 days. The proportion of plots, under trade wind conditions (2­3 m s−1), with visible trails was reduced for up to 14 days following treatment, and the number of foraging ants at randomly placed tuna-bait cards was similarly reduced. The success of these trail pheromone disruption trials in a natural ecosystem highlights the potential of this method for control of invasive ant species in this and other environments.

Egg Sterilisation of Irradiated Nezara viridula (Hemiptera: Pentatomidae).

Nezara viridula Linnaeus (Hemiptera: Pentatomidae) is a polyphagous pest of a wide range of economically important crops. Because the control of this species and other pentatomids relies primarily on insecticide application, investigation into the Sterile Insect Technique (SIT) is warranted. We aimed to investigate the irradiation biology of N. viridula for the potential application of SIT against this pest. Male and female N. viridula were gamma-irradiated at doses between 4 and 28 Gy and mated with both irradiated and nonirradiated conspecifics. Sterility of the resulting eggs followed a dose-response in each case. Irradiated males crossed with untreated females showed higher F1 egg sterility than crosses where the female was irradiated. The greatest F1 egg sterility was observed when both parents were irradiated. There was no obvious dose-response for the longevity of irradiated males, and for the fecundity of nonirradiated females mated with irradiated males. The fecundity of irradiated females appeared to decrease with irradiation dose. These results can be applied to a potential future application of SIT against N. viridula, but predominantly supports the ongoing development of SIT for Halyomorpha halys Stål (Hemiptera: Pentatomidae) and hemipteran pests in general.

Can Vibrational Playbacks Disrupt Mating or Influence Other Relevant Behaviours in Bactericera cockerelli (Triozidae: Hemiptera)?

Behaviours of insects can be manipulated by transmitting vibrational signals to host plants in order to develop pest management techniques. Bactericera cockerelli is an important pest and uses vibrations for mate-finding. In order to design a future control strategy for B. cockerelli, three different bioassays were performed to assess whether vibrational signals could affect relevant behaviours. Single males or pairs were treated with a female playback in test 1 and 2, respectively. In test 3, mixed sex groups received either different disturbance playbacks. The use of a female playback significantly reduced the mating success of males, since they were attracted towards the source of the stimulus. Moreover, test 2 revealed that B. cockerelli females are competitive, since they used their signals to cover the playback and to duet with males, while in test 3, the disturbance playback, consisting of broadband noises significantly reduced male signalling activity. However, none of the treatments of test 3 negatively affected the mating success of males, which tended to mount the other conspecifics present on the same leaf. The role of vibrations in sexual communication and their potential application as control technique for B. cockerelli are discussed as well.

Odorant-Based Detection and Discrimination of Two Economic Pests in Export Apples.

Detection of pest infestations in fresh produce traded internationally could offer improved prospects for reducing the movement of unwanted pests. Because immature stages of some pests can be difficult to find visually, other cues such as herbivore-induced volatiles that can potentially be detected at the early stages of infestation are worth investigating. In this study, we artificially infested postharvested apples (Malus × domestica 'Royal Gala') with two economic apple pests, the specialist codling moth (CM, Cydia pomonella Linnaeus, Lepidoptera: Tortricidae) and the generalist Queensland fruit fly (QFF, Bactrocera tryoni, Froggatt, Diptera: Tephritidae) and collected volatile organic compounds (VOCs) over time (days 0, 6, and 14-15). In both infestation experiments, we found a strong and significant interaction between time and treatment. Apples infested with the QFF emitted lower total amounts of VOCs than uninfested apples, whereas apples infested with the CM released similar total amounts of VOCs. Apples infested with CM had increases in several hexyl and butyl esters, which were particularly noticeable after 15 d. In contrast, changes in ethyl esters were characteristics of QFF infestation and could be detected from day 6. Our multilevel and multivariate statistical analysis identified specific volatile biomarkers for each species at each sampling time that can be used to design a new tool for remote detection and surveillance of these invasive pests in harvested apples. Nevertheless, other information such as the cultivar as well as the storage condition needs to be taken into consideration to increase accuracy of future odorant-based sensors for pest identification.

Kairomone and Camera Trapping New Zealand Flower Thrips, Thrips obscuratus.

This project investigated how kairomone lures, camera traps, and counting software could together contribute to pest management. Images of cumulative daily catch of New Zealand Flower Thrips (NZFT) attracted to a ripe peach lactone (6-pentyl-2H-pyran-2-one; 6-PAP) were automatically loaded to the internet and compared with scanned bases checked weekly using in-house software and manual counting. Camera traps were able to provide thrips counts equivalent to delta traps, but daily and remotely. An 11-fold greater NZFT count occurred within 24 h in passive traps after polyethylene sachets loaded with 250 mg of 6-PAP were placed in trees. Intensive trapping, by placing 1, 2, 4, and 8 traps per tree (500 mg/trap), resulted in a maximum 32-fold increase in thrips per tree. While 6-PAP has proved to be a useful tool for monitoring NZFT numbers, our results suggest that it is not likely to be suitable for mass trapping. Future research should investigate NZFT behavior to better understand population movement on an area-wide basis. Camera traps can be a valuable tool for recording insect flight activity remotely, but the number of traps required for statistically reliable estimates may be prohibitive.

Combined Effects of Mating Disruption, Insecticides, and the Sterile Insect Technique on Cydia pomonella in New Zealand.

Codling moth was introduced into New Zealand, and remains a critical pest for the apple industry. Apples exported to some markets require strict phytosanitary measures to eliminate the risk of larval infestation. Mating disruption and insecticide applications are the principal means of suppression in New Zealand. We tested the potential for the sterile insect technique (SIT) to supplement these measures to achieve local eradication or suppression of this pest. SIT was trialed in an isolated group of six integrated fruit production (IFP) orchards and one organic orchard (total 391 ha), using sterilized insects imported from Canada, with release by unmanned aerial vehicle and from the ground. Eradication was not achieved across the region, but a very high level of codling moth suppression was achieved at individual orchards after the introduction of sterile moths in combination with mating disruption and larvicides. After six years of releases, catches of wild codling moths at three IFP orchards (224 ha) were 90-99% lower than in 2013-2014, the year before releases began. Catches at three other IFP orchards (129 ha) decreased by 67-97% from the year before releases began (2015-2016), from lower initial levels. At a certified organic orchard with a higher initial population under only organic larvicides and mating disruption, by 2019-2020, there was an 81% reduction in wild moths capture from 2016-2017, the year before releases began.

Will Peri-Urban Cydia pomonella (Lepidoptera: Tortricidae) Challenge Local Eradication?

Codling moth, Cydia pomonella (Lepidoptera: Tortricidae), is a phytosanitary pest of New Zealand's export apples. The sterile insect technique supplements other controls in an eradication attempt at an isolated group of orchards in Hawke's Bay, New Zealand. There has been no attempt in New Zealand to characterize potential sources of uncontrolled peri-urban populations, which we predicted to be larger than in managed orchards. We installed 200 pheromone traps across Hastings city, which averaged 0.32 moths/trap/week. We also mapped host trees around the pilot eradication orchards and installed 28 traps in rural Ongaonga, which averaged 0.59 moths/trap/week. In Hastings, traps in host trees caught significantly more males than traps in non-host trees, and spatial interpolation showed evidence of spatial clustering. Traps in orchards operating the most stringent codling moth management averaged half the catch rate of Hastings peri-urban traps. Orchards with less rigorous moth control had a 5-fold higher trap catch rate. We conclude that peri-urban populations are significant and ubiquitous, and that special measures to reduce pest prevalence are needed to achieve area-wide suppression and reduce the risk of immigration into export orchards. Because the location of all host trees in Hastings is not known, it could be more cost-effectively assumed that hosts are ubiquitous across the city and the area treated accordingly.