Odor receptor responses of male gypsy and nun moths (Lepidoptera,Lymantriidae) to disparlure and its analogues

Summary The closely related species of the gypsy and the nun moth (Lymantria (Porthetria) dispar andL. monacha) were investigated with respect to their electrophysiological (electro-antennogram and single cell) responses to the sex pheromone (disparlure:cis-7,8-epoxy-2-methyl-octadecane) and 56 structurally related epoxides and the disparlure-precursor olefin. Within the limitations of reproducibility of the measurements the sequence of the effectiveness of all the tested compounds is nearly identical in both species, disparlure being every time the most effective compound. From this is deduced a high similarity in the receptor systems for female pheromones of the two moth species.     

Pheromone‐trapping the nun moth,Lymantria monacha (Lepidoptera: Lymantriidae) in Inner Mongolia,China

The nun moth, Lymantria monacha L., is one of the most important defoliators of Eurasian coniferous forests. Outbreaks during 2011–2015 in the natural/planted larch, and larch‐birch mixed forests of the Greater Khingan Range in Inner Mongolia, China, caused tremendous timber losses from severe defoliation and tree mortality. A series of trapping experiments were conducted in these outbreak areas to evaluate the efficacy of a synthetic species‐specific pheromone lure based on the female pheromone blend of European nun moth populations. Our results clearly show that the nun moth in Inner Mongolia is highly and specifically attracted to this synthetic pheromone, with few gypsy moths (Lymantria dispar) captured. Flight activity monitoring of L. monacha male moths using pheromone‐baited Unitraps at 2 locations during the summer of 2015 indicated that the flight period started in mid‐July, peaking in early August at both locations. Based on male moth captures, there was a strong diurnal rhythm of flight activity throughout the entire scotophase, peaking between 22:00 and 24:00. Unitraps and wing traps had significantly and surprisingly higher catches than the gypsy moth traps. Unitraps fastened to tree trunks 2 m above ground caught significantly more male moths than those at the ground level or at 5 m height. Male L. monacha moths can be attracted to pheromone‐baited traps in open areas 150–200 m distant from the infested forest edge. Our data should allow improvement on the performance of pheromone‐baited traps for monitoring or mass‐trapping to combat outbreaks of this pest in northeastern China.     

Discrimination and production of disparlure enantiomers by the gypsy moth and the nun moth

ABSTRACT. Two odour receptor cells were physiologically identified within male antennal hair sensillae of the gypsy moth, Lymantria dispar L, and the nun moth, L. monacha L. In the gypsy moth, one cell responded to (+)-disparlure, while a neighbouring cell responded to (-)-disparlure. In the nun moth both cells responded to (+)-disparlure. The lack of sensitivity to (-)-disparlure in the nun moth was corroborated by electroantennogram (EAG) recordings, which indicated no affinity to this enantiomer. Single cell responses of male gypsy moth to different concentrations of the synthetic enantiomers of disparlure were then compared to responses elicited by hexane extracts of female glands of both species. The gypsy moth's extracts stimulated almost exclusively the receptor cell specialized for (+)-disparlure, while both cells were simultaneously stimulated by the extracts of the nun moths. From the response characteristic of the cells it is estimated that pheromone production of the nun moth is about 10% (+) and 90% (-)-disparlure, and that of the gypsy moth is almost 100% (+)-disparlure. Stimulation of the antenna of each species by female gland extracts of both species did not indicate the presence of receptors for other hexane elutable pheromone components in either species.     

Spatial distribution of the gypsy moth [Lepidoptera: Lymantriidae] and some of its parasitoids within a forest environment

Aspects of the microhabitat distributions of the gypsy moth,Porthetria dispar (L.) (Lepidoptera: Lymantriidae), and some of its parasitoids were investigated in the field by means of sticky panels and gypsy moth egg masses exposed at different heights in trees, by egg masses exposed within forested and cleared areas, and by gypsy moth pupal collections from different heights in trees.Ooencyrtus kuwanai (Howard)(Hymenoptera: Encyrtidae), Apanteles melanoscelus Ratzeburg (Hymenoptera: Braconidae), and gypsy moths were caught most frequently on stickly panels placed in upper portions of trees. In contrast,Apanteles laeviceps Ashmead, a parasitoid of cutworms, was most often caught near the forest floor.O. kuwanai attacked equally egg masses exposed at different heights in trees, but parasitized those in a clearing less often than those within the forest prosper.Brachymeria intermedia (Nees) (Hymenoptera: Chalcididae) emerged mostly from pupae collected near the tops of trees and not at all from those collected below 5 m. The results are discussed as they relate to field sampling procedures, behavioral activities of gypsy moth and parasitoid adults, and integrated control possibilities for the gypsy moth.     

Effects of SPLAT® GM sprayable pheromone formulation on gypsy moth mating success

Several integrated pest management programs rely on the use of mating disruption tactics to control insect pests. Some programs specifically target non‐native species, such as the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae). We evaluated SPLAT^® GM, a new sprayable formulation of the gypsy moth sex pheromone disparlure, for its ability to disrupt gypsy moth mating. The study was conducted in 2006, 2007, and 2008 in forested areas in Virginia, USA. Mating success of gypsy moth females was reduced by >99% and male moth catches in pheromone‐baited traps by >90%, in plots treated with SPLAT^® GM at dosages ranging from 15 to 75 g of active ingredient (a.i.) ha^?1. Dosage‐response tests conducted in 2008 indicated that SPLAT^® GM applied at a dosage of 7.5 g a.i. ha^?1 was as effective as a 15 g a.i. ha^?1 dosage.     

Rapid identification of the Asian gypsy moth and its related species based on mitochondrial DNA

The gypsy moth—Lymantria dispar (Linnaeus)—is a worldwide forest defoliator and is of two types: the European gypsy moth and the Asian gypsy moth. Because of multiple invasions of the Asian gypsy moth, the North American Plant Protection Organization officially approved Regional Standards for Phytosanitary Measures No. 33. Accordingly, special quarantine measures have been implemented for 30 special focused ports in the epidemic areas of the Asian gypsy moth, including China, which has imposed great inconvenience on export trade. The Asian gypsy moth and its related species (i.e., Lymantria monocha and Lymantria xylina) intercepted at ports are usually at different life stages, making their identification difficult. Furthermore, Port quarantine requires speedy clearance. As such, it is difficult to identify the Asian gypsy moth and its related species only by their morphological characteristics in a speedy measure. Therefore, this study aimed to use molecular biology technology to rapidly identify the Asian gypsy moth and its related species based on the consistency of mitochondrial DNA in different life stages. We designed 10 pairs of specific primers from different fragments of the Asian gypsy moth and its related species, and their detection sensitivity met the need for rapid identification. In addition, we determined the optimal polymerase chain reaction amplification temperature of the 10 pairs of specific primers, including three pairs of specific primers for the Asian gypsy moth (L. dispar asiatic), four pairs of specific primers for the nun moth (L. monocha), and three pairs of specific primers for the casuarina moth (L. xylina). In conclusion, using our designed primers, direct rapid identification of the Asian gypsy moth and its related species is possible, and this advancement can help improve export trade in China.     

Optimization of pheromone dosage for gypsy moth mating disruption

The effect of aerial applications of the pheromone disparlure at varying dosages on mating disruption in low‐density gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae), populations was determined in field plots in Virginia, USA during 2000 and 2002. Six dosages [0.15, 0.75, 3, 15, 37.5, and 75 g active ingredient (AI)/ha] of disparlure were tested during the 2‐year study. A strongly positive dose–response relationship was observed between pheromone dosages and mating disruption, as measured by the reduction in male moth capture in pheromone‐baited traps and mating successes of females. Dosages of pheromone 15 g AI/ha (15, 37.5, and 75 g AI/ha) reduced the mating success of females by >99% and significantly reduced male moth catches in pheromone‐baited traps compared to untreated plots. Pheromone dosages <15 g AI/ha also reduced trap catch, but to a lesser extent than dosages 15 g AI/ha. Furthermore, the effectiveness of the lower dosage treatments (0.15, 0.75, and 3 g AI/ha) declined over time, so that by the end of the study, male moth catches in traps were significantly lower in plots treated with pheromone dosages 15 g AI/ha. The dosage of 75 g AI/ha was initially replaced by a dosage of 37.5 g AI/ha in the USDA Forest Service Slow‐the‐Spread (STS) of the Gypsy Moth management program, but the program is currently making the transition to a dosage of 15 g AI/ha. These changes in applied dosages have resulted in a reduction in the cost of gypsy moth mating disruption treatments.     

Comparative efficacy of two controlled-release gypsy moth mating disruption formulations

The effects of aerial applications of the gypsy moth sex pheromone, disparlure, on mating disruption and suppression of growth of populations of the gypsy moth, Lymantria dispar (L.), were investigated. Two formulations of disparlure, plastic laminate flakes applied in a single application and polymethacrylate beads applied in two applications, were compared in two separate tests conducted in 1993 and 1994. The beads were applied in two applications spaced 2 weeks apart because preliminary tests had indicated that they released pheromone too rapidly to maintain adequate emission rates throughout the period of male flight. In 1993, the flakes were applied at a rate of 50 g a.i./ha, and the beads were applied at a rate of 15 g a.i./ha for each application. In 1994, the flakes were applied at a rate of 75 g a.i./ha and the beads were applied at rates of 32.5 and 42.5 g a.i./ha for the two applications. Beads with larger average particle size were used in 1994 to prolong disparlure release. The treatments applied in 1993 resulted in >97% reduction in mating and >82% suppression of population growth in the following year. Because of a 1995 collapse of gypsy moth populations in the vicinity of the tests, reliable population growth data were not available for the treatments applied in 1994, but significant mating disruption did occur under both treatments. Based on measurements of residual disparlure after field aging, the flakes released 32 and 48% of their disparlure content during the 6 weeks of male moth flight in 1993 and 1994, respectively. The smaller beads used in 1993 released 75% of their disparlure content, and the larger beads used in 1994 released 52% of their disparlure content, during the 6 weeks of male flight. The biological efficacy data suggest that the bead and flake formulations, as applied in these tests, have similar effects on gypsy moth mating disruption and subsequent population growth. Based on the observed release rates from both 1993 and 1994, a single application of the beads would provide emission rates equal to or greater than those provided by the flakes when applied at an equal dose.     

Mechanical thinning to restore oak savanna promoted predator assemblages of gypsy moth pupae in Michigan

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Interpopulation quality in gypsy moths with implications for success of two pupal parasitoids: Brachymeria intermedia (Nees) and Coccygomimus turionellae (L.)*

Abstract.

• 1 Gypsy moth egg masses were collected from innocuous, release and outbreak populations and reared in the laboratory on synthetic diet under identical conditions.
• 2 Outbreak population gypsy moths hatched sooner, were smaller and less fecund than innocuous or release gypsy moths, but had a higher concentration of total carbohydrates in their haemolymph.
• 3 Pupae from each population source were submitted to parasitization by two pupal parasitoids. Emerging B.intermedia, an established parasitoid of the gypsy moth associated with outbreak populations, were largest on outbreak source gypsy moths. C. turionellae, not a usual parasitoid of the gypsy moth, were largest when emerging from innocuous or release population gypsy moths. Implications for population dynamics of the gypsy moth are discussed.

     

Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids

The gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis, overlap geographically as well as in their host ranges. Adult female swallowtails are incapable of distinguishing between damaged and undamaged leaves, and the opportunities for competition between these two species are numerous. We designed field and laboratory experiments to look for evidence of indirect competition between P. canadensis and L. dispar larvae. Swallowtail caterpillars were reared in the laboratory on leaves from gypsy-moth-defoliated and undefoliated trees to explore host-plant effects. We tested for pathogen-mediated interactions by rearing swallowtail larvae on both sterilized and unsterilized leaves from defoliated and undefoliated sources. In addition, we measured the effects of known gypsy moth pathogens, as well as gypsy moth body fluids, on the growth and survival of swallowtail larvae. Field experiments were designed to detect the presence of parasitoid-mediated competition, as well: we recorded parasitism of swallowtail caterpillars placed in the field either where there were no gypsy moth larvae present, or where we had artificially created dense gypsy moth populations. We found evidence that swallowtails were negatively affected by gypsy moths in several ways: defoliation by gypsy moths depressed swallowtail growth rate and survival, whether leaves were sterilized or not; sterilization significantly reduced the effect of defoliation, and gypsy moth body fluids proved lethal; and swallowtail caterpillars suffered significantly increased rates of parasitism when they were placed in the field near gypsy moth infestations.     

Lepidoptera‐specific insecticide used to suppress gypsy moth outbreaks may benefit non‐target forest Lepidoptera

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Effects of the 3M™ MEC Sprayable Pheromone® formulation on gypsy moth mating success

The study was conducted during 2000, 2001, 2003 and 2004 in forested areas in Virginia, USA to evaluate the 3M™ MEC-GM Sprayable Pheromone® formulation of the gypsy moth sex pheromone, disparlure, for its ability to disrupt mating in gypsy moth, Lymantria dispar (Lep.: Lymantriidae). Both mating success of gypsy moth females and male moth catches in pheromone-baited traps were significantly reduced in plots treated with the 3M™ MEC-GM formulation at dosages ranging from 15 to 75 g of active ingredient/ha. However, the 3M™ MEC-GM formulation reduced trap catch to a lesser extent than did the currently registered Hercon Disrupt® II plastic flakes used as a positive control and applied at similar or lower dosages. Furthermore, the effectiveness of the 3M™ sprayable formulation declined through time, so that by the end of the male flight season, male moth catches in traps were significantly higher than in plots treated with Hercon plastic flakes. Based on the reported results, 3M™ MEC-GM Sprayable Pheromone® formulation was never integrated into the operational treatment projects of USDA Forest Service Cooperative Slow-the-Spread of the Gypsy Moth management programme.     

Field evaluation of effect of temperature on release of disparlure from a pheromone-baited trapping system used to monitor gypsy moth (Lepidoptera: Lymantriidae)

Traps baited with disparlure, the synthetic form of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae), sex pheromone are used to detect newly founded populations and estimate population density across the United States. The lures used in trapping devices are exposed to field conditions with varying climates, which can affect the rate of disparlure release. We evaluated the release rate of disparlure from delta traps baited with disparlure string dispenser from 1 to 3 yr across a broad geographic gradient, from northern Minnesota to southern North Carolina. Traps were deployed over approximately 12 wk that coincided with the period of male moth flight and the deployment schedule of traps under gypsy moth management programs. We measured a uniform rate of release across all locations when considered over the accumulation of degree-days; however, due to differences in degree-day accumulation across locations, there were significant differences in release rates over time among locations. The initial lure load seemed to be sufficient regardless of climate, although rapid release of the pheromone in warmer climates could affect trap efficacy in late season. Daily rates of release in colder climates, such as Minnesota and northern Wisconsin, may not be optimal in detection efforts. This work highlights the importance of local temperatures when deploying pheromone-baited traps for monitoring a species across a large and climatically diverse landscape.     

Instrumental measurement of the gypsy moth pre-flight behavioural response to pheromone

ABSTRACT. Vibrations of the thorax and electrical activity (EMG) of gypsy moth flight muscles were recorded during wing fanning following pheromone stimulation. The percentage of positive responses and durations of bursts of flight muscle activity increased with the logarithm of pheromone dose, whereas latency decreased. The results correlated well with wing fanning responses of freely moving gypsy moths exposed to nearly identical stimulus conditions. Typical dose-response curves in the range of 0.04-400ng disparlure were obtained in both types of experiments. These methods provide an electrical analogue of wing fanning behaviour.     

Evaluation of preventive treatments in low-density gypsy moth populations using pheromone traps

Pheromone traps can be used for evaluating the success of treatments that are applied to either eradicate or delay the growth of isolated low-density populations of the gypsy moth, Lymantria dispar (L.). We developed an index of treatment success, T, that measures the reduction in moth counts in the block treated adjusted by the change in moth counts in the reference area around it. This index was used to analyze the effectiveness of treatments that were conducted as part of the USDA Forest Service Slow-the-Spread of the gypsy moth project from 1993 to 2001. Out of 556 treatments that were applied during this period, 266 (188,064 ha) were selected for the analysis based on several criteria. They included 173 blocks treated with Bacillus thuringiensis (Berliner) variety kurstaki and 93 blocks treated with racemic disparlure. Analysis using general linear models indicated that disparlure treatments were significantly more effective than B. thuringiensis treatments in reducing moth captures. The frequency of repeated treatments in the same area was higher after B. thuringiensis than after disparlure applications. Treatments were more successful if the pretreatment moth counts outside of the block treated were low compared with moth counts inside the block.     

Evidence for short-range sonic communication in lymantriine moths

Sexual communication of nun moth, Lymantria monacha (L.), pink gypsy moth, Lymantria mathura Moore, and fumida tussock moth, Lymantria fumida Butler (all Lepidoptera: Noctuidae: Lymantriinae), is known to be mediated by pheromones. We now show that males are attracted by the sounds of conspecific females over short distances and that wing fanning male and female L. monacha, L. mathura and L. fumida produce species- and sex-specific wing beat and associated click sounds that could contribute to reproductive isolation. Evidence for short-range communication in these lymantriines includes (i) scanning electron micrographs revealing metathoracic tympanate ears, (ii) laser interferometry showing particular sensitivity of tympana tuned to frequency components of sound signals from conspecifics, and (iii) phonotaxis of male L. monacha and L. fumida to speakers playing back sound signals from conspecific females. We conclude that tympanate ears of these moths have evolved in response not only to bat predation, but also for short-range mate finding and possibly recognition.     

Discrimination of pheromone enantiomers by two pheromone binding proteins from the gypsy moth Lymantria dispar

The gypsy moth, Lymantria dispar, uses (7R, 8S)-cis-2-methyl-7, 8-epoxyoctadecane, (+)-disparlure, as a sex pheromone. The (-) enantiomer of the pheromone is a strong behavioral antagonist. Specialized sensory hairs, sensillae, on the antennae of male moths detect the pheromone. Once the pheromone enters a sensillum, the very abundant pheromone binding protein (PBP) transports the odorant to the sensory neuron. We have expressed the two PBPs found in gypsy moth antennae, PBP1 and PBP2, and we have studied the affinity of these recombinant PBPs for the enantiomers of disparlure. To study pheromone binding under equilibrium conditions, we developed and validated a binding assay. We have addressed the two major problems with hydrophobic ligands in aqueous solution: (1) concentration-dependent adsorption of the ligand on vial surfaces and (2) separation of the protein-bound ligand from the material remaining free in solution. We used this assay to demonstrate for the first time that pheromone binding to PBP is reversible and that the two PBPs from L. dispar differ in their enantiomer binding preference. PBP1 has a higher affinity for the (-) enantiomer, while PBP2 has a higher affinity for the (+) enantiomer. The PBP from the wild silk moth, Antheraea polyphemus (Apol-3) bound the disparlure enantiomers more weakly than either of the L. dispar PBPs, but Apol-3 was also able to discriminate the enantiomers. We have observed extensive aggregation of both L. dispar PBPs and an increase in pheromone binding at high (>2 microM) PBP concentrations. We present a model of disparlure binding to the two PBPs.     

Underestimated mitochondrial diversity in gypsy moth Lymantria dispar from Asia

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Effects of intentional gaps in spray coverage on the efficacy of gypsy moth mating disruption

Abstract:  The study was conducted during 2001 and 2002 in forested areas in Virginia, US to examine the effects of gaps in coverage of pheromone on gypsy moth, Lymantria dispar (L.) (Lep., Lymantriidae), mating disruption. Gypsy moth male moth catches in pheromone-baited traps were significantly reduced in plots treated with the gypsy moth sex pheromone, disparlure, at an overall application rate of 37.5 g of active ingredient (AI)/ha but with untreated gaps of 30 or 90 m between 30-m wide treated swaths. In one of the two plots with 90 m gaps, significantly more males were captured in traps in the untreated areas compared with the treated areas within the plot. However, in another plot, significant differences in trap catches between treated and untreated areas were not observed. No difference in male moth catches in the pheromone-baited traps was observed between treated and untreated areas within the plots treated with 30 m gaps. Female mating success did not differ significantly between treated and untreated areas within the one plot in which it was measured. These results suggest that it may be possible to lower costs associated with gypsy moth mating disruption applications by alternating treated and untreated swaths, which would reduce flight time and fuel costs, without a reduction in efficacy.