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Concept: Lymantriidae

23

Quantifying the complex spatial dynamics taking place at range edges is critical for understanding future distributions of species, yet very few systems have sufficient data or the spatial resolution to empirically test these dynamics. This paper reviews how data from a large-scale pest management program have provided important contributions to the fields of population dynamics and invasion biology. The invasion of gypsy moth (Lymantria dispar) is well-documented from its introduction near Boston, Massachusetts USA in 1869 to its current extent of over 900,000 km(2) in Eastern North America. Over the past two decades, the USDA Forest Service Slow the Spread (STS) program for managing the future spread of gypsy moth has produced unrivaled spatiotemporal data across the invasion front. The STS program annually deploys a grid of 60,000 - 100,000 pheromone-baited traps, currently extending from Minnesota to North Carolina. The data from this program has provided the foundation for investigations of complex population dynamics and the ability to examine ecological hypotheses previously untestable outside of theoretical venues, particularly regarding invasive spread and Allee effects. This system provides empirical data on the importance of long-distance dispersal and time lags on population establishment and spatial spread. Studies showing high rates of spatiotemporal variation of the range edge, from rapid spread to border stasis and even retraction, highlight future opportunities to test mechanisms that influence both invasive and native species ranges. The STS trap data have also created a unique opportunity to study low-density population dynamics and quantify Allee effects with empirical data. Notable contributions include evidence for spatiotemporal variation in Allee effects, demonstrating empirical links between Allee effects and spatial spread, and testing mechanisms of population persistence and growth rates at range edges. There remain several outstanding questions in spatial ecology and population biology that can be tested within this system, such as the scaling of local ecological processes to large-scale dynamics across landscapes. The gypsy moth is an ideal model of how important ecological questions can be answered by thinking more broadly about monitoring data. This article is protected by copyright. All rights reserved.

Concepts: Science, Empirical, Lymantriidae, Biology, Empiricism, Ecology, Adam Copeland, Scientific method

2

Preventing the introduction and establishment of forest invasive alien species (FIAS) such as the Asian gypsy moth (AGM) is a high-priority goal for countries with extensive forest resources such as Canada. The name AGM designates a group of closely related Lymantria species (Lepidoptera: Erebidae: Lymantriinae) comprising two L. dispar subspecies (L. dispar asiatica, L. dispar japonica) and three closely related Lymantria species (L. umbrosa, L. albescens, L. postalba), all considered potential FIAS in North America. Ships entering Canadian ports are inspected for the presence of suspicious gypsy moth eggs, but those of AGM are impossible to distinguish from eggs of innocuous Lymantria species. To assist regulatory agencies in their identification of these insects, we designed a suite of TaqMan® assays that provide significant improvements over existing molecular assays targeting AGM. The assays presented here can identify all three L. dispar subspecies (including the European gypsy moth, L. dispar dispar), the three other Lymantria species comprising the AGM complex, plus five additional Lymantria species that pose a threat to forests in North America. The suite of assays is built as a “molecular key” (analogous to a taxonomic key) and involves several parallel singleplex and multiplex qPCR reactions. Each reaction uses a combination of primers and probes designed to separate taxa through discriminatory annealing. The success of these assays is based on the presence of single nucleotide polymorphisms (SNPs) in the 5' region of mitochondrial cytochrome c oxidase I (COI) or in its longer, 3' region, as well as on the presence of an indel in the “FS1” nuclear marker, generating North American and Asian alleles, used here to assess Asian introgression into L. dispar dispar. These assays have the advantage of providing rapid and accurate identification of ten Lymantria species and subspecies considered potential FIAS.

Concepts: Molecular biology, Bee, DNA, Pheromone, Polymerase chain reaction, Lymantriidae, North America, Gypsy moth

1

The gypsy moth, Lymantria dispar L., is one of the most destructive forest pests in the world. While the subspecies established in North America is the European gypsy moth (L. dispar dispar), whose females are flightless, the two Asian subspecies, L. dispar asiatica and L. dispar japonica, have flight-capable females, enhancing their invasiveness and warranting precautionary measures to prevent their permanent establishment in North America. Various molecular tools have been developed to help distinguish European from Asian subspecies, several of which are based on the mitochondrial barcode region. In an effort to identify additional informative markers, we undertook the sequencing and analysis of the mitogenomes of 10 geographic variants of L. dispar, including two or more variants of each subspecies, plus the closely related L. umbrosa as outgroup. Several regions of the gypsy moth mitogenomes displayed nucleotide substitutions with potential usefulness for the identification of subspecies and/or geographic origins. Interestingly, the mitogenome of one geographic variant displayed significant divergence relative to the remaining variants, raising questions about its taxonomic status. Phylogenetic analyses placed this population from northern Iran as basal to the L. dispar clades. The present findings will help improve diagnostic tests aimed at limiting risks of AGM invasions.

Concepts: United States, Lymantriidae, North America

0

The pervading paradigm in insect phenology models is that the response to a given temperature does not vary within a life stage. The developmental rate functions that have been developed for general use, or for specific insects, have for the most part been temperature-dependent but not age-dependent, except where age is an ordinal variable designating the larval instar. Age dependence, where age is a continuous variable, is not often reported (or investigated), and is rarely included in phenology models. I provide a short review of the seldom-investigated phenomenon of age dependence in developmental response to temperature, and compare the derivation of the winter moth egg phenology model by Salis et al. to the derivation of another egg phenology model with age-dependent responses to temperature I discuss some probable reasons for the discrepancies (acknowledged by Salis et al. between modelled and observed developmental rates of the winter moth, and discuss the contribution that geographically robust phenology models can make to estimates of species distributions.

Concepts: Lymantriidae, Developmental biology, Bee, Insect

0

A morpho-functional investigation of the different neuronal subpopulations projecting through each of the nerves IV to VI emerging bilaterally from the terminal abdominal ganglion (TAG) was correlated with the octopaminergic activity in the ganglion that controls the ovipositor movements associated with calling behavior in the female gypsy moth Lymantria dispar. Tetramethylrodamine-dextran backfills from nerve stumps resulted in a relatively low number of TAG projections, ranging from 12-13 for nerve pair IV, 12-14 for nerve pair V and 8-9 for nerve pair VI. Furthermore, as assessed by electrophysiological recordings, a number of fibres within each of these nerves displays spontaneous tonic activity, also when the ganglion is fully disconnected from the ventral nerve cord (VNC). Octopamine (OA) applications to the TAG strongly enhanced the activity of these nerves, either by increasing the firing rate of a number of spontaneously-firing units or by recruiting new ones. This octopaminergic activity affected calling behavior, and specifically the muscle activity leading to cycling extensions of the intersegmental membrane (IM) between segments VIII and IX (ovipositor). Our results indicate that in the female gypsy moth the octopaminergic neural activity of the TAG is coupld with extensions and retractions of IM for the purpose of releasing pheromone, where motor units innervated by nerve pair IV appear antagonistic with respect to those innervated by nerve pair V. This article is protected by copyright. All rights reserved.

Concepts: Lymantriidae, Gypsy moth, Axon, Pheromone, Action potential, Muscle, Nerve, Nervous system

0

Delta- and bucket-style (Universal or Unitrap) traps baited with 1 standard survey lure and 1/3 and 3 lures were compared for their attractiveness and trapping efficiencies for gypsy moth, Lymantria dispar L. (Lepidoptera: Erebidae), males. With bucket traps, the numbers of males attracted to within 2 m of traps and the proportion of these actually captured were identical among the three doses although the percentage of attracted males actually captured in bucket traps was low, less than 15%. A three-lure delta trap attracted about 70% more males than traps with the two lower doses. Capture efficiencies were above 80% for 1/3- and one-lure traps and about 60% for traps baited with three lures. The number of males captured in delta traps was equivalent for the three doses although our observations also suggest that a delta trap baited with three lures drew males from a wider range than lower dose lures and therefore would be a more sensitive trap for detecting incipient populations. We also noted that males tended to arrive in clusters, suggesting that attraction over moderate distances requires periods when the wind direction is fairly constant. This observation coupled with the great variability in the direction of male arrival to the traps also suggests that important changes in the area of influence of the plume are driven in such forested areas by slower but greater changes in wind direction compared with open habitats.

Concepts: Wind, Moth, Lepidoptera, Insect, Lymantriidae, Gypsy moth, Pheromone

0

In order to investigate the effects of heavy metal stress on woody plant defense against phytophagous insects, we studied development and reproduction traits of the gypsy moth, Lymantria dispar that were separately fed with leaves plucked from poplar seedlings (Populus alba berolinensis) grown in either non-contaminated soil (control), Cd-contaminated soil (1.5 mg/kg), Zn-contaminated soil (500 mg/kg) or Pb-contaminated soil (500 mg/kg). The results showed that feeding on Cd or Pb stressed poplar leaves significantly decreased L. dispar larval weights, body lengths and head capsule widths, pupal weights and female fecundity, and delayed the duration of larval development. Similar effects from the Zn stressed poplar leaves were also observed on all the above mentioned variables except male pupal weight and larval development duration that showed no differences from the control. Cd, Zn, or Pb stressed poplar leaves had no significant effects on L. dispar larval survival, pupation and emergence rates; in fact, both larval survival and pupation rates reached 100%. These results suggest that Cd, Zn or Pb stress in P. alba berolinensis might help the trees defend against the defoliator, however; L. dispar may in turn have an effective detoxification mechanism for lessening the effects of plant-mediated defenses and heavy metals in leaves on larval survival, pupation and eclosion.

Concepts: Populus, Bee, Lymantriidae, Heavy metal, Lepidoptera, Populus alba, Insect, Heavy metal music

0

Larvae of the gypsy moth, Lymantria dispar, infected with the microsporidium, Nosema lymantriae, release infective spores with feces. We tested the effects of simulated light rain on transmission in cages, providing random contamination of host plant foliage with feces. Contamination by larvae in the intermediate stage of infection, 15-16 days post inoculation, entailed transmission to a mean 4.4 to 16.7% of test larvae. Simulated rain significantly increased transmission to 30.0 to 57.3%. Transmission success significantly increased with disease progress. Experiments demonstrated that feces are a suitable source of spores and a likely transmission pathway in the field.

Concepts: Bee, Lymantriidae, Infection

0

Interactions between species can have cascading effects that shape subsequent interactions. For example, herbivory can induce plant defenses that affect subsequent interactions with herbivores, pathogens, mycorrhizae, and pollinators. Parasitic plants are present in most ecosystems, and play important roles in structuring communities. However, the effects of host herbivory on parasitic plants, and the potential mechanisms underlying such effects, are not well known. We conducted a greenhouse study to ask whether gypsy moth (Lymantria dispar) damage, host cultivar, and their interaction affected preference of the stem parasite dodder (Cuscuta spp.) on cranberry hosts (Vaccinium macrocarpum). We then assessed the mechanisms that could underlie such effects by measuring induced changes in phytohormones and secondary compounds. We found that damage by gypsy moths delayed dodder attachment by approximately 0.3 days when dodder stems were added 2 days after damage, and reduced attachment by more than 50% when dodder stems were added 1 week after host plant damage. Gypsy moth damage significantly increased jasmonic acid (JA) levels, total volatile emissions, and the flavonol, quercetin aglycone, suggesting possible mechanisms underlying variation in dodder ability to locate or attach to hosts. Dodder preference also differed between cranberry cultivars, with the highest attachment on the cultivar that had significantly lower levels of total volatile emissions and total phenolic acids, suggesting that volatile composition and phenolics may mediate dodder preference. Our results indicate that herbivory can reduce subsequent attachment by a highly damaging parasitic plant, demonstrating the potential importance of early damage for shaping subsequent species interactions.

Concepts: Symbiosis, Quercetin, Lymantriidae, Cuscuta, Parasitism, Gypsy moth, Parasitic plant, Plant

0

The goal of this study was to develop effective and practical field sampling methods for quantifying aerial deposition of airborne conidia of Entomophaga maimaiga over space and time. This important fungal pathogen is a major cause of larval mortality in invasive gypsy moth (Lymantria dispar) populations in the United States. Airborne conidia of this pathogen are relatively large (similar in size to pollen) with unusual characteristics, requiring specialized methods for collection and quantification. Initially, dry sampling (settling of spores from the air onto a dry surface) was used to confirm the detectability of E. maimaiga at field sites with L. dispar mortality caused by E. maimaiga using quantitative PCR (qPCR) methods. We then measured the signal degradation of conidial DNA on dry surfaces under field conditions, ultimately rejecting dry sampling as a reliable method due to rapid DNA degradation. We modified a chamber-style trap commonly used in palynology to capture settling spores in buffer. We tested this wet-trapping method in a large-scale (137 km) spore-trapping survey across gypsy moth outbreak regions undergoing epizootics in Pennsylvania in the summer of 2016. Using four-day collection periods during the period of late instar and pupal development, we detected variable amounts of target DNA settling from the air. The amounts declined over the season and with distance from the nearest defoliated area, indicating airborne spore dispersal from outbreak areas.IMPORTANCE We report on a method for trapping and quantifying airborne spores of Entomophaga maimaiga, an important fungal pathogen impacting gypsy moth (Lymantria dispar) populations. This method can be used to track dispersal of E. maimaiga from epizootic areas and ultimately provide critical understanding of the spatial dynamics of gypsy moth-pathogen interactions.

Concepts: Asexual reproduction, Pheromone, Bee, Fungus, Lymantriidae, Polymerase chain reaction, Spore