Influence of the braconid Glyptapanteles liparidis on the juvenile hormone titer of its larval host,the gypsy moth,Lymantria dispar

The increase in the juvenile hormone (JH) III titer in the hemolymph of Lymantria dispar larvae that were parasitized by the endoparasitoid braconid, Glyptapanteles liparidis, during the host's premolt to third instar, coincided with the molt of the parasitoid larvae to the second instar between day 5 and 7 of the fourth host instar. It reached a maximum mean value of 89 pmol/ml on day 7 of the fifth instar while it remained below 1 pmol/ml in unparasitized larvae. Only newly molted fifth instar hosts showed a low JH III titer similar to that of the unparasitized larvae. JH II, which is the predominant JH homologue in unparasitized gypsy moth larvae, also increased relative to controls in the last two samples (days 7 and 9) from parasitized fourth and fifth instars. Compared to unparasitized larvae, a generally reduced activity of JH esterase (JHE) was found in parasitized larvae throughout both larval stages. The reduction in enzyme activity at the beginning and at the end of each instar, when the JHE activity in unparasitized larvae was high, may be in part responsible for the increased JH II and JH III titers in parasitized larvae. Ester hydrolysis was the only pathway of JH metabolism in the hemolymph of unparasitized and parasitized gypsy moth larvae as detected by chromatographic assays. © 1996 Wiley-Liss, Inc.     

Adult feeding affects fecundity of the predator,Calosoma sycophanta (Col.: Carabidae)

Calosoma sycophanta L. adults were fed either gypsy moth (Lymantria dispar L.) larvae or split grapes for set periods of time while their reproduction was monitored. Few female beetles reproduced unless fed gypsy moth larvae during the first week after they ended hibernation. Even females initially fed grapes that were later fed larvae had reduced reproduction. The implications these results have for relationships between beetle and gypsy moth populations are discussed.     

Facilitation between invasive herbivores: hemlock woolly adelgid increases gypsy moth preference for and performance on eastern hemlock

1. Interactions between invertebrate herbivores with different feeding modes are common on long-lived woody plants. In cases where one herbivore facilitates the success of another, the consequences for their shared host plant may be severe. Eastern hemlock (Tsuga canadensis), a canopy-dominant conifer native to the eastern U.S., is currently threatened with extirpation by the invasive stylet-feeding hemlock woolly adelgid (Adelges tsugae). The effect of adelgid on invasive hemlock-feeding folivores remains unknown. 2. This study evaluated the impact of feeding by hemlock woolly adelgid on gypsy moth (Lymantria dispar) larval preference for, and performance on, eastern hemlock. To assess preference, 245 field-grown hemlocks were surveyed for gypsy moth herbivory damage and laboratory paired-choice bioassays were conducted. To assess performance, gypsy moth larvae were reared to pupation on adelgid-infested or uninfested hemlock foliage, and pupal weight, proportional weight gain, and larval period were analysed. 3. Adelgid-infested hemlocks experienced more gypsy moth herbivory than did uninfested control trees, and laboratory tests confirmed that gypsy moth larvae preferentially feed on adelgid-infested hemlock foliage. Gypsy moth larvae reared to pupation on adelgid-infested foliage gained more weight than larvae reared on uninfested control foliage. 4. These results suggest that the synergistic effect of adelgid and gypsy moth poses an additional threat to eastern hemlock that may increase extirpation risk and ecological impact throughout most of its range.     

Pheromonotropic activity in the gypsy moth Lymantria dispar: evidence for a neuropeptide

The brain-suboesophageal ganglion complex of the gypsy moth, Lymantria dispar, contains pheromonotropic activity detectable using a Helicoverpa zea in vivo bioassay for pheromone-biosynthesis-activating neuropeptide. Pheromonotropic activity was detected as early as the third larval instar and was present throughout development and through day 6 post-eclosion. Activity in the adult is presumably associated with pheromone production, while it is speculated that larval activity may be related to melanization. Adult pheromonotropic activity is associated with a peptide of approximately 3.500 kDa. It is heat labile and only partially stable when incubated at 35°C or exposed to freeze-thawing. Isolation of L. dispar pheromonotropic factor should facilitate the elucidation of the mechanism of pheromone production in this insect pest.Abbreviations ED ₅₀ dose at which one-half maximal response is observal - eq equivalent - MRCH melanization and reddish colorization hormone - MW molecular weight - PBAN pheromone biosynthesis activating neuropeptide - SOG suboesophageal ganglion - TFA trifluoroacetic acid - Z11-16: Ald (Z)-11-hexadecenal     

Leaf Surface Lipophilic Compounds as One of the Factors of Silver Birch Chemical Defense against Larvae of Gypsy Moth

Plant chemical defense against herbivores is a complex process which involves a number of secondary compounds. It is known that the concentration of leaf surface lipophilic compounds (SLCs), particularly those of flavonoid aglycones are increased with the defoliation treatment of silver birch Betula pendula. In this study we investigated how the alteration of SLCs concentration in the food affects the fitness and innate immunity of the gypsy moth Lymantria dispar. We found that a low SLCs concentrations in consumed leaves led to a rapid larval development and increased females’ pupae weight (= fecundity) compared to larvae fed with leaves with high SLCs content. Inversely, increasing the compounds concentration in an artificial diet produced the reverse effects: decreases in both larval weight and larval survival. Low SLCs concentrations in tree leaves differently affected larval innate immunity parameters. For both sexes, total hemocytes count in the hemolymph increased, while the activity of plasma phenoloxidase decreased when larvae consume leaves with reduced content of SLCs. Our results clearly demonstrate that the concentration of SLCs in silver birch leaves affects not only gypsy moth fitness but also their innate immune status which might alter the potential resistance of insects against infections and/or parasitoids.     

Hostplant,larval age,and feeding behavior influence midgut pH in the gypsy moth (Lymantria dispar)

Summary The midgut pH of late instar gypsy moth (Lymantria dispar L.) larvae is strongly alkaline, and varies with diet, larval stadium, and time since feeding. Midgut pH rises with time since feeding, and does so more quickly, reaching greater maximum values, on some diets than others. Leaf tissues of 23 tree species resist increases in alkalinity differentially; this trait and differing initial leaf pH may explain the impact of diet on gut pH. Third instar larvae may have gut conditions favorable for tannin-protein binding shortly after ingesting certain foods, but with time midgut alkalinity becomes great enough to dissociate tannin-protein complexes. Older instars rarely exhibit gut pHs low enough to permit tannin activity. Alkaline gut conditions may explain the gypsy moth's ability to feed on many tanniniferous plant species, especially in later instars. Consequences for pathogen effectiveness are discussed.     

First record of Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) in Slovakia

The entomopathogenic fungus Entomophaga maimaiga was found for the first time in Slovakia in 2013. Late instar larvae of gypsy moth, Lymantria dispar, from two sites with different population densities were dissected to evaluate the presence of pathogens. The presence of conidia and resting spores of E. maimaiga in gypsy moth cadavers was confirmed from both sites.     

Microbial synergists pathogenic to Lymantria dispar: Chitinolytic and fermentative bacterial interactions

A chitinolytic bacterium isolated from a healthy gypsy moth, Lymantria dispar, larva was shown to be pathogenic to larvae when administered per os after growth on chitin broth. However, the chitin hydrolase produced by this isolate had a pH optimum for activity of 5.5 and the high alkalinity in the mesenteron of L. dispar larvae severely limited chitinolysis of the midgut lining. Fermentative, nonpathogenic, acid-producing bacteria isolated from healthy gypsy moth larvae effectively lowered larval mesenteron pH when administered per os and the combination of fermentative isolates with a crude culture aliquot of the chitinolytic strain produced a synergistic increase in mortality over either dose administered by itself. Increased mortality was also observed for most fermentative strains when they were combined with crude supernatants of centrifuged cultures of the chitinolytic strain, although these combinations proved less effective than when fermenters were added to the whole-culture aliquots of the chitinolytic strain. In vitro studies showed that other bacteria isolated from environments foreign to that of the gypsy moth could ferment carbohydrates with acid production at an alkaline pH; however, in vivo studies demonstrated that these bacteria were incapable both of poising larval midgut pH and of enhancing mortality when added to chitinolytic bacteria.     

Effect of conidial dispersal of the fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) on survival of its gypsy moth (Lepidoptera: Lymantriidae) host

Several researchers have developed a one-generational computer model that simulates infection prevalence of gypsy moth, Lymantria dispar, caterpillars by its fungal pathogen, Entomophaga maimaiga. Inputs required are temperature, humidity, and rainfall records, a measure of fungus resting spore load in the soil, and an estimate of gypsy moth larval density. In a previous study, the model accurately tracked fungal-induced host mortality as long as airborne fungal conidia were allowed to disperse freely over a local area. In 2002, dispersal of conidia and its influence on the impact of the fungus on the gypsy moth was investigated. Gypsy moth densities and fungus resting spore loads were measured in 15 plots within a 3 km area. In 7 of the plots, prevalence of fungal disease was determined weekly by collecting and rearing gypsy moth larvae. Different strategies were used to disperse conidia within the model, and resulting simulated prevalence rates were compared to actual data. Model output was most accurate when airborne conidia were permitted to disperse equally to all plots. Thus, to accurately assess the impact of the fungus in one location, it is necessary to take into account fungal activity throughout the local area.     

NADPH-cytochrome-c-reductase: Changes in specific activity in gypsy moth larvae

NADPH-cytochrome-c-reductase from guts of gypsy moth, Porthetria dispar, oxidized NADPH at the following rates: 11·6, 41·9, and 57·6 nmol/30 min per 0·6 mg protein, in the third, fourth and fifth instar, respectively. The increase in specific activity may be due to a natural induction process controlled by materials in the food. This could also explain the observed decreases just prior to ecdysis at which time the larvae have ceased feeding.     

Asynchrony between Host Plant and Insects-Defoliator within a Tritrophic System: The Role of Herbivore Innate Immunity

The effects of asynchrony in the phenology of spring-feeding insect-defoliators and their host plants on insects’ fitness, as well as the importance of this effect for the population dynamics of outbreaking species of insects, is a widespread and well-documented phenomenon. However, the spreading of this phenomenon through the food chain, and especially those mechanisms operating this spreading, are still unclear. In this paper, we study the effect of seasonally declined leafquality (estimated in terms of phenolics and nitrogen content) on herbivore fitness, immune parameters and resistance against pathogen by using the silver birch Betula pendula—gypsy moth Lymantria dispar—nucleopolyhedrovirus as the tritrophic system. We show that a phenological mismatch induced by the delay in the emergence of gypsy moth larvae and following feeding on mature leaves has negative effects on the female pupal weight, on the rate of larval development and on the activity of phenoloxidase in the plasma of haemolymph. In addition, the larval susceptibility to exogenous nucleopolyhydrovirus infection as well as covert virus activation were both enhanced due to the phenological mismatch. The observed effects of phenological mismatch on insect-baculovirus interaction may partially explain the strong and fast fluctuations in the population dynamics of the gypsy moth that is often observed in the studied part of the defoliator area. This study also reveals some indirect mechanisms of effect related to host plant quality, which operate through the insect innate immune status and affect resistance to both exogenous and endogenous virus.     

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.     

Effects of heavy metal stress on free amino acids in the haemolymph and proteins in haemolymph and total body tissue of Lymantria dispar larvae parasitized by Glyptapanteles liparidis

Heavy metal contamination of the forest pest insect Lymantria dispar (L.) (Lepidoptera; Lymantriidae), the gypsy moth, can alter its haemolymph composition, as has already been shown for carbohydrates and lipids in recent studies. L. dispar larvae are frequently parasitized by Glyptapanteles liparidis (Bouché) (Hymenoptera; Braconidae) larvae, which can—to some extent—regulate the population size of the pest insect. The parasitoids feed on the haemolymph of L. dispar larvae; hence, a different haemolymph composition of the host alters the trophic situation of the parasitoids. The aim of the present study was to investigate whether metal contamination also affects the concentrations of free amino acids in L. dispar haemolymph, and protein concentrations in their haemolymph and tissue. L. dispar larvae were parasitized on the first day of the second instar and then reared on diets contaminated with Cd, Pb, Cu or Zn at two concentrations each. Haemolymph and total body tissue of the larvae (fourth instar/third day) were analyzed. The concentrations of the free amino acids were elevated in five out of the eight contamination groups (Cd6, Pb4, Cu6, Cu10, Zn60), whereas haemolymph protein concentrations were significantly reduced in all contaminated individuals. The haemolymph protein concentration was 18 mg/ml in the control group and decreased to less than 10 mg/ml due to cadmium and zinc contamination at both concentrations and in the low copper contamination group. In contrast, total body proteins (136 g/mg dry weight in the control group) were elevated due to heavy metal stress. Analyses of haemolymph protein concentrations during the fourth instar demonstrated an increase of the proteins from day one to day four (followed by a decrease on the fifth day) in the control group and the cadmium contamination group. A steady increase of proteins from the first to the fifth day in the copper and zinc contaminated larvae indicated a retarded development in these groups. Thus, the present study along with other recent studies demonstrated, that heavy metal stress changes the concentrations of all main haemolymph compounds of L. dispar larvae.     

Influence of Diet and Density on Laboratory Cannibalism Behaviors in Gypsy Moth Larvae (Lymantria dispar L.)

The gypsy moth (Lymantria dispar) is an insect folivore that feeds on a broad range of hosts, and undergoes intermittent outbreaks that cause extensive tree mortality. Like many other herbivorous insects, gypsy moth larvae consume a substrate that is low in nitrogen. Gypsy moth larvae have been known to cannibalize under crowded conditions in the laboratory. In this study, we assessed the influence of nitrogen and density on cannibalism behavior in gypsy moth larvae. Cannibalism rates increased with decreased nitrogen and increased density. There was no interaction between these two parameters. Developmental experiments confirmed that low dietary nitrogen is detrimental, in agreement with previous studies. In a second experiment, we assessed the influence of previous cannibalism experiences on subsequent cannibalism behavior. Gypsy moth larvae that had previously cannibalized other larvae subsequently exhibited higher cannibalism rates than those larvae that had not cannibalized. In conclusion, low nitrogen, high larval density, and previous cannibalism experience are important factors contributing to gypsy moth larval cannibalism. Future studies are needed to estimate benefits to larvae, and to more closely approximate field conditions.     

Underestimated mitochondrial diversity in gypsy moth Lymantria dispar from Asia

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Specificity of Developmental Resistance in Gypsy Moth （Lymantria dispar） to two DNA-Insect Viruses

Gypsy moth (Lymantria dispar) larvae displayed marked developmental resistance within an instar to L. dispar M nucleopolyhedrovirus (LdMNPV) regardless of the route of infection (oral or intrahemocoelic) in a previous study, indicating that in gypsy moth, this resistance has a systemic component. In this study, gypsy moth larvae challenged with the Amsacta moorei entomopoxvirus (AMEV) showed developmental resistance within the fourth instar to oral, but not intrahemocoelic, inoculation. In general, gypsy moth is considered refractory to oral challenge with AMEV, but in this study, 43% mortality occurred in newly molted fourth instars fed a dose of 5×10⁶ large spheroids of AMEV; large spheroids were found to be more infectious than small spheroids when separated by a sucrose gradient. Developmental resistance within the fourth instar was reflected by a 2-fold reduction in mortality (18%–21%) with 5×10⁶ large spheroids in larvae orally challenged at 24, 48 or 72 h post-molt. Fourth instars were highly sensitive to intrahemocoelic challenge with AMEV; 1PFU produced approximately 80% mortality regardless of age within the instar. These results indicate that in gypsy moth, systemic developmental resistance may be specific to LdMNPV, reflecting a co-evolutionary relationship between the baculovirus and its host.     

Characterization of hemolymph juvenile hormone esterase from Lymantria dispar

A major peak of juvenile hormone esterase (JHE) activity approaching 330 nmol JH III hydrolyzed/min/ml of hemolymph was observed during the last larval growth stage in Lymantria dispar. A smaller peak of JHE occurred 3–5 days after pupation. The gypsy moth JHE was purified from larval hemolymph using a classical approach. A specific activity of 766 units per mg of protein and a K_m of 3.6 × 10⁻⁷ M for racemic JH III and the (10R, 11S) enantiomer of JH II was determined for the purified enzyme. The 62 kDa esterase was insensitive to inhibition by O,O-diisopropyl phosphorofluoridate (DFP), or by phenylmethylsulfonyl fluoride (PMSF). Two forms of JHE isolated by RP-HPLC were indistinguishable by HPLC tryptic peptide mapping and share an identical N-terminal amino acid sequence. Polyclonal antisera raised against gypsy moth enzyme cross-reacted with JHE from Trichoplusia ni but not with JHE from Manduca sexta. A weak cross-reactivity was observed with JHE from Heliothis virescens. Forty amino acid residues of the N-terminus were placed in sequence. The N-terminal sequence of JHE from L. dispar showed little homology to the sequence of JHE from H. virescens. The immunological and structural data support the conclusion that markedly different esterases, which catalyze the hydrolysis of juvenile hormone, are present in the hemolymph of different Lepidoptera.     

Accumulation of Cd and Pb in various body parts,organs and tissues of Lymantria dispar asiatica (Lepidoptera: Erebidae)

To investigate the accumulation patterns of Cd and/or Pb in various body parts, organs and tissues of the Asian gypsy moth (Lymantria dispar) larvae under Cd and/or Pb stress, Cd and Pb treated artificial diets were used to feed the larvae in the current study. These larval body parts/organs/tissues included the heads, integuments (body walls), alimentary canals, fat bodies and hemolymphs. Our results showed that under Cd and/or Pb stress, their accumulations in larval body parts/organs/tissues were significantly higher than those in the control, with the amounts of tested metals in the fat bodies and hemolymphs and alimentary canals being significantly higher than those in the heads and integuments. Under the single Cd (0, 7.5, 10.5 mg/kg) or Pb stress (0, 55, 90, 125 mg/kg), the accumulations of these heavy metals were positively correlated with their concentrations in diets. Under the combined stress (Cd × Pb), the Cd accumulation at the lower Pb concentrations was higher than that at higher Pb concentrations for the body parts/organs/tissues, similar effects of Cd concentrations on Pb accumulations were also recorded. These results clearly showed that Cd and/or Pb were accumulated in various body parts/organs/tissues at different levels under the heavy metal stress. And accumulations of Pb/Cd were positively correlated with their concentrations in the diets under the single stress. Under the combined stresses, Cd and Pb had synergistic effects at low concentrations whereas antagonistic effects at high concentrations. The accumulations of Cd and/or Pb in the gypsy moth larvae affects normal physiological and biochemical functions, and thus affects their growth and development.     

Neurometamorphosis of the ear in the gypsy moth,Lymantria dispar,and its homologue in the earless forest tent caterpillar moth,Malacosoma disstria

The adult gypsy moth, Lymantria dispar (Lymantriidae: Noctuoidea) has a pair of metathoracic tympanic ears that each contain a two-celled auditory chordotonal organ (CO). The earless forest tent caterpillar moth, Malacosoma disstria (Lasiocampidae: Bombycoidea), has a homologous pair of three-celled, nonauditory hindwing COs in their place. The purpose of our study was to determine whether the adult CO in both species arises from a preexisting larval organ or if it develops as a novel structure during metamorphosis. We describe the larval metathoracic nervous system of L. dispar and M. distria, and identify a three-celled chordotonal organ in the anatomically homologous site as the adult CO. If the larval CO is severed from the homologue of the adult auditory nerve (IIIN1b1) in L. dispar prior to metamorphosis, the adult develops an ear lacking an auditory organ. Axonal backfills of the larval IIIN1b1 nerve in both species reveal three chordotonal sensory neurons and one nonchordotonal multipolar cell. The axons of these cells project into tracts of the central nervous system putatively homologous with those of the auditory pathways in adult L. dispar. Following metamorphosis, M. disstria moths retain all four cells (three CO and one multipolar) while L. dispar adults possess two cells that service the auditory CO and one nonauditory, multipolar cell. We conclude that the larval IIIN1b1 CO is the precursor of both the auditory organ in L. dispar and the putative proprioceptor CO in M. disstria and represents the premetamorphic condition of these insects. The implications of our results in understanding the evolution of the ear in the Lepidoptera and insects in general are discussed. © 1996 John Wiley & Sons, Inc.