Persistence of Resting Spores ofEntomophaga maimaiga,a Fungal Pathogen of the Gypsy Moth,Lymantria dispar

We investigated the association of environmental factors (temperature, photoperiod, host molting status) and fungal factors (isolate, dose, strain attenuation) with the production of conidia versus resting spores by the entomopathogenic fungus Entomophaga maimaiga infecting the larvae of the gypsy moth Lymantria dispar. Fungal spores produced from individual cadavers of larvae killed by E. maimaiga can include conidia discharged from the cadaver surface, resting spores (azygospores) within the cadaver, or both spore types. The single factor having the greatest impact on the type of spore produced was host age; second instars virtually never contained resting spores, independent of temperature, while fifth instar cadavers contained resting spores more frequently at higher temperatures. However, there was increased conidiation at lower temperatures. Photoperiod was the only factor studied that did not significantly influence the type of spore produced. Resting spore production was negatively associated with the molting cycle; cadavers of those larvae that molted or exhibited premolt characteristics during the period between infection and death contained fewer resting spores. Increased fungal dose yielded more resting spores, as did extensive serial passage, which simultaneously caused a decrease in conidiation. Fungal isolates varied in the types of spores produced, with fewer cadavers of larvae killed by the least virulent isolate discharging conidia. Results from this study support the hypothesis that both the condition of the fungal pathogen as well as the environment surrounding it contribute to the types of spores produced. Keywords: fungal sporulation, resting spores, azygospores, Entomophthorales, Entomophaga maimaiga, biological control.

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Isolation and characterization of Entomophaga maimaiga sp. nov., a fungal pathogen of gypsy moth, Lymantria dispar, from Japan

Journal of Invertebrate Pathology ◽

10.1016/0022-2011(88)90030-4 ◽

1988 ◽

Vol 51 (3) ◽

pp. 229-241 ◽

Cited By ~ 50

Author(s):

Richard S. Soper ◽

Mitsuaki Shimazu ◽

Richard A. Humber ◽

Mark E. Ramos ◽

Ann E. Hajek

Keyword(s):

Gypsy Moth ◽

Lymantria Dispar ◽

Fungal Pathogen ◽

Isolation And Characterization ◽

Entomophaga Maimaiga

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Quantitative Analysis of a Pathogen-Induced Premature Collapse of a “Leading Edge” Gypsy Moth (Lepidoptera: Lymantriidae) Population in Virginia

Journal of Entomological Science ◽

10.18474/0749-8004-34.1.84 ◽

1999 ◽

Vol 34 (1) ◽

pp. 84-100 ◽

Cited By ~ 11

Author(s):

R. E. Webb ◽

G. B. White ◽

K. W. Thorpe ◽

S. E. Talley

Keyword(s):

Gypsy Moth ◽

Lymantria Dispar ◽

Nuclear Polyhedrosis Virus ◽

Leading Edge ◽

Late Season ◽

Early Appearance ◽

Entomophaga Maimaiga ◽

Resting Spores ◽

Nuclear Polyhedrosis ◽

Second Wave

The population dynamics of a “leading edge” (= at the edge of the expanding gypsy moth invasion) gypsy moth, Lymantria dispar (L.), population was monitored for 3 years (1995–97), with emphasis on the interactions of the gypsy moth nuclear polyhedrosis virus (LdNPV) and the fungus Entomophaga maimaiga Humber, Shimazu, & Soper. Gypsy moth populations in the woodlots varied from very sparse to high (potentially defoliating) levels. LdNPV was strongly density dependent, being confirmed only from the higher populated woodlots. In contrast, the fungus was similarly active in both sparse and highly-populated woodlots. In 1995, the fungal epizootic developed late in the season, with most larvae succumbing during stadia 5–6 and producing mainly resting spores (azygospores). Estimated mortality due to fungus averaged 68% in high-density plots and 85% in low-density plots. LdNPV mortality occurred in a two-wave epizootic, although second-wave LdNPV mortality was undoubtedly reduced because of the reduction of late-season larvae due to fungus activity. Estimated mortality due to LdNPV averaged 14% in highly-populated plots and 1% in low-population plots. In 1996, high levels of fungal-induced mortality occurred earlier in the gypsy moth season than in the previous year. Most gypsy moth larvae in 1996 died in a mid-season wave of fungal-induced mortality, with necropsied cadavers containing only conidia. This resulted in relatively few larvae surviving to late instars. At this time, a second wave of fungus-induced mortality occurred, with over half of the necropsied cadavers containing resting spores. The depletion of the gypsy moth populations by the fungus in 1995 resulted in a greatly reduced first wave of LdNPV in all plots in 1996, and perhaps due to the early appearance of the fungus in 1996, LdNPV was nearly absent from late-season larvae collected from all plots. In 1997, gypsy moth populations were uniformly low, and no dead larvae were found in any of the plots.

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Storage of Resting Spores of the Gypsy Moth Fungal Pathogen, Entomophaga maimaiga

Biocontrol Science and Technology ◽

10.1080/09583150120076184 ◽

2001 ◽

Vol 11 (5) ◽

pp. 637-647 ◽

Cited By ~ 5

Author(s):

Ann E. Hajek ◽

Micheal M. Wheeler ◽

Callie C. Eastburn ◽

Leah S. Bauer

Keyword(s):

Gypsy Moth ◽

Fungal Pathogen ◽

Entomophaga Maimaiga ◽

Resting Spores

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Detecting the titer in forest soils of spores of the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen, Entomophaga maimaiga (Zygomycetes: Entomophthorales)

The Canadian Entomologist ◽

10.4039/ent134269-2 ◽

2002 ◽

Vol 134 (2) ◽

pp. 269-279 ◽

Cited By ~ 13

Author(s):

Ronald M. Weseloh ◽

Theodore G. Andreadis

Keyword(s):

Forest Soils ◽

Gypsy Moth ◽

Fungal Pathogen ◽

Spore Viability ◽

Resting Spore ◽

Entomophaga Maimaiga ◽

Resting Spores ◽

A Site ◽

Spore Load

AbstractBioassays and direct counts were used to assess the abundance of resting spores of the gypsy moth, Lymantria dispar (L.), fungal pathogen, Entomophaga maimaiga Humber, Shimazu and Soper in forest soils. Resting spores in soil collected in October, January, and March and held under refrigeration germinated as readily as spores collected in April, but those collected in April germinated faster. Bioassays of resting spores in soils from different sites in Connecticut were directly related to results obtained from physically counting spores in the soil, and weakly correlated with a previously developed forest-based bioassay. The number of resting spores in a site was inversely related to the number of years since the site had last been defoliated by the gypsy moth, resulting in an implied maximum viability of resting spores of about 10 years. This maximum longevity was similar to a direct measure of long-term resting-spore viability. The study implies that resting-spore load in the soil may be an important determinant of the ability of the pathogen to control the gypsy moth.

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Interactions between the introduced fungal pathogen Entomophaga maimaiga and indigenous tachinid parasitoids of gypsy moth Lymantria dispar in Bulgaria

Phytoparasitica ◽

10.1007/s12600-012-0269-6 ◽

2012 ◽

Vol 41 (2) ◽

pp. 125-131 ◽

Cited By ~ 5

Author(s):

Georgi Georgiev ◽

Zdravko Hubenov ◽

Margarita Georgieva ◽

Plamen Mirchev ◽

Maria Matova ◽

...

Keyword(s):

Gypsy Moth ◽

Lymantria Dispar ◽

Fungal Pathogen ◽

Entomophaga Maimaiga

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Formation and germination of Entomophaga maimaiga azygospores

Canadian Journal of Botany ◽

10.1139/b97-888 ◽

1997 ◽

Vol 75 (10) ◽

pp. 1739-1747 ◽

Cited By ~ 33

Author(s):

Ann E. Hajek ◽

Richard A. Humber

Keyword(s):

Gypsy Moth ◽

Lymantria Dispar ◽

Early Summer ◽

Resting Spore ◽

Body Development ◽

Entomophaga Maimaiga ◽

Resting Spores ◽

Late Instar ◽

Hyphal Bodies ◽

Hyphal Body

Azygospores (resting spores) of the gypsy moth fungal pathogen Entomophaga maimaiga are produced in abundance during late spring and early summer in late-instar gypsy moth larvae (Lymantria dispar). Azygospores subsequently form, each from an individual hyphal body. Development of azygospores occurs asynchronously over several days; by 5 days after host death, greater than 60% of fungal cells had matured from hyphal bodies to the final double-walled resting state. Azygospores undergo constitutive dormancy and, under field conditions, will not germinate for approximately 9 months after production. Azygospores do not require nutrients to germinate. Germination of field-collected resting spores under laboratory conditions began more than 2 days after transfer from the field to the laboratory. Higher levels of germination occurred with a 14 h L: 10 h D cycle compared with 13 h L: 11 h D or 12 h L: 12 h D. Azygospores germinate relatively slowly and germination rates were greatest between 4 and 8 days, with a total of 71.8 or 72.5% germination by 16 days at 14 h L: 10 h D and 15 or 20 °C, respectively. During 1994 and 1995, resting spores began causing infections in experimental larvae in early May, about 1 – 2 weeks prior to gypsy moth egg hatch, and ceased causing infections in mid to late June, when late instars were present. This latter timing is a correction of previously reported information. Bioassays investigating resting spore activity determined that during 1994, once resting spores began germinating in the field, levels of infection were positively associated with soil moisture. Key words: azygospores, resting spores, entomopathogenic fungi, Entomophaga maimaiga, Lymantria dispar, biological control.

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Modification of a Pollen Trap Design To Capture Airborne Conidia of Entomophaga maimaiga and Detection of Conidia by Quantitative PCR

Applied and Environmental Microbiology ◽

10.1128/aem.00724-17 ◽

2017 ◽

Vol 83 (17) ◽

Cited By ~ 3

Author(s):

Tonya D. Bittner ◽

Ann E. Hajek ◽

Andrew M. Liebhold ◽

Harold Thistle

Keyword(s):

Quantitative Pcr ◽

Gypsy Moth ◽

Lymantria Dispar ◽

Fungal Pathogen ◽

Large Scale ◽

The United States ◽

Trap Design ◽

Content Type ◽

Entomophaga Maimaiga ◽

Airborne Conidia

ABSTRACT The goal of this study was to develop effective and practical field sampling methods for quantification of aerial deposition of airborne conidia of Entomophaga maimaiga over space and time. This important fungal pathogen is a major cause of larval death 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, and require 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 deaths 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 in Pennsylvania undergoing epizootics, in the summer of 2016. Using 4-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 affecting gypsy moth (Lymantria dispar) populations. This method can be used to track dispersal of E. maimaiga from epizootic areas and ultimately to provide critical understanding of the spatial dynamics of gypsy moth-pathogen interactions.

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