Pathology and epizootiology of Entomophaga maimaiga infections in forest Lepidoptera

Abstract

The insect-pathogenic fungal pathogen Entomophaga maimaiga is endemic to northeastern Asia and was first found in North America in 1989. Due to repeated epizootics and spread within populations of the major forest defoliator in northeastern North America, the gypsy moth (Lymantria dispar), this pathogen has gained much notoriety. Although this pathogen was purposely introduced to North America for biological control of L. dispar in 1910 to 1911, it is questionable whether it became established at the time of release and then remained at innocuous levels until relatively recently. Alternatively, the fungal strain present in North America today could be a more recent accidental introduction. DNA analysis demonstrates that this pathogen differs significantly from North American members of the same species complex (the Lepidoptera-specific Entomophaga aulicae species complex), and, to date, isolates of this introduced pathogen display little heterogeneity in North America. Nonsusceptible lepidopteran larvae have been identified, and either E. maimaiga is unable to penetrate the cuticle or the fungus cannot survive within the hemocoel. In the latter case, although E. maimaiga grows as protoplasts lacking cell walls in the host hemolymph, glycoproteins on plasma membranes of the protoplasts could lead to host recognition. Epizootiological studies demonstrate a clear association between fungal activity and environmental moisture but little association with host density under hypothesized conditions of high fungal density. Prediction of the occurrence of epizootics is not yet possible. E. maimaiga is easily established in new areas by releasing azygospores, but the ability to use this pathogen further for biological control will depend, in large part, on the development of mass production systems.

FIG. 1

Distribution of E. maimaiga in the United States in 1989. Open circles, locations where E. maimaiga was not found; solid circles, locations where E. maimaiga was found during June and July 1989; circles containing stars, locations where the 1984 isolate of E. maimaiga from Japan was released in 1985 and 1986. Lines indicate limits of defoliation caused by L. dispar as it spread from its original introduction site near Boston (arrow). Reprinted from reference with permission of the publisher.

FIG. 2

Spread of E. maimaiga in the United States from 1989 to 1992. Reprinted from reference with permission of the publisher.

FIG. 3

(A) Pear-shaped conidia actively discharged from the surface of cadavers (average conidial dimensions, 20.6 by 26.6 μm). (B) Double-walled azygospores containing lipid droplets, produced within later-instar cadavers (average azygospore diameter, 32.1 μm).

FIG. 4

Conidia of E. maimaiga that have germinated and produced germ tubes, at the end of which appressoria (arrows) have formed near the base of a secondary seta on the L. dispar cuticle. Bar, 10 μm. Reprinted from reference with permission of the publisher.

FIG. 5

Multinucleate protoplasts of E. maimaiga within infected L. dispar, late in an infection. Bar, 20 μm.

FIG. 6

Scanning electron micrograph of conidiophores of E. maimaiga bearing conidia. Reprinted from reference with permission of the publisher. (Image by T. M. Butt.)

FIG. 7

Early-instar L. dispar larva killed by E. maimaiga, with conidia being discharged. The cadaver is attached to a twig in the understory vegetation. Photograph by D. Specker. Reprinted from reference with permission of the publisher.

FIG. 8

Later-instar L. dispar larva killed by E. maimaiga and containing azygospores. There is no external indication of fungal mortality, and the cadaver is positioned on tree bark with its head facing downward. Photograph by D. Specker.

FIG. 9

Densities of E. maimaiga azygospores at different soil depths and distances from tree trunks. Data from reference .

FIG. 10

Phase-contrast image of E. maimaiga protoplasts grown in Grace’s insect tissue culture medium plus 5% fetal bovine serum. Bar, 10 μm. Reprinted from reference with permission of the publisher.