Fecal Transmission of Nucleopolyhedroviruses: A Neglected Route to Disease?

Abstract

Nucleopolyhedroviruses of lepidopteran larvae (Alphabaculovirus, Baculoviridae) form the basis for effective and highly selective biological insecticides for the control of caterpillar pests of greenhouse and field crops and forests. Horizontal transmission is usually achieved following the release of large quantities of viral occlusion bodies (OBs) from virus-killed insects. In the present review, I examine the evidence for productive midgut infection in different host species and the resulting transmission through the release of OBs in the feces (frass) of the host. This has been a neglected aspect of virus transmission since it was initially studied over six decades ago. The different host-virus pathosystems vary markedly in the quantity of OBs released in feces and in their ability to contaminate the host's food plant. The release of fecal OBs tends to increase over time as the infection progresses. Although based on a small number of studies, the prevalence of transmission of fecal inoculum is comparable with that of recognized alternative routes for transmission and dissemination, such as cannibalism and interactions with predators and parasitoids. Finally, I outline a series of predictions that would affect the importance of OBs in feces as a source of inoculum in the environment and which could form the basis for future lines of research.

Keywords: Alphabaculovirus; Baculoviridae; Lepidoptera; frass; midgut infection.

Figure 1

Virus-induced mortality observed in bioassays of fecal samples collected at different times post-inoculation. The details of each study are provided in Table 1.

Figure 2

Logarithm of the quantities of OBs produced in feces at each sample time point for (A) HypuNPV and (B) SfMNPV in their homologous hosts. The total OB production in feces was obtained by adding the estimated production at each time point over the course of the infection prior to death (Supplemental Tables S1 and S2).

Figure 3

Sodium ascorbate treatment of ODVs resulted in complete loss of activity, whereas treatment of OBs had no significant effect on mortality of Bombyx mori third instars in a laboratory bioassay. Error bars indicate SE. Data on ODVs from experiment 1 (Table 2, 10⁰ dilution) and data on OBs from experiment 4 (Table 3, 10⁻² dilution) in Arakawa [27] (Welch’s t-test, N.S. p > 0.05, ** p = 0.01).

Figure 4

Lepidopteran feces produced when feeding on an artificial diet or plants. (A) Feces produced by Spodoptera frugiperda larva on an artificial diet. (B) Feces of S. frugiperda contaminate the leaf whorl of a maize plant. Feces of S. exigua larvae accumulate in the (C) leaf axil and (D) flower of a sweet pepper plant and (E) over the surface of leaves of a cucumber plant and (F) around the buds of sweet pepper plants.