Preferential infectivity of entomopathogenic nematodes in an envenomed host

Authors: MBATA, GEORGE - Fort Valley State University; Shapiro Ilan, David; Alborn, Hans; STRAND, MICHAEL - University Of Georgia

Submitted to: International Journal for Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/22/2019
Publication Date: 8/1/2019
Citation: Mbata, G., Shapiro Ilan, D.I., Alborn, H.T., Strand, M. 2019. Preferential infectivity of entomopathogenic nematodes in an envenomed host. International Journal for Parasitology. 49(9):737-745. https://doi.org/10.1016/j.ijpara.2019.05.002.
DOI: https://doi.org/10.1016/j.ijpara.2019.05.002

Interpretive Summary: Indian meal moths are common pests of stored grains. Entomopathogenic nematodes (also called beneficial nematodes) and parasitic wasps attack Indian meal moth larvae. The beneficial nematodes and wasps may be used as natural pest control agents. When the wasps sting the Indian meal moth larvae, they inject venom that causes paralysis. In previous research, we discovered that the nematodes preferentially infect Indian meal moth larvae that were envenomed (stung) by the wasps; if the nematodes are given a choice between envenomed larvae versus non-envenomed larvae, they choose the envenomed larvae. However, we did not know why the nematodes choose the stung larvae. In the current study, we explored mechanisms to explain why the nematodes prefer the envenomed larvae. Mechanisms differed between two species (two kinds) of nematodes. In one case, paralysis of the envenomed insect host was the causal factor – the nematodes prefer the envenomed host simply because it cannot escape. This may be akin to wolves taking down the wounded caribou (easier prey). For the other nematode species, a chemical compound that is released by envenomed Indian meal moth larvae induces infection – the chemical apparently attracts the nematodes to the envenomed insect and so the nematodes choose the stung larvae over larvae that are not stung. These findings build a foundation for additional studies on why parasites prefer one host over another.

Technical Abstract: Entomopathogenic nematodes and parasitoid wasps are used as biological control agents for management of insect pests like the Indian meal moth, Plodia interpunctella. The parasitoid wasp Habrobracon hebetor injects a paralytic venom into P. interpunctella larvae before laying eggs. A previous study reported that the entomopathogenic nematode Heterorhabditis indica preferentially infects P. interpunctella that have been envenomed by H. hebetor while results in this study showed a similar preference by the entomopathogenic nematode, Steinernema glaseri. We therefore tested four hypotheses for why nematode infection rates are higher in envenomed hosts: 1) elevated CO2 emission from envenomed hosts attracts nematodes, 2) paralysis prevents hosts from escaping nematodes, 3) volatile chemicals emitted from envenomed hosts attract nematodes and increases infection, and 4) reduced immune defenses in envenomed hosts increases nematode survival. Results showed that envenomed P. interpunctella larvae emitted lower amounts of CO2 than non-envenomed larvae. Physical immobilization of P. interpunctella larvae did not increase infection rates by S. glaseri but did increase infection rates by H. indica. Emissions from envenomed hosts were collected and analyzed by thermal desorption gas chromatography/mass spectrometry. The most abundant compound, 3-methyl-3-buten-1-ol (3-mpethyl-3-buten-1-ol) was found to be an effective cue for S. glaseri attraction and infection but was not an effective stimulus for H. indica. Envenomed P. interpunctella exhibited a stronger immune response toward nematodes than non-envenomed hosts. Altogether, we conclude that different mechanisms underlie preferential infection in the two nematode species: host immobilization for H. indica and chemical cues for S. glaseri.