Abstract
BackgroundEntomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors. Although EPNs have been successfully commercialized for pest control, their efficacy in the field is often inconsistent for reasons that remain elusive. EPN infective juveniles (IJs) actively search for hosts to infect using a diverse array of host-emitted odorants. Here we investigate whether their host-seeking behavior is subject to context-dependent modulation.ResultsWe find that EPN IJs exhibit extreme plasticity of olfactory behavior as a function of cultivation temperature. Many odorants that are attractive for IJs grown at lower temperatures are repulsive for IJs grown at higher temperatures and vice versa. Temperature-induced changes in olfactory preferences occur gradually over the course of days to weeks and are reversible. Similar changes in olfactory behavior occur in some EPNs as a function of IJ age. EPNs also show temperature-dependent changes in their host-seeking strategy: IJs cultured at lower temperatures appear to more actively cruise for hosts than IJs cultured at higher temperatures. Furthermore, we find that the skin-penetrating rat parasite Strongyloides ratti also shows temperature-dependent changes in olfactory behavior, demonstrating that such changes occur in mammalian-parasitic nematodes.ConclusionsIJs are developmentally arrested and long-lived, often surviving in the environment through multiple seasonal temperature changes. Temperature-dependent modulation of behavior may enable IJs to optimize host seeking in response to changing environmental conditions, and may play a previously unrecognized role in shaping the interactions of both beneficial and harmful parasitic nematodes with their hosts.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0259-0) contains supplementary material, which is available to authorized users.
Highlights
Entomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors
Temperature and age often vary during commercial application of EPNs, and our results suggest that this variability will cause changes in host-seeking behavior that may alter the efficacy of EPNs as biocontrol agents
Steinernema carpocapsae olfactory responses are modulated by temperature We first examined the olfactory behavior of Steinernema carpocapsae, an EPN with a broad geographical distribution a Life cycle of EPNs
Summary
Entomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors. The widespread use of chemical insecticides in agriculture is a growing health and ecological concern, with an increasing number of studies revealing detrimental effects on organisms such as non-pest insects, aquatic animals, and humans [1,2,3,4]. Entomopathogenic nematodes (EPNs) of the genera Steinernema and Heterorhabditis are lethal parasites of insects that are used throughout the world as biocontrol agents for insect pests [9]. EPNs offer a number of advantages as biocontrol agents – they are found on all continents except Antarctica and are considered non-invasive [10], kill a wide variety of insect agricultural pests [11], are amenable to low-cost mass production [12], and are considered safe to humans and the environment [13]. A number of variables have been found to influence their effectiveness, including temperature, humidity, soil type, and timing of
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