Abstract

Animals explore their environment to encounter suitable food resources. Despite its vital importance, this behavior puts individuals at risk by consuming limited internal energy during locomotion. We have developed a novel assay to investigate how food-search behavior is organized in Drosophila melanogaster larvae dwelling in hydrogels mimicking their natural habitat. We define three main behavioral modes: resting at the gel's surface, digging while feeding near the surface, and apneic dives. In unstimulated conditions, larvae spend most of their time digging. By contrast, deep and long exploratory dives are promoted by olfactory stimulations. Hypoxia and chemical repellents impair diving. We report remarkable differences in the dig-and-dive behavior of D. melanogaster and the fruit-pest D. suzukii. The present paradigm offers an opportunity to study how sensory and physiological cues are integrated to balance the limitations of dwelling in imperfect environmental conditions and the risks associated with searching for potentially more favorable conditions.

Highlights

  • The natural habitats populated by individual species of the Drosophila group comprise a wide range of food resources ranging from fermenting fruits to vegetables (Hansson and Stensmyr, 2011)

  • Our results indicate that D. suzukii undergo a transient attractive response to the food-odor ethyl acetate in the dig-and-dive assay

  • While larval orientation behavior has been extensively examined on planar surfaces in response to stable airborne odor gradients (Louis et al, 2008; Gershow et al, 2012), larvae live in complex tridimensional hydrogel structures formed by fruits and decaying organic materials

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Summary

Introduction

The natural habitats populated by individual species of the Drosophila group comprise a wide range of food resources ranging from fermenting fruits to vegetables (Hansson and Stensmyr, 2011). Most of the substrates where larvae grow are characterized by soft semiliquid structures similar to hydrogels. When placed on a slice of fresh tomato, D. melanogaster larvae readily locate the soft middle layer of the fruit, called the locular gel, and dig into it (Figure 1A and A’). Not surprisingly, digging takes place when the softness of low-density-agarose gels is similar to the natural habitats of Drosophila melanogaster (for stiffness measurements related to tomato pulp, see Grant et al, 2012; Li et al, 2012). As nutritional and pH conditions vary along the depth of a fruit, exploratory dives permit larvae to search for conditions that satisfy their metabolic and physiological needs

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