The hungry caterpillar: an analysis of how carbohydrates stimulate feeding in Manduca sexta.

In most insects, the taste of carbohydrates stimulates an immediate appetitive response. The caterpillar of Manduca sexta is an exception to this general pattern. Despite eliciting a strong peripheral gustatory response, high concentrations of carbohydrates (e.g. glucose or inositol) stimulate the same intensity of biting as water during 2-min tests. We suspected that the lack of feeding stimulation reflected the fact that prior studies used single carbohydrates (e.g. sucrose), which M. sexta would rarely encounter in its host plants. We hypothesized that the feeding control system of M. sexta responds selectively to carbohydrate mixtures. To test this hypothesis, we ran three experiments. First, we stimulated the two taste sensilla that respond to carbohydrates (the lateral and medial styloconic) with a battery of carbohydrates. These sensilla responded exclusively to sucrose, glucose and inositol. Second, we determined the response properties of the carbohydrate-sensitive taste cells within both sensilla. We found that one class of carbohydrate-sensitive taste cell responded to sucrose, and two other classes each responded to glucose and inositol. Third, we examined the initial biting responses of caterpillars to disks treated with solutions containing single carbohydrates (sucrose, glucose or inositol) or binary mixtures of these carbohydrates. The only solutions that stimulated sustained biting were those that activated all three classes of taste cell (i.e. sucrose+inositol or sucrose+glucose). We propose that the brain of M. sexta monitors input from the different classes of carbohydrate-sensitive taste cell, and generates protracted feeding responses only when all three classes are activated.