Sensory flexibility in hawkmoth foraging behavior: lessons from Manduca sexta and other species.

Introduction Neuroethologists wish to understand how animals detect, integrate and perceive sensory stimuli relevant to complex behaviors, and how such processes are modified by physiological state and experience. The tobacco hornworm moth (Manduca sexta) is an excellent model organism for these purposes, due to its large size, rapid generation time and well-defined adult behaviors. Upwind-flight to sex phero-mone (males), oviposition on appropriate hostplants (females) and feeding on floral nectar (both sexes) all require both olfaction and vision (Willis and Arbas, 1991). Although these behaviors feature sequences of stereotyped events, recent studies indicate plasticity in responses to critical sensory stimuli, depending upon the context in which they are perceived. Here we outline three themes of sensory flexibility or variation in hawkmoth behavior: (i) phyloge-netic shifts in feeding niche, (ii) spatial and temporal scale of signal presentation and (iii) task specificity and signal redundancy. The diversity of feeding niches and diel activity patterns observed among the >1000 species of hawkmoths suggests that the relative importance of vision and olfaction should vary widely between species. Kitching and Cadiou (2000) suggest that long proboscides and adult feeding are derived conditions in the family Sphingidae. Crepuscular nectar-feeders like M. sexta use olfaction and vision to feed from flowers (Brantjes, 1978; Kawano et al., 1995), whereas diurnal nectar-feeders like Macroglossum stellatarum find flowers using vision alone (Kelber, 1997). Hawkmoths that feed from fermenting sap (Darapsa pholus; Fleming, 1970) or bee honey (Acherontia atropos; Kitching, 2003) must rely heavily on olfactory cues to find food. Finally, species that are active day and night (Hyles lineata) or feed from flowers and rotting fruit (Amphion floridensis) (Raguso and Willis (2003) probably modify their behavior based on light intensity, food availability and prior experience. Thus, inter-specific variation in sensory modality utilization should be expected in the Sphingidae. However, comparing behavior across species requires experimental parameters to be standardized (e.g. Chittka et al., 2001). Daly and Smith (2000) classically conditioned M. sexta to single odorants with sucrose and measured conditioned responses as cibarial pump muscle activity. When released, these moths flew up wind tunnels and extended their probosces to the conditioned stimulus (K.C. Daly et al., unpublished data). Conversely, Kelber et al. (2003) showed with operant conditioning that Deilephila elpenor and Hyles lineata learn to probe at scentless colored targets associated with sugar rewards. Differences in experimental conditions and learning paradigms limit the extent to which the relative importance of olfactory …