Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Sensory Flexibility in Hawkmoth Foraging Behavior: Lessons from Manduca sexta and Other Species
Department of Biological Sciences, University of South Carolina, Columbia SC 29208 USA
Correspondence to be sent to: Robert Raguso, e-mail: raguso{at}biol.sc.edu
Key words: appetitive learning, behavioral sequences, Sphingidae, water balance
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Introduction |
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 Top Introduction Phylogenetic patterns and...Spatial and temporal scale...Task specificity, sensory cues...AcknowledgementsReferences |
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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 pheromone (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) phylogenetic shifts in feeding
niche, (ii) spatial and temporal scale of signal presentation and (iii) task specificity
and signal redundancy. |
Phylogenetic patterns and constraints |
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TopIntroductionPhylogenetic patterns and...Spatial and temporal scale...Task specificity, sensory cues...AcknowledgementsReferences |
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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 and visual inputs to these species can be compared.
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Spatial and temporal scale of signal presentation |
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TopIntroductionPhylogenetic patterns and...Spatial and temporal scale...Task specificity, sensory cues...AcknowledgementsReferences |
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Nectar foraging by hawkmoths involves behavioral responses to sensory inputs at different spatial scales, including distance orientation (>10 m), floral approach (<10 m), and, at a flower’s threshold, proboscis extension and feeding. Raguso and Willis (2003
) summarized
the evidence for hawkmoth upwind flight to flower and fruit odors. Fragrance and visual
contrast synergize floral approach and feeding by lab-reared and wild M. sexta
(Raguso and Willis, 2002, 2005).
Although Knoll’s (1926) classic experiments indicated visual guidance of proboscis
placement by Hyles lineata livornica,
Desai and Raguso (2002) showed that
M. sexta use visual contrast, tactile and gustatory cues to probe for nectar.
Thus, sensory switching by M. sexta during nectar foraging is a consequence of
the flowers’ physical proximity and the sensory information they present.
Temporal components of floral signal presentation also impact
M. sexta’s foraging behavior. All nectar-feeding animals assess the
relative profitability of individual flowers or patches while foraging (Bell, 1986); one problem they encounter is
variance in the correlation between floral signals and reward quality. Post-pollination
fragrance- and color-change are too gradual to reliably indicate nectar absence to
foraging moths in short-lived flowers (Eisikowitch
and Lazar, 1987;
Tollsten, 1993). Do other cues track
nectar availability on the scale of minutes, rather than hours or days? Many
night-blooming flowers show dramatic bud growth preceding anthesis, coupled with
intensive nectar and fragrance production (Raguso
and Willis, 2003). Such metabolic activity predicts the accumulation of
floral CO2, which
Guerenstein et al. (2004)
have confirmed for Datura wrightii, a night-blooming plant favored by M.
sexta as a nectar source in North America’s Sonoran Desert. Most feeding by
M. sexta occurs within the first hour after Datura flowers open, when
repeated moth visits deplete both nectar and CO2 concentrations
(P. Guerenstein, unpublished data). Manduca sexta sensitively detect
CO2 through labial pit organ receptors (Kent et al., 1986), and naïve moths innately
prefer scented paper flowers with 765 p.p.m. CO2 over those with ambient
levels, but preference is not maintained in the absence of nectar (Thom et al., 2004). Thus, floral CO2
may function as an olfactory nectar-guide for M. sexta. It remains unclear
whether CO2 is redundant, complementary or synergistic to other floral cues at
different spatial scales or levels of experience.
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Task specificity, sensory cues and context |
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TopIntroductionPhylogenetic patterns and...Spatial and temporal scale...Task specificity, sensory cues...AcknowledgementsReferences |
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In addition to nectar feeding, M. sexta and other hawkmoths drink water from puddles and flowing streams (Nabokov, 1947
;
Janzen, 1984). These behaviors satisfy
different physiological requirements (flight fuel versus water balance), but both involve
proboscis extension. How might the same behavior (proboscis extension) result from
different combinations of sensory cues? Naïve M. sexta require both visual
and olfactory cues for proboscis extension in a nectar-feeding context, but escaped moths
in the lab probe at faucets above wet sinks, suggesting that humidity and chrome are
super-normal water-surface cues.
We designed a randomized block experiment in which naïve, starved M.
sexta were exposed to an air stream of either dry or humidified air alone or pumped
over a strongly scented Magnolia grandiflora flower, for a total of four
treatments. Moths’ responses were measured to only one stimulus. The null
hypothesis that neither water vapor nor fragrance is sufficient to elicit proboscis
extension was rejected for males (
2 = 9.0, 3 df, P
= 0.02) and females (2 = 8.0, P < 0.05). Water
vapor alone and floral scent with dry air elicited proboscis extension in some cases, but
their combination had an additive (male 2 = 0.62, P >
0.75; female 2 = 1.7, P > 0.5), rather than
synergistic effect (male 2 = 46.05, P < 0.001; female
2 = 43.06, P < 0.001). Perhaps fragrance and water
vapor are functionally redundant cues that remain contextually distinct under field
conditions. Alternatively, moth responses to floral scent may have been artifacts due to
water vapor or CO2 in Magnolia floral headspace. Further experiments
are needed to decouple these cues by either desiccating the fragrant air or using
essential oils with versus without humidified air or CO2.
Here we have focused on sequences of behavioral events that comprise
feeding, but we know much less about the factors that influence the motivational
state that precedes these events (Martin
and Bateson, 1993). A balanced experimental design in which starvation, prior
feeding, age and mating status are manipulated would provide insight into what motivates
moths to respond to the sensory signals that modulate feeding and drinking behavior.
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Acknowledgements |
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TopIntroductionPhylogenetic patterns and...Spatial and temporal scale...Task specificity, sensory cues...AcknowledgementsReferences |
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R.A.R. thanks Drs Mamiko Ozaki and Takashi Yamamoto for inviting him to Kyoto. Drs David Wethey, Richard Vogt and Sarah Woodin generously helped with the wind tunnel, M. sexta colony and departmental support, respectively. Drs Mark Willis, Almut Kelber, Michael Pfaff and the Hildebrand lab contributed to our thinking about moth behavior. Funding was provided by the Howard Hughes Medical Institute, a USC Research and Productive Scholarship grant, and NSF grants DEB-9806840 and DEB-9977047. A.R.L. was supported by NSF grant DBI-9820456 as part of the Undergraduate Research in Integrated Evolutionary Biology program at USC. B.O.S. was supported by the Alexander von Humboldt Foundation, with matching funds from USC.
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