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First published online March 31, 2007
Journal of Experimental Biology 210, 1398-1405 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02752
The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta
1 Department of Biological Sciences, Coker Life Sciences Building, 700
Sumter Street, University of South Carolina, Columbia, SC 29208,
USA
2 Oberlin College, Oberlin, OH 44074, USA
* Author for correspondence (e-mail: jgoyret{at}biol.sc.edu)
Accepted 12 February 2007
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Summary |
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Key words: olfactory stimulus, sensory stimulus, temporal pattern, spatial pattern, temporal decoupling, hawkmoth
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Introduction |
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). In
goal-seeking tasks such as close-range searching, where effective stimuli are
often emitted by the target (e.g. food, shelter, hosts), multiple sensory
inputs provide animals with several advantages, including behaviorally
flexible `contingency plans' conferred by redundant inputs
(Brantjes, 1978;
Raguso, 2004). Another
advantage of multi-modal communication is the reinforcement of highly
specialized information content, such as host-specificity or flower constancy,
due to the integration of sensory modalities
(Gegear, 2005;
Hebets and Papaj, 2005). For
example, cabbage moths (Mamestra brassicae) orient more frequently to
the combination of visual and olfactory host-plant cues than to either cue
presented alone (Rojas and Wyatt,
1999). Diachasmimorpha longicaudata, the hymenopteran
parasitoids of tephritid fruit flies, show different responses when stimulated
by different fruit signals in a wind tunnel, landing 5-fold more often on
appropriately scented visual targets than on odorless guava fruit models
(Jang et al., 2000).
Björklund et al. found similar, but in this case additive, effects when
using visual and olfactory cues from conifer seedlings to attract the pine
weevil Hylobius abietis
(Björklund et al., 2005).
Thus, stimulation of more than one sensory system can elicit additive as well
as synergistic responses (see Raguso and
Willis, 2002).
The interplay between olfactory and visual cues is known to mediate the
sequence of feeding behaviors (i.e. from flower approach to proboscis
extension) of several species of moths
(Brantjes, 1978;
Naumann et al., 1990;
Raguso and Willis, 2002) and
butterflies (Tinbergen, 1958;
Andersson and Dobson, 2003;
Omura and Honda, 2005), but
little is known about how these substantially different sensory systems
interact during the decision-making process(es) of foraging lepidopterans. The
butterfly Vanessa indica is more attracted to scented than to
unscented paper flowers when their color is relatively unattractive (e.g.
purple), but prefers unscented yellow flower models over scented purple flower
models in choice tests (Omura and Honda,
2005). The innate attraction of these butterflies to yellow is
stronger than their attraction to a scented but unattractive colored flower
model. Balkenius and Kelber documented a similar sensory bias in a study of
odor learning by the diurnal hawkmoth Macroglossum stellatarum
(Balkenius and Kelber, 2006),
which shows appetitive conditioning to sugar-rewarded odors associated with
unattractive flower colors (e.g. yellow) but cannot learn to distinguish
between differently scented blue flowers, which they innately prefer. These
authors (Balkenius et al.,
2006) have shown that the ecology of the animal is an important
factor regarding the weight given to the different sensory cues. Thus, the
nocturnal hawkmoth Deilephila elpenor responds preferentially to
floral scent over visual targets in choice assays within a wind tunnel, but
the diurnal M. stellatarum shows the converse preference for visual
stimuli. However, it is also possible that the feeding response of D.
elpenor is odor guided because these moths also feed from fermented fruit
and sap without strong visual contrast
(Newman, 1965). These studies
indicate that Lepidoptera generally use multi-modal sensory inputs during
nectar foraging but that the integration of such cues may be complex and
hierarchical.
Manduca sexta, a crepuscular, nectar-feeding hawkmoth native to
the Americas, has been well studied as a model system for flight energetics
and biomechanics (Tu and Daniel,
2004), visual and olfactory neurophysiology and development
(White et al., 2003;
Reisenman et al., 2005). These
moths are known to be attracted by a range of sensory stimuli, including
floral odors and visual display (Brantjes,
1978; Raguso and Willis,
2002; Raguso and Willis,
2005), water vapor (Raguso et
al., 2005), carbon dioxide
(Thom et al., 2004) and
hostplant volatiles (Mechaber et al.,
2002). Behavioral events associated with foraging are released by
an apparently synergistic interplay between olfactory and visual cues, such
that the combined signal elicits proboscis extension (while hovering) in both
naïve and wild M. sexta
(Raguso and Willis, 2002;
Raguso and Willis, 2005). In
these studies, M. sexta moths approached either visual targets or
odor sources, but only extended their proboscides towards a visual target when
olfactory cues were present. These authors concluded that odor and visual cues
were both needed for feeding by M. sexta, but could not distinguish
between an odor-gated visual approach and simultaneous olfactory–visual
stimulation of feeding. Are these sensory inputs perceived as a single
composite signal with an enhanced predictive value for a nectar source, or
does odor `activate' a visually guided search behavior?
In previous studies of feeding behavior by M. sexta and other Lepidoptera, experimental manipulation was limited to the presence or absence of visual and/or olfactory floral stimuli, and thus was insufficient to acquire fine-scale information on how the integration of olfactory and visual signals affects foraging decisions. For example, visual contact with flower targets can be temporarily obstructed, and olfactory stimulation can be intermittently affected by wind turbulence in the natural environments in which hawkmoths forage for nectar (see Eisikowitz and Galil, 1971). Thus, in the present work, we address an important gap in studies of lepidopteran foraging behavior by spatially and temporally manipulating the presentation of visual and olfactory stimuli to naïve M. sexta moths.
In the first experiment, we spatially decoupled the presentation of olfactory and visual stimuli in a laminar flow wind tunnel, by creating an odor plume and a visual target (artificial flower) separated by different incremental distances. We used this design to test the following hypotheses:
In the second experiment, we temporally decoupled olfactory and visual stimuli by presenting moths with a discrete odor puff at different times in the presence of an odorless visual target. In each manipulation, we quantitatively evaluated the moths' decisions to probe at a visual target or not, contrasting the following hypotheses:
;
Knoll, 1926) and Brantjes
(Brantjes, 1978)]. In the third experiment, we challenged moths to choose between the visual target and the odor source separated by 40 cm, to determine whether they show an innate bias for either modality at the final stage of the searching behavior (i.e. probing):
); Our results are discussed in the framework of multi-modal sensory usage by foraging M. sexta and other Lepidoptera.
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Materials and methods |
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Animals
We used 3–5-day-old Manduca sexta L. adults reared from eggs
provided by Dr Lynn Riddiford, University of Washington, Seattle, WA, USA.
Larvae were fed ad libitum on an artificial diet
(Bell and Joachim, 1976) and
were kept as pupae under a 16 h:8 h light:dark, 24:21°C cycle. Moths were
separated by sex as pupae and were housed in different incubators (Precision
818; Winchester, VA, USA) under the same ambient regime and emerged within
45x45x45 cm screen cages (BioQuip, Inc., Rancho Dominguez, CA,
USA). Adults were starved for 3–4 days before being used in experiments
to increase their appetitive motivation.
General procedure in the wind tunnel and recorded variables
At the beginning of scotophase (15:00 h), the naïve, starved adult
moths were placed individually at the downwind end of a 3x1.5x1.5
m laminar flow wind tunnel, with a flow rate of 1 m s–1. Each
moth was allowed to fly freely inside the wind tunnel for 5 min, during which
its behavior was recorded. In experiments 1 and 2, we recorded whether or not
moths approached (i.e. hovered in front of) and probed an artificial flower at
least once with their extended proboscides. Both variables were expressed as
proportions of the number of animals flown in each treatment. We also recorded
the amount of time (approach time, in s) during which moths flew inside the
tunnel before probing the artificial flower. In experiment 3 (choice
experiment; see below), we recorded the proportions of moths that probed on
the artificial flower (visual stimulus) vs the odor source as their
initial response when these stimuli were spatially decoupled. We also recorded
the total number of choices and total time probing (s) at each stimulus, as
well as the latency (time elapsed before the first choice, in s).
Sensory stimuli
A cotton swab was soaked with 25 µl of bergamot essential oil (Body
Shop, Columbia, SC, USA) for each experimental trial that included an
olfactory stimulus and was refreshed every 15 min in order to maintain odor
intensity. This odor source is a reliable feeding stimulant for M.
sexta (Goyret and Raguso,
2006) and, like many night-blooming flowers visited by this
species, is dominated by linalool and related monoterpenoid odors (see
Raguso and Pichersky, 1999).
The wooden stem of the swab (2.5 cm) was affixed to a 3 cm3 piece
of dark gray modeling clay at a 45° angle to the black ring stand and 1 cm
below the flower. In the treatments testing visual cues without odor, a
scentless cotton swab was affixed to the ring stand to present the same amount
of visual contrast.
The visual stimulus consisted of a white artificial flower with a paper perianth (9 cm in diameter; no reward was present) positioned on the vertical ring stand at a height of 50 cm against a black background. Spectrophotometer readings of flowers (not shown) revealed that the paper absorbed UV wavelengths but reflected light nearly uniformly from 400 to 700 nm. Volatile analysis (not shown) using solid phase microextraction combined with gas chromatography–mass spectrometry revealed that the artificial flower did not emit volatile compounds. In the treatments without a white flower, we constructed a black flower to control for turbulence effects on the odor plume. White and red tungsten lamps were positioned above the wind tunnel, providing diffuse illumination through a white cotton sheet (see below).
Experiment 1: spatial decoupling of visual and olfactory cues
We manipulated the presence and relative position of olfactory and visual
stimuli at the upwind end of the tunnel (see
Table 1 for treatment summary).
In the first four treatments, by moving the artificial flower to the right or
left of the centrally positioned odor source
(Fig. 1), we wished to observe
whether probing behavior varies with increasing distance between stimuli. The
fifth and sixth treatments allowed us to compare responses when only one
stimulus was present. The seventh treatment was designed to measure baseline
responses by the moths to the ancillary structures utilized in the other
treatments (ring stand, cotton swab and tape). Light intensity measured within
the wind tunnel ranged from 0.011 lx to 0.023 lx (approximate conditions of a
bright starlit night).
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Experiment 2: temporal decoupling of visual and olfactory cues
Given that the spatial separation of visual and olfactory cues also implies
a non-simultaneous presentation for which we had no control, we designed a
second experiment in which these cues were decoupled temporally. Here, we
always presented the white artificial flower at the upstream end of the wind
tunnel but manipulated the timing of the olfactory stimulation, either before
releasing the moth (downwind puff), during the whole trial (odor plume) or at
the flower (flower puff) (treatments are summarized in
Table 2). We used a different
set of syringes, tubing and artificial flowers to avoid odor
contamination.
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Compared with pilot experiments, feeding responses in the positive control of experiment 1 were less probable, thus, in this experiment, light intensity was increased to 0.054 lx [approximate conditions of a (half)moonlit night] by the addition of a second white bulb. Increased illumination could affect the conspicuousness of the visual target, but given the positive and negative controls in this experiment, we could still evaluate the effect of the temporal sequence of stimulation (see Discussion).
Experiment 3: stimulus preference in a dual-choice set-up
We performed a choice experiment using the set-up from the `Visual at 40
cm' (O+V@40) treatment of experiment 1. Instead of having the odor source at
the center of the wind tunnel and the flower at 40 cm to its left or right
side, here we randomly placed each stimulus 20 cm apart from the center but in
opposite directions. We analyzed the relative feeding responses towards the
visual display (artificial flower) and odor source (scented cotton swab) with
a larger sample of moths (N=56), to see whether they showed an innate
preference for either the visual or the olfactory stimulus. Light conditions
were set as described above for experiment 1.
Statistical analysis
In experiments 1 and 2, the categorical variables `approach' and `probing'
were analyzed by means of a log-likelihood test (G-test) when testing overall
treatment effects and by using binomial tests when comparing pairs of
proportions (binomial distributions). An 
-level of significance of
0.0045 was adopted for experiment 1 to preserve a global -value of
0.05, because we performed 11 statistical tests on these data. Approach time
was analyzed as a continuous dependent variable using one-way analysis of
variance (ANOVA) (with treatments as factors – see
Table 1) because data met the
assumptions of this test, and an orthogonal a priori comparison was
performed (positive control vs treatments with spatially separated
stimuli – 10, 20 and 40 cm apart).
In experiment 2, mean ranks of `approach time' data were analyzed using the Kruskal-Wallis non-parametric test, because the data were refractory to transformation. In experiment 3, the dependent variables `total visits' and `total visit time' were square root and log transformed, respectively, for ANOVA. Finally, initial moth choice was analyzed using the binomial test with the null hypothesis of equal attraction to olfactory and visual stimuli [P(odor source)=P(visual target)=0.5].
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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=0.0045; see Materials and
methods) (Fig. 2A).
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Analysis of variance of Approach time showed a marginally non-significant effect of treatment (F5,56=2.35, P=0.055) (Fig. 2B), but the a priori comparison showed that the mean approach time to the flower in the positive control (55 s) was significantly shorter (by half) than the approach time when the artificial flower was spatially separated from the odor source (10, 20 and 40 cm treatments; mean approach time=114.67 s; F1,42=6.99, P=0.01) (Fig. 2B).
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Experiment 3: stimulus preference in a dual-choice set-up
Slightly more than half (55%) of all experimental moths responded by
approaching and probing the test stimuli, with 94% of the first choices to the
visual target and only 6% of first choices to the odor source. These
proportions differed significantly (P<0.0001, N=33;
binomial test) (Fig. 4A). When
all probing events for each moth were evaluated, we found that 61% probed only
the visual target, 3% probed only the odor source and 36% probed both stimuli
(N=33) (Fig. 4B). When
we analyzed total number of probes to the visual target (3.41±0.49) and
to the odor source (1.62±0.16), we found significant differences
between means (F1,43=5.60, P=0.023; ANOVA with
square root transformation). We also analyzed total visit time and found that
moths spent more time probing the visual target (43.56±10.54 s) than
the odor source (10.85±3.52 s; F1,43=4.65,
P=0.037; ANOVA with log transformation).
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Discussion |
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Of course, the threshold distances defined in our study are relevant only
to the laminar flow wind tunnel, which is designed to reduce or eliminate
turbulence (Willis and Arbas,
1991; Vickers,
2000). Floral scent plumes are unlikely to indicate point sources
in natural blooming populations and are likely to show turbulence and complex
three-dimensional structure (Murlis et
al., 1992). Manipulative experiments in which the visual and
olfactory floral cues of Datura wrightii were decoupled
(Raguso and Willis, 2005)
showed that the spatial threshold of visual–olfactory synergism for wild
M. sexta foraging in open desert environments is on the scale of
meters, rather than centimeters. Taken together, these studies demonstrate the
contextual importance of odor in the perception of bright visual targets as
nectar sources by M. sexta.
Temporal decoupling of olfactory and visual cues
In experiment 2, we temporally decoupled olfactory and visual stimulation
to determine whether simultaneous perception of both modalities is
necessary to trigger the probing response with high probabilities
(Hypothesis2A; see Introduction). The alternative view, described
by Brantjes (Brantjes, 1973)
and implied by Knoll (Knoll,
1922; Knoll,
1926), is that odor `gates' or releases a sequence of visually
guided feeding behaviors, for which odor is superfluous
(Hypothesis2B; see Introduction). Instead of rejecting either of
these hypotheses, our results lead us to provisionally accept both, which
indicates that they are not mutually exclusive. Indeed, we have observed an
unexpected flexibility in feeding behavior by M. sexta, such that
olfactory stimulation before, during or after visual stimulation is sufficient
to elicit probing. Thus, an odor plume can guide a moth to its source (the
flower) when sustained, but it also can increase a moth's responsiveness to a
visual target when transient (see below). Moths that approached the visual
target in the absence of odor showed very low probabilities of proboscis
extension, but this behavior could be reversed by a transient odor puff
administered as moths hovered in front of the flower model
(Fig. 3A). Such responses
increased probing probability to the levels of the positive control, where
moths could be guided by both olfactory and visual inputs. These results
support the hypothesis that simultaneous visual and olfactory stimulation has
the highest probability of triggering proboscis extension
(Hypothesis2A). Nevertheless, odor-gated visual foraging can occur
in M. sexta, increasing responsiveness of naïve moths above that
occurring in the absence of odor (Hypothesis2B;
Fig. 3A). Transient
presentation of the olfactory stimulus before flight led to longer latencies
(Fig. 3B), which behaviorally
could be explained by a repetitive up- and downwind, looping flight pattern
observed solely under this treatment. Unfortunately, we did not record flight
tracks to quantify this flight behavior, which differs fundamentally from the
upwind casting flight tracks limited to the vertical plane of a continuous
odor plume, as shown by Raguso and Willis
(Raguso and Willis, 2003). As
described by Brantjes (Brantjes,
1973), olfactory stimulation appears to `arrest' moths into an
odor-plume search and at the same time increases the chances of probing upon
encounter with a visual target (Fig.
3A).
Choosing between olfactory and visual signals of a flower
In experiment 3, we forced moths to choose between decoupled visual and
olfactory floral cues, providing a distinct test of the necessity for
concomitance of stimuli and addressing the potential for sensory hierarchies
observed by Omura and Honda (Ômura
and Honda, 2005) and Balkenius and Kelber
(Balkenius and Kelber, 2006)
for other nectar-feeding Lepidoptera. We found that first visits by M.
sexta overwhelmingly favored the visual target over the odor source
(Fig. 4A), suggesting that
Hypothesis3A should be rejected in favor of Hypothesis3B
(see Introduction). Balkenius et al. used a wind tunnel to perform similar
experiments with two nectar-feeding European hawkmoth species
(Balkenius et al., 2006). In
their study, M. stellatarum, a diurnal hawkmoth species, approached a
visual target instead of an odor source, while the nocturnal D.
elpenor more frequently approached the odor source. M.
stellatarum can feed on scentless flower models
(Kelber, 1997), while D.
elpenor has been shown to require olfactory stimulation to feed from
flowers (Brantjes, 1978).
Although few moths in our experiment (6%) probed the odor source first,
nearly 40% of all moths did so at least once during their trial flights
(Fig. 4B), providing additional
evidence that the sensory requirements and preferences of naïve M.
sexta, however strong, are not rigid. The sensory flexibility of foraging
hawkmoths is also apparent in the experimental demonstration that appetitive
conditioning can override or reverse innate sensory preferences
(Kelber, 1996;
Balkenius and Kelber, 2006).
The results of preference experiments are likely to shift as individual moths
gain foraging experience, particularly for hawkmoths that feed from rotting
fruit and sap as well as floral nectar (e.g. Amphion floridensis),
for whom visual cues may be conditionally useful but not essential. Even
M. sexta will feed from a scentless feeder after it has been in the
flight cage for one or two nights (J.G., personal observation). We are now
addressing how quantitative aspects of the visual stimulus, such as color,
size, contrast and light intensity, as well as larval diet quality, could
affect the tendency of M. sexta to probe at the visual target rather
than at the odor source.
Multi-sensory cues in the study of sensory ecology
Our experiments allowed us to identify a non-linear relationship between
visual and olfactory stimuli and nectar feeding behavior in M. sexta.
We also showed that the dynamics of sensory stimulation, besides the
stimulation per se, represent a fundamental component in the
decision-making process of M. sexta. Olfactory–visual
integration appears to be flexible, in the sense that it allows M.
sexta to search and probe under different temporal patterns of
stimulation rather than requiring a prefixed order or concomitance of stimulus
presentation. The diversity of growth forms, floral density and sources of
odor (flowers vs leaves) in plants pollinated by nocturnal hawkmoths
(Haber and Frankie, 1989; Raguso and
Willis, 2005) suggests that wild foraging M. sexta should
encounter variance in the spatial and temporal concomitance of floral visual
displays and odor plumes. Our results show that M. sexta would be
able to identify and feed from flowers under such conditions.
Sensory flexibility, rather than the exception, may prove to be the rule
for opportunistic, generalist flower-feeding animals, especially when foraging
under different photic conditions or when preferred colors or odors are not
available. Recent studies indicate considerable flexibility in the sensory
information used by glossophagine bats
(von Helversen et al., 2000;
von Helversen et al., 2003;
Winter et al., 2003) and
bumblebees (Saleh et al.,
2006) in nectar foraging behavior. Thus, in behavioral studies it
may be more fruitful to address sensory systems as interacting sub-systems
whose properties contribute to an animal's functional relationship with its
environment, rather than as isolated components of their perceptual
apparatus.
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Acknowledgments |
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