The roles of vision and antennal mechanoreception in hawkmoth flight control
- Lund University, Sweden
- Tata Institute of Fundamental Research, India
Figures
Figure 1 with 1 supplement
Flight control in hawkmoths requires vision and mechanosensation.
(A) Flight control in insects requires sensory feedback on perturbations of body position. The visual system supplies such feedback, but with comparably long response latencies. In addition, insects …
Figure 1—figure supplement 1
Antennal surgery.
To obtain flagella ablated animals, the flagella were cut between the 5th and 10th annulus (red arrows in middle panel). The flagella were preserved and re-attached to the same individual with a …
Figure 2 with 2 supplements
Flagella ablated hawkmoths showed greater thorax and abdomen movements during hovering flight at a stationary flower.
(A) When hawkmoths hovered in front of a stationary flower at 3000 lux, it was notable that flagella ablated moths jittered around their target position with larger amplitudes than moths of the …
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Figure 2—source data 1
Contains the source data for the frequency spectra shown in Figure 2 and Figure 2—figure supplement 2.
- https://doi.org/10.7554/eLife.37606.008
Figure 2—figure supplement 1
Hawkmoth flower approach.
Flight tracks of hawkmoths approaching a stationary flower in bright (A, 3000 lux) and dim (B, 30 lux) light. Before refers to time intervals before their proboscis made contact with the nectary of …
Figure 2—figure supplement 2
Flagella ablated hawkmoths performed less stable hovering at a stationary flower at 30 lux.
Thorax (A) and abdomen (B) position of hawkmoths hovering in front of a stationary flower at 30 lux. Post-hoc tests were performed as part of a general linear model including antennal treatment and …
Figure 3 with 4 supplements
Flagella ablated hawkmoths showed reduced tracking performance of flowers moving at high frequencies.
(A, C) Trajectories of hawkmoths tracking moving flowers with the sum-of-sines (A) and the chirp (C) stimulus. Trajectories of the different antennal conditions are stacked for comparability. When …
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Figure 3—source data 1
Contains the source data for the original traces of flower and moth for all moving flower experiments shown in Figure 3, and further analyzed in Figure 4A,B and Figure 3—figure supplements 1,3,4.
- https://doi.org/10.7554/eLife.37606.014
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Figure 3—source data 2
Contains the source data complex valued responses of moths tracking the sum-of-sines stimulus shown in Figure 3 and Figure 3—figure supplement 1.
- https://doi.org/10.7554/eLife.37606.015
Figure 3—figure supplement 1
Hawkmoth tracking performance with the sum-of-sines stimulus in bright and dim light.
Tracking error (A–C), gain (D–F) and phase (G–I) of hawkmoths tracking a moving robotic flower which moved as a sum-of-sines (see Materials and methods) at 3000 and 30 lux. Curves show the mean and …
Figure 3—figure supplement 2
Frequency analysis of sum-of-sines stimulus tracking performance.
(A, C) Amplitude spectrum of the flight tracks (colours) while following the sum-of-sines stimulus (black). (B,C) Cross power spectral density of the moth tracks and the stimulus. (E,F) Cross …
Figure 3—figure supplement 3
Frequency analysis of chirp stimulus tracking performance.
(A, C) Amplitude spectrum of the flight tracks (colours) while following the chirp stimulus (black). (B,C) Cross power spectral density of the moth tracks and the chirp stimulus. (E,F) Cross …
Figure 3—figure supplement 4
Flower tracking performance with chirp stimuli in dim light.
Comparison of the temporal frequency of the flower at which the moths aborted tracking across antennal treatments at 30 lux. A Friedman test was used to compare between the treatments (***p<0.001, …
Figure 4
Light intensity had the same effect on all antennal treatments.
To test the effect of visual feedback and its possible interaction with antennal mechanosensory feedback on flower tracking, we performed all experiments both in bright (3000 lux) and dim (30 lux) …
Author response image 1
Author response image 2
Tables
Table 1
Proportion of hawkmoths performing specific behaviours across antennal conditions and light intensities.
Proportion of trials in which animals performed the following behaviours: no flight, flight (but no tracking of the flower), tracking. This dataset is based on the animals participating in the …
| Control | Ablated | Reattach | ||
|---|---|---|---|---|
| bright | No flight | 0.03 | 0.11 | 0.05 |
| Flight | 0.15 | 0.29 | 0.1 | |
| Tracking | 0.82 | 0.60 *** | 0.85 | |
| Total | 38 | 42 | 20 | |
| dim *** | No flight | 0.03 | 0.34 | 0.08 |
| Flight | 0.09 | 0.30 | 0.08 | |
| Tracking | 0.88 | 0.36 *** | 0.84 | |
| Total | 35 | 66 | 25 |
Additional files
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Source data 1
Contains the ‘sum-of-sines’ and ‘chirp’ stimulus used in this study as MATLAB arrays, as well as MATLAB scripts to generate the stimuli.
- https://doi.org/10.7554/eLife.37606.017
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Supplementary file 1
Results of the statistical models assessing the effect of antennal treatment and light intensity on the proportion of different behaviours in the flight cages.
The behaviour of each animal was classified into the following categories: no flight, flight (but no tracking of the flower), and tracking. Some moths were tested multiple times to collect the necessary tracking data, and thus have contributed multiple trials to this dataset. Statistical comparisons were performed using multinomial regression including the identity of individual moths as a random factor, to model the rates of one of the three behaviours as a function of antennal condition and lighting. As no significant interaction between antennal condition and light intensity was found, the fixed effects of the fitted model took the form: behavioural category (no flight, flight, tracking)~antennal condition+light intensity. All statistical results are expressed in relation to the probability of observing the no flight behaviour in the control condition in bright light.
- https://doi.org/10.7554/eLife.37606.018
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Supplementary file 2
Results of the statistical models assessing the effect of antennal treatment on thorax jitter in the stationary experiment in bright light (Figure 2B).
A general linear model was constructed with antennal treatment and frequency (binned to the logarithmic scale) as factors: log(response)~antennal condition * frequency +1|individual.
- https://doi.org/10.7554/eLife.37606.019
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Supplementary file 3
Results of the statistical models assessing the effect of antennal treatment on abdomen jitter in the stationary experiment in bright light (Figure 2C).
A general linear model was constructed with antennal treatment and frequency (binned to the logarithmic scale) as factors: log(response)~antennal condition * frequency +1|individual.
- https://doi.org/10.7554/eLife.37606.020
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Supplementary file 4
Results of the statistical model assessing the effect of antennal treatment on flower tracking performance with the sum-of-sines stimulus in bright light (Figure 3B): a general linear model was constructed with antennal treatment and frequency (binned to the logarithmic scale) as factors: log(response)~antennal condition * frequency +1|individual.
- https://doi.org/10.7554/eLife.37606.023
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Supplementary file 5
Results of the statistical model assessing the effect of antennal treatment on flower tracking performance with the chirp stimulus in bright light (Figure 3D): a Friedman test was performed, with a Tukey-Kramer post-hoc comparison correction for multiple comparisons.
- https://doi.org/10.7554/eLife.37606.024
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Supplementary file 6
Results of the statistical model assessing the effect of antennal condition on the difference in flower tracking error between light conditions with the chirp stimulus (Figure 4B).
A Friedman test was performed, with a Tukey-Kramer post-hoc comparison correction for multiple comparisons.
- https://doi.org/10.7554/eLife.37606.028
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Supplementary file 7
Results of the statistical model assessing the effect of antennal condition on the difference in thorax stability during hovering between light conditions (Figure 4C).
A Friedman test was performed, with a Tukey-Kramer post-hoc comparison correction for multiple comparisons.
- https://doi.org/10.7554/eLife.37606.029
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Supplementary file 8
Results of the statistical model assessing the effect of antennal condition on the difference in flower tracking error between light conditions with the sum-of-sines stimulus (Figure 4A).
A Friedman test was performed, with a Tukey-Kramer post-hoc comparison correction for multiple comparisons.
- https://doi.org/10.7554/eLife.37606.027
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Supplementary file 9
Results of the statistical models assessing the effect of antennal treatment on thorax jitter in the stationary experiment in dim light (Figure 2—figure supplement 2A).
A general linear model was constructed with antennal treatment and frequency (binned to the logarithmic scale) as factors: log(response)~antennal condition * frequency +1|individual.
- https://doi.org/10.7554/eLife.37606.021
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Supplementary file 10
Results of the statistical models assessing the effect of antennal treatment on abdomen jitter in the stationary experiment in dim light (Figure 2—figure supplement 2B).
A general linear model was constructed with antennal treatment and frequency (binned to the logarithmic scale) as factors: log(response)~antennal condition * frequency +1|individual.
- https://doi.org/10.7554/eLife.37606.022
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Supplementary file 11
Results of the statistical model assessing the effect of antennal treatment on flower tracking performance with the sum-of-sines stimulus in dim light (Figure 3—figure supplement 1): a general linear model was constructed with antennal treatment and frequency (binned to the logarithmic scale) as factors: log(response)~antennal condition * frequency +1|individual.
- https://doi.org/10.7554/eLife.37606.025
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Supplementary file 12
Results of the statistical model assessing the effect of antennal treatment on flower tracking performance with the chirp stimulus in dim light (Figure 3—figure supplement 4): a Friedman test was performed, with a Tukey-Kramer post-hoc comparison correction for multiple comparisons.
- https://doi.org/10.7554/eLife.37606.026
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Supplementary file 13
Results of the statistical model assessing the effect of antennal condition on the difference in abdomen stability during hovering between light conditions (Figure 4D).
A Friedman test was performed, with a Tukey-Kramer post-hoc comparison correction for multiple comparisons.
- https://doi.org/10.7554/eLife.37606.030
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Transparent reporting form
- https://doi.org/10.7554/eLife.37606.031
