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Luminance-dependent visual processing enables moth flight in low light

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Science  12 Jun 2015:
Vol. 348, Issue 6240, pp. 1245-1248
DOI: 10.1126/science.aaa3042

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  1. Fig. 1 The effect of light intensity on moths tracking robotic flowers.

    (A) Human photoreceptors, like those of all animals, are capable of detecting even single photons (28). However, human color vision (colored arc), as well as our ability to resolve motion and spatial detail, deteriorates below the photopic visual threshold (1 to 10 cd m−2) corresponding to light levels at dusk (11, 29). This is also true for diurnal insects such as the blowfly Calliphora (30). Human scotopic vision (gray arc) is strictly monochromatic (29). The hawkmoth Deilephila is truly nocturnal, with color vision throughout much of the scotopic range (2). [In (A), “*” indicates experimental light levels. “?” indicates that data are not available.] Manduca is crepuscular and is hypothesized to adjust its visual processing (B) in order to visually track flowers over its large range of light intensity (>106 cd m−2) (10, 27). (CNS, central nervous system.) Robotic, three-dimentional printed flowers generated repeatable moth flight maneuvers (C) (movies S1 and S2). We moved the flowers with a trajectory of many superimposed sinewaves to sample many of the frequencies of movement simultaneously (D). Fourier transformations (E and F) of the flower’s (green) and moth’s (blue) movements show high coherence [(E), gray line], which is the normalized cross-power spectral density (18, 24). Flower movements were prescribed to have equal peak velocities at each frequency (F), which helps avoid saturation in the moth’s ability to track.

  2. Fig. 2 Visual processing slows in low light.

    The relative amplitudes of moth and flower give the tracking gain (A), and their relative timing gives the phase difference (B) with means ± 95% confidence intervals (CIs). The qualitative shape of the response is consistent with the drift-compensation response in the diurnal hawkmoth Macroglossum (8). Regressing phase onto frequency [(B), dash-dotted lines] estimates the best-fit time constant across all frequencies (C) or just those <10 Hz (D). We created a prediction for the low-luminance response (light blue) from a closed-loop model of the high-luminance response (orange) with a delayed sensory gain (fig. S3). This prediction successfully captures the overshooting (E) and phase shift (F) evident in the actual low-light response (dark blue) replotted from (A) and (B) on a log axis.

  3. Fig. 3 Tracking performance and real flower movements.

    Tracking error [(A), mean ± 95% CI] is a function of frequency for both luminance conditions. Three distinct frequency bands result, denoted by dashed lines. Behavioral performance of moths (B) was scored as no flight (~F); flight, but not tracking (F, ~T); or flight and tracking (T). The power spectra (C) of hawkmoth-pollinated flowers blowing in breezes from 0.1 to 2.7 m/s are normalized to the total power. 94% of the cumulative power in the flower’s movement (black: mean) occurs in frequencies below 1.7 Hz, where ε ≈ 0.2 to 0.4 (D).