Synchronization of speed, sound and iridescent color in a hummingbird aerial courtship dive

Abstract

Many animal signals are complex, often combining multimodal components with dynamic motion. To understand the function and evolution of these displays, it is vital to appreciate their spatiotemporal organization. Male broad-tailed hummingbirds (Selasphorus platycercus) perform dramatic U-shaped courtship dives over females, appearing to combine rapid movement and dive-specific mechanical noises with visual signals from their iridescent gorgets. To understand how motion, sound and color interact in these spectacular displays, we obtained video and audio recordings of dives performed by wild hummingbirds. We then applied a multi-angle imaging technique to estimate how a female would perceive the male's iridescent gorget throughout the dive. We show that the key physical, acoustic and visual aspects of the dive are remarkably synchronized-all occurring within 300 milliseconds. Our results highlight the critical importance of accounting for motion and orientation when investigating animal displays: speed and trajectory affect how multisensory signals are produced and perceived.

Fig. 1

During the dive, sound and color change markedly as a function of trajectory and speed. a Representative dive aligned with the origin at the nadir (point of lowest height). The asterisk indicates estimated female position. Colored sections correspond to the sonogram of sonations during the dive. b Sonogram corresponding to the representative dive. Colors indicate sections of dive sonation. Purple: wing-generated main dive sonations (section A). Orange: tail-generated sonations. Teal: wing-generated short sonations (section B). Pink: wing-generated long sonations (section C). c Plot of all tracked dives aligned as above and overlaid (n = 48). d Mean estimated speed during the dive. Shaded area indicates standard deviation (n = 17 bouts of diving containing 48 dives). Also overlaid with transparency are individual measures from all tracked dives (n = 48). e The perceived color of the gorget changes from red to black. Above: Female's relative cone stimulation values, estimating perception of the male's gorget (based on 10 male specimens), as predicted by a hummingbird vision model as a function of male orientation. Negative x values indicate that the beak is rotated toward the observer. Positive x values indicate that the beak is rotated away. Points indicate measured values, lines show smoothing spline interpolation of the mean, and the shaded area indicates standard deviation of the mean. Red: longwave-sensitive cone. Green: mediumwave-sensitive cone. Blue: shortwave-sensitive cone. Magenta: ultraviolet-sensitive cone. Black: double cone. Note that double cone stimulation is not relative to the other cones but to the reflectance standard in each image (0–1). Below: examples of extracted gorget images, and an illustration of the average hue of the gorgets at each orientation (irrespective of intensity/brightness). The arrow represents the direction of perceived color change that occurs for a female at the nadir of the dive; see main text below

Fig. 2

Horizontal velocity, sound and color are remarkably synchronized, occurring within 300 ms. a Box-and-whisker plot of measured and estimated times for various parts of the diving behavior: mean time of maximal estimated speed, mean time of maximal Y (vertical) and X (horizontal) velocity, mean times of tail-generated sonation onset and cessation, mean times of gorget visibility, mean time of maximal estimated luminance of the gorget, mean time of maximal estimated female LWS stimulation, mean time of maximal color shift, and the mean time of maximal female visual angle taken up by the male. N = 17 (17 bouts of diving containing 48 dives) for all measures, dotted lines indicate −230 ms, 0 s, and 70 ms. For each measure, box tails indicate 25th and 75th percentiles, and the central line indicates the median. b Mean estimated Doppler effect. Shaded area indicates one standard deviation (N = 17). Also plotted with transparency is estimated Doppler effect for individual dives. c Estimated female relative cone stimulation during the dive. Red: longwave-sensitive (LWS) cone stimulation. Green: mediumwave-sensitive cone stimulation. Blue: shortwave-sensitive cone stimulation. Magenta: ultraviolet-sensitive cone stimulation. Black: double cone stimulation. d Averaged sonograms of 30 dives, with minor contrast enhancement to highlight the darkening due to the low frequencies of tail-generated sonations. e Representative sonogram from one dive; colored bars correspond to sections in Fig. 1a and b. All values are temporally aligned such that the time of maximal visual angle, i.e., the nadir of the dive, is 0