Opsin switch reveals function of the ultraviolet cone in fish foraging

Abstract

Although several studies have shown that ultraviolet (UV) wavelengths are important in naturally occurring, visually guided behaviours of vertebrates, the function of the UV cone in such behaviours is unknown. Here, I used thyroid hormone to transform the UV cones of young rainbow trout into blue cones, a phenomenon that occurs naturally as the animal grows, to test whether the resulting loss of UV sensitivity affected the animal's foraging performance on Daphnia magna, a prey zooplankton. The distances and angles at which prey were located (variables that are known indicators of foraging performance) were significantly reduced for UV knock-out fish compared with controls. Optical measurements and photon-catch calculations revealed that the contrast of Daphnia was greater when perceived by the visual system of control versus that of thyroid-hormone-treated fish, demonstrating that the UV cone enhanced the foraging performance of young rainbow trout. Because most juvenile fishes have UV cones and feed on zooplankton, this finding has wide implications for understanding the visual ecology of fishes. The enhanced target contrast provided by UV cones could be used by other vertebrates in various behaviours, including foraging, mate selection and communication.

Figure 1.

Illustration of foraging search parameters, and lighting conditions during the experiments. (a) Schematic of a typical rainbow trout search path and attack sequence illustrating the parameters measured to analyse rainbow trout foraging performance. The solid dots along the line represent stationary pauses whereas the open circle indicates a prey item. (b) Downwelling irradiances (upper traces), and average sidewelling (horizontal) radiances (lower traces), used in the foraging experiments, as measured at the centre of the aquarium. Each horizontal radiance is the average of four scans corresponding to measurements along the four sides of the aquarium. FS, full spectrum; SW, short wavelength spectrum; LW, long wavelength spectrum.

Figure 2.

Cone opsin mRNA expression, visual pigment absorbance and optic nerve spectral sensitivity responses of control and thyroid-hormone-treated alevin rainbow trout. (a,b) Retinal sections double labelled with riboprobes encoding the SWS1 (red) and SWS2 (blue) opsin mRNAs. Single cones expressed SWS1 opsin mRNA (black arrows) in control fish (a) and SWS2 opsin mRNA (white arrows) in thyroid-hormone-treated fish (b). White arrowheads indicate double cones. Magnification bars, 8 µm. (c) Single cones of control fish possessed a UV visual pigment, whereas those of thyroid-hormone-treated fish had an S visual pigment (records are representative traces from individual cones). (d) Spectral sensitivity responses showing a UV cone mechanism in control fish and an S cone mechanism in thyroid-hormone-treated fish (data points are means ± s.d., n = 3). The two embedded photographs illustrate typical control and treatment fish; the latter became silvery as a result of thyroid hormone exposure.

Figure 3.

Absorbance of Daphnia magna body parts and photographic appearance under various spectral backgrounds. (a) Daphnia magna photographed using transmitted light from the Xenon source. Magnification bar = 0.25 mm. (b) Absorbance spectra from various regions of the Daphnia body illustrated in (a). (c,d) The same D. magna photographed using the filters that produced the long wavelength (LW) and short wavelength (SW) backgrounds, respectively.