A spitting image: specializations in archerfish eyes for vision at the interface between air and water

Abstract

Archerfish are famous for spitting jets of water to capture terrestrial insects, a task that not only requires oral dexterity, but also the ability to detect small camouflaged prey against a visually complex background of overhanging foliage. Because detection of olfactory, auditory and tactile cues is diminished at air-water interfaces, archerfish must depend almost entirely on visual cues to mediate their sensory interactions with the aerial world. During spitting, their eyes remain below the water's surface and must adapt to the optical demands of both aquatic and aerial fields of view. These challenges suggest that archerfish eyes may be specially adapted to life at the interface between air and water. Using microspectrophotometry to characterize the spectral absorbance of photoreceptors, we find that archerfish have differentially tuned their rods and cones across their retina, correlated with spectral differences in aquatic and aerial fields of view. Spatial resolving power also differs for aquatic and aerial fields of view with maximum visual resolution (6.9 cycles per degree) aligned with their preferred spitting angle. These measurements provide insight into the functional significance of intraretinal variability in archerfish and infer intraretinal variability may be expected among surface fishes or vertebrates where different fields of view vary markedly.

Figure 1.

Mean maximum absorbance (λ_max ± s.d.) of archerfish (Toxotes chatareus) photoreceptors fit three basic patterns coinciding with three retinal areas, measured using microspectrophotometry. Grey crosses, rods; circles, single cones; triangles, each outer segment member of the double cones (ventro-temporally the λ_max values of the two outer segment members differed significantly (p < 0.001) and are connected by a dashed line to indicate that they are one functional unit).

Figure 2.

Normalized corrected absorptance curves (see text) for single cones (dashed lines) and double cones (solid and dotted lines) measured from three areas of the archerfish (Toxotes chatareus) retina, compared with normalized spectral radiance (grey filled curves) for the respective field of view (measured in the natural environment; Laura River, Cape York, Queensland, Australia). The lack of dotted lines in plots of dorsal and ventro-nasal areas reflects the similarity in λ_max values of the two outer segment members of the double cones in these retinal areas; a single line was used to reduce crowding.

Figure 3.

Topographic distribution of cones (left inset) and ganglion cells (right inset) of the archerfish (Toxotes chatareus) correctly oriented and overlaid on an image of an archerfish spitting. Cell densities are reported as cells mm⁻². Red line demarcates the line of sight to the target, note the bending of light as it passes through the air–water interface owing to differences in refractive indices of air and water.