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.

Morphometric and meristic variation in two congeneric archer fishes Toxotes chatareus (Hamilton 1822) and Toxotes jaculatrix (Pallas 1767) inhabiting Malaysian coastal waters

“…Despite this specialized hunting technique, they are opportunistic feeders and will consume a wide range of prey, including terrestrial insects, shrimps, and teleosts . Both species are euryhaline, inhabiting primarily the brackish mangroves of the South Pacific and Indian Oceans, although they can also be found far upstream in fresh waters and more saline coastal waters (Allen, 1978;2001;Froese and Pauly, 2005;Temple, 2007;Temple et al, 2010). These fishes are relatively difficult to collect within the complex rooting systems of mangrove forests, together with their sharp vision and fast swimming speed (Blaber, 2000).…”

Comparison of functional and anatomical estimations of visual acuity in two species of coral reef fish

“…For ganglion cells, counts were made at the same distances at 100× magnification, resulting in approximately 150-200 points being sampled across the retina. All clearly identifiable neural elements lying within the ganglion cell layer were counted irrespective of size (Collin and Pettigrew, 1988a,b;Litherland and Collin, 2008;Temple et al, 2010;Lee and O'Brian, 2011;Champ et al, 2013). Because of their distinct elongated shape and dense staining (Collin and Pettigrew, 1988c), glial cells were easily identifiable and were excluded from cell counts.…”

“…For the anatomical visual acuity estimate, it was assumed that all of the photoreceptors (double and single cones) in the mosaic were being used for the animal's visual acuity (Matsuda et al, 2008;Haug et al, 2010;Temple et al, 2010Temple et al, , 2013Champ et al, 2013).…”

“…Species found inhabiting open water can have much larger differences in acuity (for example, Lethrinus chrysostomus and Gymnocranuis bitorquatus: 19 and 27 cycles deg −1 , respectively) (Collin and Pettigrew, 1989). The visual acuity of fish has been measured using a range of behavioural (Brunner, 1934;Yamanouchi, 1956;Nakamura, 1968;Hodos and Yolen, 1976;Hairston et al, 1982;Neave, 1984;Pankhurst et al, 1993;Neumeyer, 2003b;Haug et al, 2010;Lee and O'Brian, 2011;Champ, 2012) and anatomical methods (Hodos and Yolen, 1976;Collin and Pettigrew, 1989;Fritsches et al, 2003;Matsuda et al, 2005Matsuda et al, , 2008Theiss et al, 2007;Litherland and Collin, 2008;Kino et al, 2009;Carton and Vaughan, 2010;Temple et al, 2010;Lee and O'Brian, 2011;Champ, 2012). However, because of the many differences in methodology, comparisons between studies are difficult.…”

Pop-out in visual search of moving targets in the archer fish

“…To address these questions we studied the archer fish [21][22][23][24][25][26] , a species that lacks a cortex 27 but exhibits complex visual behaviours and unique hunting practices. Owing to its remarkable ability to shoot down prey found on foliage above the water level, and its ability to learn to distinguish between artificial targets presented on a computer monitor in an experimental setting 28 , the archer fish exhibits overt target selection that can be leveraged for reporting psychophysical decisions in controlled lab experiments 24,26,29,30 .…”