Functional differences between the extraordinary eyes of deep-sea hyperiid amphipods

Abstract

The ocean's midwater is a uniquely challenging yet predictable and simple visual environment. The need to see without being seen in this dim, open habitat has led to extraordinary visual adaptations. To understand these adaptations, we compared the morphological and functional differences between the eyes of three hyperiid amphipods-Hyperia galba, Streetsia challengeri and Phronima sedentaria. Combining micro-CT data with computational modelling, we mapped visual field topography and predicted detection distances for visual targets viewed in different directions through mesopelagic depths. Hyperia's eyes provide a wide visual field optimized for spatial vision over short distances, while Phronima's and Streetsia's eyes have the potential to achieve greater sensitivity and longer detection distances using spatial summation. These improvements come at the cost of smaller visual fields, but this loss is compensated for by a second pair of eyes in Phronima and by behaviour in Streetsia. The need to improve sensitivity while minimizing visible eye size to maintain crypsis has likely driven the evolution of hyperiid eye diversity. Our results provide an integrative look at how these elusive animals have adapted to the unique visual challenges of the mesopelagic.

Keywords: low light vision; midwater adaptations; retinal topography; spatial summation; visual field.

Figure 1.

Eye shape, ommatidial viewing directions and distribution of facet diameters differed between Hyperia (left column), Phronima (centre column) and Streetsia (right column). (a–c) Ommatidial axes (black lines), defined by connecting centres of corneas (black dots) to centres of rhabdom/light guides (red dots), are shown on eye shapes of specimen 1 of each genus. Arrows and pink letters indicate the orientations of the visual fields: D, dorsal; L, lateral; F, frontal. Scale bars 1 mm. (d–i) Ommatidial viewing directions mapped from the centre onto a surrounding sphere (blue: right eye, black: left eye) in oblique and dorsal view. (j–l) Facet diameters (µm) across the dorsal visual field indicating relative sensitivity. Right eyes are shown in saturated and left eyes in unsaturated colours. Numbers on maps indicate regions from which visual parameters were taken for modelling dorsal (1) and frontal/lateral (2) regions.

Figure 2.

Facet diameter (a) and acceptance and interommatidial angles (b) from specimen 1 used as inputs for the modelling of detection distances (figure 3; electronic supplementary material, figure S8) from the dorsal (D, region 1 in figure 1) and frontal/lateral visual fields (F/L, region 2 in figure 1). Numbers above bars indicate the ratio of acceptance to interommatidial angle (Hyperia: [9]; Phronima: calculated; Streetsia horizontal: [6]).

Figure 3.

Detection distances and depth range of vision are increased with spatial summation for all targets. All values are compared with the performance when spatially summing seven ommatidia. (a) Detection distances are shown viewing against downwelling radiance across depths for the dorsal eye regions of Hyperia (left column), Phronima (middle column) and Streetsia (right column). Model results are shown for a point source (top row) and a 1 cm extended dark object with 50% transparency (second row). Grey shading indicates where detection can occur. Black dots indicate 10 cm detection distances used in (b). (b) Change in the upper and lower depth range of vision when detecting a point source (upper panel) and a 1 cm dark object (lower panel) viewed from 10 cm distance against downwelling radiance with increasing summation. (c) Percentage improvement for different amounts of spatial summation in the dorsal eye regions compared with the summation of direct ommatidial neighbours (7 ommatidia summed).