Retinal Topography in Two Species of Baleen Whale (Cetacea: Mysticeti)

Abstract

Little is known about the visual systems of large baleen whales (Mysticeti: Cetacea). In this study, we investigate eye morphology and the topographic distribution of retinal ganglion cells (RGCs) in two species of mysticete, Bryde’s whale (Balaenoptera edeni) and the humpback whale (Megaptera novaeanglia). Both species have large eyes characterised by a thickened cornea, a heavily thickened sclera, a highly vascularised fibro-adipose bundle surrounding the optic nerve at the back of the eye, and a reflective blue-green tapetum fibrosum. Using stereology and retinal whole mounts, we estimate a total of 274,268 and 161,371 RGCs in the Bryde’s whale and humpback whale retinas, respectively. Both species have a similar retinal topography, consisting of nasal and temporal areas of high RGC density, suggesting that having higher visual acuity in the anterior and latero-caudal visual fields is particularly important in these animals. The temporal area is larger in both species and contains the peak RGC densities (160 cells mm^–2 in the humpback whale and 200 cells mm^–2 in Bryde’s whale). In the Bryde’s whale retina, the two high-density areas are connected by a weak centro-ventral visual streak, but such a specialisation is not evident in the humpback whale. Measurements of RGC soma area reveal that although the RGCs in both species vary substantially in size, RGC soma area is inversely proportional to RGC density, with cells in the nasal and temporal high-density areas being relatively more homogeneous in size compared to the RGCs in the central retina and the dorsal and ventral retinal periphery. Some of the RGCs were very large, with soma areas of over 2,000 µm². Using peak RGC density and eye axial diameter (Bryde’s whale: 63.5 mm; humpback whale: 48.5 mm), we estimated the peak anatomical spatial resolving power in water to be 4.8 cycles/degree and 3.3 cycles/degree in the Bryde’s whale and the humpback whale, respectively. Overall, our findings for these two species are very similar to those reported for other species of cetaceans. This indicates that, irrespective of the significant differences in body size and shape, behavioural ecology and feeding strategy between mysticetes and odontocetes (toothed whales), cetacean eyes are adapted to vision in dim light and adhere to a common “bauplan” that evolved prior to the divergence of the two cetacean parvorders (Odontoceti and Mysticeti) over 30 million years ago.

The oblique extraocular muscles in cetaceans: Overall architecture and accessory insertions

“…Nevertheless, the breadth and depth of eye movement research over the past century allows ample room for informed speculation regarding the consequences of ocular, orbital, and neuromuscular structure/function features. As shown by the present anatomical data, cetacean SO and IO clearly form a suitable agonist-antagonist configuration for driving ocular rotations about the optical axis (or axes, Lisney & Collin, 2019;Mass & Supin, 2009).…”

Immunohistochemical Characterisation of the Whale Retina

“…But the retinas of other terrestrial artiodactyls, such as the giraffe, the camel, and the water buffalo have 1 million or more RGCs. Conversely, some odontocete cetaceans as the Amazonian River dolphin and the tucuxi, have much lower numbers (approximately 15,000 and 45,000, respectively; Lisney and Collin, 2018). On the other hand, the low RGC density found in the fin whale could be explained by the large very size of their retina.…”

“…For example, the cetacean eye has well developed extraocular muscles, as well as a thick cornea and sclera to protect against high pressures (Mengual et al, 2015). Collecting the eyes of whales, such as mysticetes (including the genus Balaenoptera), in a sufficiently well-preserved state for histological analysis can be problematic (Lisney and Collin, 2018), although several studies have described morphological characteristics of the cetacean retina, including one of the largest, the fin whale (Balaenoptera physalus: Pilleri and Wandeler, 1964). The topographic organisation of RGCs has been analysed in a variety of cetacean species in order to estimate their visual acuity and to compare visual specialisation.…”

A comparative analysis of cone photoreceptor morphology in bowhead and beluga whales

“…Of the three morphologies observed, cones containing OS and IS compartments characteristic of traditional mammalian photoreceptors were located in a restricted region of the bowhead retina. In the retina, areas with greater density of GCs and photoreceptors correlate with increased sensory acuity (Lisney & Collin, 2018; Peichl, 2005; Viets et al, 2016). Typically, this is either somewhat circular (area centralis) or elongated (visual streak).…”

“…We chose to only focus within area of presumed highest photoreceptor density (fovea; temporal retina) and outside (superior). The fovea in some cetaceans has been identified (through quantification of ganglion cell [GC]) to reside predominantly across the temporal retina and streak into the nasal region (Lisney & Collin, 2018; Mass, 2001; Mass & Supin, 1997).…”