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The river hippopotamus (Hippopotamus amphibius), one of the closest extant relatives to cetaceans, is a large African even-toed ungulate (Artiodactyla) that grazes and has a semiaquatic lifestyle. Given its unusual phenotype, ecology, and evolutionary history, we sought to measure the topographic distribution of retinal ganglion cell density using stereology and retinal wholemounts. We estimated a total of 243,000 ganglion cells of which 3.4% (8,300) comprise alpha cells. The topographic distribution of both total and alpha cells reveal a dual topographic organization of a temporal and nasal area embedded within a well-defined horizontal streak. Using maximum density of total ganglion cells and eye size (35 mm, axial length), we estimated upper limits of spatial resolving power of 8 cycles/deg (temporal area, 1,800 cells/mm2 ), 7.7 cycles/deg (nasal area, 1,700 cells/mm2 ), and 4.2 cycles/deg (horizontal streak, 250 cells/mm2 ). Enhanced resolution of the temporal area toward the frontal visual field may facilitate grazing, while resolution of the horizontal streak and nasal area may help the discrimination of objects (predators, conspecifics) in the lateral and posterior visual fields, respectively. Given the presumed role of alpha cells to detect brisk transient stimuli, their similar distribution to the total ganglion cell population may facilitate the detection of approaching objects in equivalent portions of the visual field. Our finding of a nasal area in the river hippopotamus retina supports the notion that this specialization may enhance visual sampling in the posterior visual field to compensate for limited neck mobility as suggested for rhinoceroses and cetaceans.
This study sought to determine whether the retinal organization of the white rhinoceros (Ceratotherium simum), a large African herbivore with lips specialized for grazing in open savannahs, relates to its foraging ecology and habitat. Using stereology and retinal wholemounts, we estimated a total of 353,000 retinal ganglion cells. Their density distribution reveals an unusual topographic organization of a temporal (2,000 cells/mm2 ) and a nasal (1,800 cells/mm2 ) area embedded within a well-defined horizontal visual streak (800 cells/mm2 ), which is remarkably similar to the retinal organization in the black rhinoceros. Alpha ganglion cells comprise 3.5% (12,300) of the total population of ganglion cells and show a similar distribution pattern with maximum densities also occurring in the temporal (44 cells/mm2 ) and nasal (40 cells/mm2 ) areas. We found higher proportions of alpha cells in the dorsal and ventral retinas. Given their role in the detection of brisk transient stimuli, these higher proportions may facilitate the detection of approaching objects from the front and behind while grazing with the head at 45 °. Using ganglion cell peak density and eye size (29 mm, axial length), we estimated upper limits of spatial resolving power of 7 cycles/deg (temporal area), 6.6 cycles/deg (nasal area), and 4.4 cycles/deg (horizontal streak). The resolution of the temporal area potentially assists with grazing, while the resolution of the streak may be used for panoramic surveillance of the horizon. The nasal area may assist with detection of approaching objects from behind, potentially representing an adaptation compensating for limited neck and head mobility. J. Comp. Neurol., 525:2484-2498, 2017. © 2017 Wiley Periodicals, Inc.
Megachiropteran bats (megabats) show remarkable diversity in microhabitat occupation and trophic specializations, but information on how vision relates to their behavioral ecology is scarce. Using stereology and retinal wholemounts, we measured the topographic distribution of retinal ganglion cells and determined the spatial resolution of eight African megachiropterans with distinct roosting and feeding ecologies. We found that species roosting in open microhabitats have a pronounced streak of high retinal ganglion cell density, whereas those favoring more enclosed microhabitats have a less pronounced streak (or its absence in Hypsignathus monstrosus). An exception is the cave-dwelling Rousettus aegyptiacus, which has a pronounced horizontal streak that potentially correlates with its occurrence in more open environments during foraging. In all species, we found a temporal area with maximum retinal ganglion cell density (∼5,000-7,000 cells/mm2 ) that affords enhanced resolution in the frontal visual field. Our estimates of spatial resolution based on peak retinal ganglion cell density and eye size (∼6-12 mm in axial length) range between ∼2 and 4 cycles/degree. Species that occur in more enclosed microhabitats and feed on plant material have lower spatial resolution (∼2 cycles/degree) compared with those that roost in open and semiopen areas (∼3-3.8 cycles/degree). We suggest that the larger eye and concomitant higher spatial resolution (∼4 cycles/degree) in H. monstrosus may have facilitated the carnivorous aspect of its diet. In conclusion, variations in the topographic organization and magnitude of retinal ganglion density reflect the specific ecological needs to detect food/predators and the structural complexity of the environments. J. Comp. Neurol. 525:186-203, 2017. © 2016 Wiley Periodicals, Inc.
The giraffe (Giraffa camelopardalis) is a browser that uses its extensible tongue to selectively collect leaves during foraging. As the tallest extant terrestrial mammal, its elevated head height provides panoramic surveillance of the environment. These aspects of the giraffe's ecology and phenotype suggest that vision is of prime importance. Using Nissl-stained retinal wholemounts and stereological methods, we quantitatively assessed the retinal specializations in the ganglion cell layer of the giraffe. The mean total number of retinal ganglion cells was 1,393,779 and their topographic distribution revealed the presence of a horizontal visual streak and a temporal area. With a mean peak of 14,271 cells/mm(2), upper limits of spatial resolving power in the temporal area ranged from 25 to 27 cycles/degree. We also observed a dorsotemporal extension (anakatabatic area) that tapers toward the nasal retina giving rise to a complete dorsal arch. Using neurofilament-200 immunohistochemistry, we also detected a dorsal arch formed by alpha ganglion cells with density peaks in the temporal (14-15 cells/mm(2)) and dorsonasal (10 cells/mm(2)) regions. As with other artiodactyls, the giraffe shares the presence of a horizontal streak and a temporal area which, respectively, improve resolution along the horizon and in the frontal visual field. The dorsal arch is related to the giraffe's head height and affords enhanced resolution in the inferior visual field. The alpha ganglion cell distribution pattern is unique to the giraffe and enhances acquisition of motion information for the control of tongue movement during foraging and the detection of predators.
The Nubian ibex (Capra nubiana) occurs in information-rich visual habitats including the edges of cliffs and escarpments. In addition to needing enhanced spatial resolution to find food and detect predators, enhanced visual sampling of the lower visual field would be advantageous for the control of locomotion in such precarious terrains. Using retinal wholemounts and stereology, we sought to measure how the ganglion cell density varies across the retina of the Nubian ibex to reveal which portions of its surroundings are sampled with high resolution. We estimated a total of ~1 million ganglion cells in the Nubian ibex retinal ganglion cell layer. Topographic variations of ganglion cell density reveal a temporal area, a horizontal streak, and a dorsotemporal extension, which are topographic retinal features also found in other artiodactyls. In contrast to savannah-dwelling artiodactyls, the horizontal streak of the Nubian ibex appears loosely organized possibly reflecting a reduced predation risk in mountainous habitats. Estimates of spatial resolving power (~17 cycles/degree) for the temporal area would be reasonable to facilitate foraging in the frontal visual field. Embedded in the dorsotemporal extension, we also found an unusual dorsotemporal area not yet reported in any other mammal. Given its location and spatial resolving power (~6 cycles/degree), this specialization enhances visual sampling toward the lower visual field, which would be advantageous for visually guided locomotion. This study expands our understanding of the retinal organization in artiodactyls and offers insights on the importance of vision for the Nubian ibex ecology.
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