Retinal ganglion cell topography and spatial resolving power in the white rhinoceros (Ceratotherium simum)

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Rhinoceroses comprise a small, but diverse, group of the odd‐toed hoofed mammals (Perissodactyla) (Price and Bininda‐Emonds, 2009; Dinerstein, 2011). They occupy a wide variety of habitats with distinct structural complexities ranging from open grasslands and woodlands in Africa to enclosed rainforests and floodplains with tall grass in Asia (Dinerstein, 2011). All species of rhinoceroses are herbivores and can be predominantly grazers or browsers, or may alternate between these two feeding methods depending on the seasonal availability of plant material (Dinerstein, 2011). They exhibit important morphological adaptations of their oral labia that allow them to exploit a diverse range of vegetation types and occupy distinct feeding niches (Dinerstein, 2011). For example, the black rhinoceros (Diceros bicornis) is a browser with a prehensile upper lip that facilitates plucking leaves and grasping stems in relatively more enclosed woodland microhabitats (Hillman‐Smith and Groves, 1994). In contrast, the white rhinoceros (Ceratotherium simum) is a strict grazer having specialized broad and square lips that enable the clipping of the grass close to the ground in open savannah habitats (Groves, 1972) (Fig. 1).
Variations in the topographic distribution of retinal neurons generally reflect ecological variables (i.e., feeding niche and habitat type) and are key predictors of the relative importance of vision to behavior (Hughes, 1977; Collin, 1999). Elongated topographic patterns (i.e., horizontal streaks) of retinal neuronal density distributions, which are common in species that occur in more open microhabitats, allow for improved panoramic visual sampling across the horizon (Hughes, 1977; Collin, 1999). In contrast, concentric patterns (i.e., areas), which are found in species that occur in more enclosed microhabitats, allow for enhanced visual sampling in a more localized portion of the visual field (Hughes, 1977; Collin, 1999). In the black rhinoceros, the only species of rhinoceros examined to date, the topographic distribution of retinal ganglion cells reveals a remarkably unusual organization for terrestrial mammals. In this species, retinal ganglion cells reach their maximum density in two concentric areas located in the temporal and nasal portions of the retina, which enables simultaneous vision in the frontal and posterior visual fields, presumably assisting with foraging and predator detection, respectively (Pettigrew and Manger, 2008). The level of spatial resolution afforded by these two areas (∼5–6 cycles/deg) is sufficient to allow the black rhinoceros to detect small leaves at relevant foraging distances. Moreover, black rhinoceroses also have a horizontal streak of high density of retinal ganglion cells, which allows for enhanced panoramic vision across the horizon, and potentially facilitates the detection of predators and conspecifics (Pettigrew and Manger, 2008).
Despite the wealth of information that can be predicted about habitat use and foraging ecology from retinal organization (Hughes, 1977; Collin, 1999), no information is available about the topographic distribution of neurons in the retina of the white rhinoceros. Here we sought to determine whether the retina of the white rhinoceros shows a dual topographic organization similar to that of the black rhinoceros or whether it shows variations that reflect their grazing habits (i.e., lower visual resolution) and occurrence in open environments (i.e., more pronounced horizontal streak). Using retinal wholemounts and stereology, we mapped the topographic distribution of the total population of retinal ganglion cells and estimated the upper limits of spatial resolution of the white rhinoceros eye. We also mapped the population of presumed alpha retinal ganglion cells in Nissl‐stained wholemounts and confirmed our cytological criteria with neurofilament immunohistochemistry. In mammals, alpha cells comprise a morphologically distinct type of retinal ganglion cells, which are rich in neurofilaments and have large cell bodies and dendritic trees (Peichl et al., 1987; Peichl, 1991; Sanes and Masland, 2015).
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