Topographic specializations in the retinal ganglion cell layer of Australian passerines

Abstract

Thornbills, honeyeaters, and silvereyes represent an abundant group of Australian passerines, whose diversity in niche differentiation suggests a pivotal role for vision. Using stereological methods and retinal wholemounts, we studied the topographic distribution of neurons in the ganglion cell layer of insectivorous, nectarivorous, and frugivorous species occupying terrestrial and arboreal microhabitats. All species studied have a central convexiclivate fovea (peak densities from 130,000 to 160,000 cells/mm(2)), which is shallow in the terrestrial/insectivorous yellow-rumped thornbill and deep in the arboreal/nectarivorous honeyeaters and frugivorous silvereye. Surrounding the fovea, neuronal densities in the ganglion cell layer form a broadly ovoid and asymmetric plateau in the yellow-rumped thornbill and a more restricted, circular and symmetric plateau in the other species. These differences in the plateau organization may reflect specific needs to locate food on the ground or among dense vegetation. We also found a temporal area (peak densities from 43,000 to 54,000 cells/mm(2)) across species, which increases spatial resolution in the frontal visual field and assists with foraging. Using microtubule-associated protein 2 (MAP2) immunohistochemistry, we detected a higher concentration of giant ganglion cells forming an area gigantocellularis in the temporal retina of all species. Giant ganglion cell densities also form a horizontal streak in all species, except in the yellow-rumped thornbill, which has an unusual increase toward the retinal periphery. In the yellow-rumped thornbill and silvereye, giant ganglion cells also peak in the nasal retina. We suggest that these topographic variations afford differential sampling of motion signals for the detection of predators.

Eye Morphology and Retinal Topography in Hummingbirds (Trochilidae: Aves)

“…Although we do not have direct evidence to support this, the central area in A. tzacatl and P. superciliosus may also contain a shallow fovea, which we were not able to detect in whole mounts for these species. Support for this suggestion comes from the fact that the presence of a central fovea is a very common feature in the retinas of a diverse range of birds, including pigeons [Binggeli and Paule, 1969;Querubin et al, 2009], kingfishers [Slonaker, 1897;Moroney and Pettigrew, 1987], terns [Slonaker, 1897;Fite and Rosenfield-Wessels, 1975], swallows [Slonaker, 1897], passerines [Slonaker, 1897;Fite and RosenfieldWessels, 1975;Coimbra et al, 2006Coimbra et al, , 2009Coimbra et al, , 2014bMoore et al, 2013Moore et al, , 2015, parrots [Coimbra et al, 2014a], falcons, eagles, and vultures [Slonaker, 1897;Fite and RosenfieldWessels, 1975;Frost et al, 1990;Inzunza et al, 1991;Lisney et al, 2013b]. In addition, the presence of a second, temporally located area of peak density (which may or may not be foveated) has been reported in many of the groups of birds mentioned above.…”

“…This indicates that in A. tzacatl and C. anna , as well as in many other avian species, the lateral, monocular visual fields (viewed by the central high-density areas) and the frontal, binocular visual field (viewed by the temporal high-density areas) are of particular importance, irrespectively of their specific ecological niches. Having said this, differences in foveal organization and location, for example, may reflect adaptations to specific niches [Lisney et al, 2013b;Coimbra et al, 2014b]. Future studies should measure visual fields in hummingbirds in order to assess the degree to which the central and temporal retinal specializations we identified in A. tzacatl and C. anna map on to the monocular and binocular visuals fields [e.g.…”

“…Indeed, a small proportion of the diet of many species of hummingbirds, including A. tzacatl, C. anna, and P. superciliosus, is comprised of insects and spiders, which they catch by aerial hawking or gleaning from foliage, branches, and spider webs [Wagner, 1946;Pearson, 1954;Stiles, 1995;del Hoyo et al, 1999;Warwick et al, 2012]. Interestingly, brown honeyeaters (Lichmera indistincta), which are nectarivorous passerine birds that also occasionally feed on insects, have a retinal topography similar to that of A. tzacatl and C. anna [Coimbra et al, 2014b].…”

“…Nissl-stained neurons were counted provided they either lay entirely within the counting frame or they touched an acceptance line without also touching a rejection line [Gundersen, 1977]. We did not attempt to differentiate between RGC and displaced amacrine cells also found in the RGC layer because we could not reliably distinguish between the two neuron types using cytological criteria in the areas of high neuron density [also see Coimbra et al, 2006Coimbra et al, , 2009Coimbra et al, , 2014bLisney et al, 2012aLisney et al, , b, 2013a. However, presumptive glial cells, identified on the basis of their small size, dark staining and small, round or elongated shape [Hughes, Wathey and Pettigrew, 1989;Coimbra et al, 2009Coimbra et al, , 2014b, were not included in the counts ( fig.…”

“…The position of these specializations in the retina reveals which part or parts of the visual field are sampled with increased spatial resolving power (SRP) and are thus of particular importance for survival tasks such as location of food and mates, predator surveillance, and obstacle avoidance. In addition to our aforementioned studies, recently a large number of retinal topography studies have revealed important information about retinal organization and evolution in a wide range of birds including waterfowl [Fernández-Juricic et al, 2011a;Lisney et al, 2013a], pen-guins [Coimbra et al, 2012], parrots [Coimbra et al, 2014a], and a variety of passerines [Coimbra et al, 2006[Coimbra et al, , 2009Fernández-Juricic et al, 2011a;Moore et al, 2013Moore et al, , 2015Coimbra et al, 2014b]. Here, as well as providing detailed descriptions of eye morphology and retinal topography in a range of hummingbird species, we tested the following two predictions.…”