Niche convergence suggests functionality of the nocturnal fovea

Abstract

The fovea is a declivity of the retinal surface associated with maximum visual acuity. Foveae are widespread across vertebrates, but among mammals they are restricted to haplorhine primates (tarsiers, monkeys, apes, and humans), which are primarily diurnal. Thus primates have long contributed to the view that foveae are functional adaptations to diurnality. The foveae of tarsiers, which are nocturnal, are widely interpreted as vestigial traits and therefore evidence of a diurnal ancestry. This enduring premise is central to adaptive hypotheses on the origins of anthropoid primates; however, the question of whether tarsier foveae are functionless anachronisms or nocturnal adaptations remains open. To explore this question, we compared the diets of tarsiers (Tarsius) and scops owls (Otus), taxa united by numerous anatomical homoplasies, including foveate vision. A functional interpretation of these homoplasies predicts dietary convergence. We tested this prediction by analyzing stable isotope ratios that integrate dietary information. In Borneo and the Philippines, the stable carbon isotope compositions of Tarsius and Otus were indistinguishable, whereas the stable nitrogen isotope composition of Otus was marginally higher than that of Tarsius. Our results indicate that species in both genera consumed mainly ground-dwelling prey. Taken together, our findings support a functional interpretation of the many homoplasies shared by tarsiers and scops owls, including a retinal fovea. We suggest that the fovea might function similarly in tarsiers and scops owls by calibrating the auditory localization pathway. The integration of auditory localization and visual fixation during prey detection and acquisition might be critical at low light levels.

Keywords: Otus lempiji; Otus megalotis; Tarsius bancanus; Tarsius syrichta; diet; fovea centralis; stable isotopes; visual predation.

FIGURE 1

The phyletic relationships of select primates and the sister taxon Dermoptera (the Sunda colugo, Galeopterus variegatus). The distinction between nocturnal (black zone) and diurnal (white zone) activity patterns is strongly associated with variation in retinal ganglion cell (RGC) counts (mm^-2), cone densities (mm^-2), and rod densities (mm^-2) in the area centralis or fovea centralis (data sources: Webb and Kaas, 1976; Perry and Cowey, 1985; Curcio et al., 1990; Wikler and Rakic, 1990; Silveira et al., 1993; Ogden, 1994; Wilder et al., 1996; Hendrickson et al., 2000; Dkhissi-Benyahya et al., 2001; Peichl et al., 2001; Ross, 2004; Tetreault et al., 2004; Finlay et al., 2008; Moritz et al., 2013). Ancestral character states based in part on these values suggest a diurnal ancestry for Tarsius and Aotus; and, by extension, stem anthropoids (e.g., Ross, 2000; Williams et al., 2010). Accordingly, the foveae of Tarsius and Aotus are most likely vestigial traits. A problem with this view is evident in the densities of RGCs, cones, and rods. Relative to Tarsius, the retina of Aotus has advanced further toward a nocturnal phenotype despite a substantially younger vintage of 5–20 million years (see text).

FIGURE 2

(A) Orthopteran insects such as katydids are a common prey item in the diet of tarsiers (photograph of Tarsius lariang by Stefan Merker, reproduced with permission). (B) Orthopteran insects are also consumed by scops owls (photograph of Otus scops by Clément and Julien Pappalardo, reproduced with permission). (C) Tarsiers also consume geckos (photograph of T. spectrum by David J. Slater, reproduced with permission). (D) In Singapore, geckos are reported to be the most common food item in the diet of O. lempiji (Lok et al., 2009; photograph by Tiah Khee Lee, reproduced with permission).

FIGURE 3

(A) The skull and eye of Tarsius bancanus (modified from Castenholz, 1984; Ross, 2004) together with the fovea of T. spectrum (modified from Hendrickson et al., 2000). (B) The skull, eye, and fovea of a composite strigiform (modified from Fite, 1973; Menegaz and Kirk, 2009). Because ocular mobility is constrained by the hyperenlarged eyes of tarsiers and scops owls, an extraordinary degree of cervical rotation is necessary to enable rapid prey localization and fixation. (C) The increased cervical mobility of tarsiers allows them to rotate their head 180° in azimuth (Castenholz, 1984; photograph of T. bancanus by Nick Garbutt, reproduced with permission). (D) Owls can rotate their head 270° in azimuth (Harmening and Wagner, 2011; photograph of O. lempiji by Paul B. Jones, reproduced with permission). Extreme head rotation is thought to enhance the sit-and-wait ambush mode of predation common to tarsiers and scops owls (Niemitz, 1985).

FIGURE 4

The distribution of sampling localities in Borneo (Otus lempiji and Tarsius bancanus) and in Philippines (O. megalotis and T. syrichta).

FIGURE 5

Bivariate plot of δ¹³C and δ¹⁵N values (mean ± 1 SD) in the keratin of Bornean tarsiers (Tarsius bancanus), Philippine tarsiers (T. syrichta), Sunda scops owls (Otus lempiji), and Philippine scops owls (O. megalotis). To illustrate an approximate full dietary trophic step, the keratin-derived δ¹³C and δ¹⁵N values of a frugivore (Müller’s Bornean gibbon, Hylobates muelleri) and a predator of vertebrates (leopard cat, Felis bengalensis) from Sabah, northern Borneo are also plotted.