Eye Morphology in Cathemeral Lemurids and Other Mammals

University of Texas at Austin, Austin, TX 78712, USA.
Folia Primatologica (Impact Factor: 0.89). 02/2006; 77(1-2):27-49. DOI: 10.1159/000089694
Source: PubMed


The visual systems of cathemeral mammals are subject to selection pressures that are not encountered by strictly diurnal or nocturnal species. In particular, the cathemeral eye and retina must be able to function effectively across a broad range of ambient light intensities. This paper provides a review of the current state of knowledge regarding the visual anatomy of cathemeral primates, and presents an analysis of the influence of cathemerality on eye morphology in the genus Eulemur. Due to the mutual antagonism between most adaptations for increased visual acuity and sensitivity, cathemeral lemurs are expected to resemble other cathemeral mammals in having eye morphologies that are intermediate between those of diurnal and nocturnal close relatives. However, if lemurs only recently adopted cathemeral activity patterns, then cathemeral lemurids would be expected to demonstrate eye morphologies more comparable to those of nocturnal strepsirrhines. Both predictions were tested through a comparative study of relative cornea size in mammals. Intact eyes were collected from 147 specimens of 55 primate species, and relative corneal dimensions were compared to measurements taken from a large sample of non-primate mammals. These data reveal that the five extant species of the cathemeral genus Eulemur have relative cornea sizes intermediate between those of diurnal and nocturnal strepsirrhines. Moreover, all Eulemur species have relative cornea sizes that are comparable to those of cathemeral non-primate mammals and significantly smaller than those of nocturnal mammals. These results suggest that Eulemur species resemble other cathemeral mammals in having eyes that are adapted to function under variable environmental light levels. These results also suggest that cathemerality is a relatively ancient adaptation in Eulemur that was present in the last common ancestor of the genus (ca. 8-12 MYA).

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    • "In Madagascar, field studies clearly suggest that the diurnal time budgets of lemurs may be affected by habitat disturbance (Donati et al. 2011; Irwin 2008; Schwitzer et al. 2007a, 2011). This is particularly relevant for species of Eulemur, as these primates, like most ungulates and micro-mammals, do not appear constrained by specialized eye adaptations that would keep their activity limited to either the nocturnal or the diurnal phase (Kirk 2006). However, cathemeral activity has rarely been investigated in relation to habitat disturbance. "
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    ABSTRACT: The ultimate determinants of cathemerality, i.e., activity spread over the 24-h cycle, in primates have been linked to various ecological factors. Owing to the fast rate of habitat modification, it is imperative to know whether and how this behavioural flexibility responds to anthropogenic disturbance. The true lemurs (Eulemur clade) constitute a valuable case to study these potential effects, as all species studied so far exhibit cathemerality. Here we explored the effects of anthropogenic disturbance on activity patterns of Eulemur while controlling for ecological factors proposed as determinants of activity shifts. We first performed a meta-analysis using 13 long-term studies conducted over the last three decades on various populations of Eulemur. We fitted a beta regression using the proportion of diurnality (the activity taking place between sunrise and sunset) as the response variable and seven climatic, ecological, and anthropogenic disturbance variables at each site as predictors. We also present a validation with original data using year-round, 24-h activity of collared brown lemurs (Eulemur collaris) in forest fragments with different levels of disturbance in southeastern Madagascar. Diurnality was prevalent at most sites. Seasonality, proportions of leaves in the diet, and group size were all found to be significant predictors of the proportion of diurnal activity. After controlling for socioecological factors in the model, overall anthropogenic disturbance emerged as a negative predictor of diurnality. Our validation suggests that the lemurs in the more disturbed area exhibited more nocturnal activity than those in the less disturbed area. It is unclear whether the plasticity observed might allow populations of Eulemur to persist in disturbed areas longer than lemurs with less flexible activity patterns.
    International Journal of Primatology 11/2015; DOI:10.1007/s10764-015-9876-7 · 1.99 Impact Factor
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    • "comm.). Other species of Eulemur appear to be devoid of this sensitivity-enhancing structure, although the histological evidence is contradictory and uncertain (Castenholz 1965; Kirk 2006). Field reports variously describe the presence or absence of eyeshine in closely related species (e.g., E. (macaco) macaco -absent, Colquhoun 1997; E (macaco) flavifrons -present, Schwitzer et al. 2007, but see Fig S7). "
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    ABSTRACT: In contrast to the majority of primates, which exhibit dedicated diurnality or nocturnality, all species of Eulemur are cathemeral. Color vision, in particular, is strongly affected by the spectral composition and intensity of ambient light, and the impact of activity period on the evolution of primate color vision is actively debated. We studied three groups of wild brown lemurs (Eulemur fulvus) in Ankarafantsika National Park, Madagascar over a one-year span. We also used non-invasive fecal DNA collection and analysis to study the opsin genes underlying the color vision of 24 individuals. We quantify the color and brightness of dietary fruits and modeled the chromaticity and discriminability of food objects to different visual phenotypes under daylight, twilight, and moonlight conditions. We found that E. fulvus possesses routine dichromacy, unlike its congener E. flavifrons, for which polymorphic trichromacy has been reported. Our models suggest that dichromacy is well-suited to the foraging ecology of E. fulvus. The performance of modeled dichromats and trichromats is comparable under nocturnal illuminants and the luminance values of most diet items are detectable across light conditions. The trichromatic phenotype demonstrates a modest advantage under daylight conditions only. Our results, taken together with reports of polymorphic trichromacy in E. flavifrons, suggest functional ecological variation in the visual system of the genus Eulemur. Interspecific phenotypic variation in the color vision of a genus is both unexpected and instructive. Ecological differences between species of Eulemur could reveal thresholds for the origins of polymorphic trichromacy, which preceded the evolution of routine trichromatic vision in humans and other primates. This article is protected by copyright. All rights reserved.
    Functional Ecology 09/2015; DOI:10.1111/1365-2435.12575 · 4.83 Impact Factor
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    • "Accordingly, the eyes of Eulemur exhibit intermediate ocular morphologies (e.g. absolute eye diameters; the ratio of mean corneal diameter to transverse and axial eye diameters) suggesting that cathemerality is an ancient trait that has been under stabilizing selection for ~9–13 million years (Tattersall 1987; Kirk 2006; Griffin, Matthews & Nunn 2012). Compatible with this view is a recent phylogenetic analysis indicating that cathemerality preceded diurnality in lemurs, and is of relatively ancient origin (Santini et al. 2015). "

    Functional Ecology 01/2015; · 4.83 Impact Factor
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