Morphology and evolution of the snake cornea

To investigate whether the thickness of the cornea in snakes correlates with overall anatomy, habitat or daily activity pattern, we measured corneal thickness using optical coherence tomography scanning in 44 species from 14 families (214 specimens) in the collection at the Natural History Museum (Denmark). Specifically, we analyzed whether the thickness of the cornea varies among species in absolute terms and relative to morphometrics, such as body length, spectacle diameter, and spectacle thickness. Furthermore, we examined whether corneal thickness reflects adaptation to different habitats and/or daily activity patterns. The snakes were defined as arboreal (n = 8), terrestrial (n = 22), fossorial (n = 7), and aquatic (n = 7); 14 species were classified as diurnal and 30 as nocturnal. We reveal that the interspecific variation in corneal thickness is largely explained by differences in body size, but find a tendency towards thicker corneas in diurnal (313 ± 227 μm) compared to nocturnal species (205 ± 169 μm). Furthermore, arboreal snakes had the thickest corneas and fossorial snakes the thinnest. Our study shows that body length, habitat, and daily activity pattern could explain the interspecific variation in corneal morphology among snakes. This study provides a quantitative analysis of the evolution of the corneal morphology in snakes, and it presents baseline values of corneal thickness of multiple snake species. We speculate that the cornea likely plays a role in snake vision, despite the fact that results from previous studies suggest that the cornea in snakes is not relevant for vision (Sivak, Vision Research, 1977, 17, 293–298).     

Effects of activity pattern on eye size and orbital aperture size in primates

Among primates, nocturnal species exhibit relatively larger orbital apertures than diurnal species. Most researchers have considered this disparity in orbital aperture size to reflect differences in eye size, with nocturnal primates having relatively large eyes in order to maximize visual sensitivity. Presumed changes in eye size due to shifts in activity pattern are an integral part of theoretical explanations for many derived features of anthropoids, including highly convergent orbits and a postorbital septum. Here I show that despite clear differences in relative orbital aperture size, many diurnal and nocturnal primates do not differ in relative eye size. Among nocturnal primates, relative eye size is influenced by diet. Nocturnal visual predators (e.g., Tarsius, Loris, and Galago moholi) tend to have larger relative eye sizes than diurnal primates. By contrast, nocturnal frugivores (e.g., Perodicticus, Nycticebus, and Cheirogaleus) have relative eye sizes that are comparable to those of diurnal primates. Although some variation in orbital aperture size can be attributed to variation in eye size, both cornea size and orbit orientation also exert a strong influence on orbital aperture size. These findings argue for caution in the use of relative orbital aperture size as an indicator of activity pattern in fossil primates. These findings further suggest that existing scenarios for the evolution of unique orbital morphologies in anthropoids must be modified to reflect the importance of ecological variables other than activity pattern.     

Eye size in geckos: Asymmetry, allometry, sexual dimorphism, and behavioral correlates

The function of the vertebrate eye depends on its absolute size, and the size is presumably adapted to specific needs. We studied the variation of eye size at all levels, from intra-individual to inter-specific, in lid- less, spectacled, gecko lizards (Gekkonomorpha). We mea sured 1,408 museum specimens of 62 species, representing subfamilies Diplodactylinae, Gekkoninae, and Sphaerodactylinae. Intra-individually, eye size showed significant directional asymmetry in Stenodactylus sthenodactylus. A latitudinal study of six species confirmed that during postnatal ontogeny eye size undergoes conventional negative allometry; the slope is steeper among adults than among juveniles, expressing the need of juveniles for relatively larger eyes. Within species with sexual size dimorphism, commonly the larger sex possessed larger eyes in absolute terms but not relative to head-and-body length. Interspecifically, eye size showed negative allometry, with slope significantly steeper than those of intraspecific ontogenetic allometry, again expressing the need of juveniles for relatively larger eyes and showing that eye-size differences among species do not merely result from body-size differences. Finally, adult eye size varied interspecifically in correlation with parameters of behavioral ecology: eyes were significantly larger in nocturnal than in diurnal species, and significantly larger in cursorial than in scansorial species.     

Length–mass allometry in snakes

Body size and body shape are tightly related to an animal's physiology, ecology and life history, and, as such, play a major role in understanding ecological and evolutionary phenomena. Because organisms have different shapes, only a uniform proxy of size, such as mass, may be suitable for comparisons between taxa. Unfortunately, snake masses are rarely reported in the literature. On the basis of 423 species of snakes in 10 families, we developed clade‐specific equations for the estimation of snake masses from snout–vent lengths and total lengths. We found that snout–vent lengths predict masses better than total lengths. By examining the effects of phylogeny, as well as ecological and life history traits on the relationship between mass and length, we found that viviparous species are heavier than oviparous species, and diurnal species are heavier than nocturnal species. Furthermore, microhabitat preferences profoundly influence body shape: arboreal snakes are lighter than terrestrial snakes, whereas aquatic snakes are heavier than terrestrial snakes of a similar length. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Dentition and diet in snakes: adaptations to oophagy in the Australian elapid genus Simoselaps

Most small fossorial proteroglyphous Australian snakes of the genus Simoselaps feed on adult lizards, but the species of one lineage (the semifasciatus group) feed exclusively on the eggs of squamate reptiles. Examination of cleared, alizarin preparations showed that dentition of the saurophagous species is similar to that of other elapids, but dentition of the oophagous taxa is highly modified. The anterior (palatine and maxillary) teeth other than the fangs are reduced in size and number whereas those of the pterygoid (and in S. 'ropert ', the dentary) are enlarged posteriorly, becoming compressed along a longitudinal plane and angled medially. The shape of the pterygoid and quadrate is also modified.
Two Simoselaps species with broader diets (eating both adult lizards and their eggs) show typical 'saurophagous' dentition in one case, 'oophagous' dentition in the other, showing that either type of dentition can be used to capture and ingest either type of prey. We suggest functional explanations for the dentitional modifications in the egg-eating snakes, primarily in terms of the advantages of applying considerable force to the eggshell. Oophagous modifications within Simoselaps are convergent with those seen in several independently-derived lineages of oophagous colubrid snakes, but (perhaps because of the presence of the fang) differ in having the enlarged blade-like teeth on the pterygoid or dentary rather than the maxilla.     

Repeated loss of frontal sinuses in arctoid carnivorans

Many mammal skulls contain air spaces inside the bones surrounding the nasal chamber including the frontal, maxilla, ethmoid, and sphenoid, all of which are called paranasal sinuses. Within the Carnivora, frontal sinuses are usually present, but vary widely in size and shape. The causes of this variation are unclear, although there are some functional associations, such as a correlation between expanded frontal sinuses and a durophagous diet in some species (e.g., hyenas) or between absent sinuses and semiaquatic lifestyle (e.g., pinnipeds). To better understand disparity in frontal sinus morphology within Carnivora, we quantified frontal sinus size in relationship to skull size and shape in 23 species within Arctoidea, a clade that is ecologically diverse including three independent invasions of aquatic habitats, by bears, otters, and pinnipeds, respectively. Our sampled species range in behavior from terrestrial (rarely or never forage in water), to semiterrestrial (forage in water and on land), to semiaquatic (forage only in water). Results show that sinuses are either lost or reduced in both semiterrestrial and semiaquatic species, and that sinus size is related to skull size and shape. Among terrestrial species, frontal sinus size was positively allometric overall, but several terrestrial species completely lacked sinuses, including two fossorial badgers, the kinkajou (a nocturnal, arboreal frugivore), and several species with small body size, indicating that factors other than aquatic habits, such as space limitations due to constraints on skull size and shape, can limit sinus size and presence. J. Morphol. 276:22–32, 2015. © 2014 Wiley Periodicals, Inc.     

The relationship of ocular morphology to feeding modes and activity periods in shallow marine teleosts from New Zealand

Synopsis Thirty one species of shallow water teleosts were captured from the NE coast of New Zealand. Ocular morphology was assessed in terms of eye size, pupil shape, theoretical sensitivity and acuity based on retinal morphology, and regional distribution of photoreceptors within the retina. Eye size was relatively or absolutely larger in carnivores than herbivores. Diurnal planktivores and nocturnal species of small body size maximise vision by having relatively large eyes. Anterior aphakic spaces were present in most of the species examined, and 25% of the species also had posterior aphakic spaces. Theoretical sensitivity was generally higher among nocturnal than diurnal species, however, a number of benthic and pelagic carnivores showed retinal specialization for enhanced sensitivity. Diurnal species displayed high spatial acuity, with maximum acuity occurring in carnivorous species. Crepuscular species had either high or low acuity, whereas that of nocturnal species was generally lower than in diurnal species. Ten species displayed regional variation in rod density, with crepuscular and nocturnal species showing streaks of high rod density in the retina. Eleven species of carnivores displayed regional variation in cone density, with highest density usually occurring in the caudal part of the retina. In most of the species with areas of high cone density, there was a forward visual axis that coincided with the location of the aphakic space, suggestive of accomodation along that axis.     

Australian Snakes Do Not Follow Bergmann’s Rule

Bergmann’s Rule (i.e., the tendency of body size to increase with decreasing environmental temperature) was originally explained by a mechanism that is unique to endotherms. Nevertheless, geographic variation of body size of ectotherms, including snakes, is increasingly studied, and some claim that the rule should apply to ectotherms, or to thermoregulating ectotherms. Such studies usually focus on assemblages or on species in a region, but mostly ignore species’ ecological and biological traits when seeking biogeographic patterns. We examined the relationship between environmental temperatures and body size of 146 Australian snake species. We examined this relationship while considering the effects of ecological traits (activity time and habitat use), climatic variables which are thought to influence snake body size, and shared ancestry. Our finding suggest that Bergmann’s Rule is not a valid generalization across species of Australian snakes. Furthermore, ecological traits greatly influence the relationship between snake body size and environmental temperature. Body size of fossorial species decreases with environmental temperature, whereas body size of nocturnal, surface active species increases. Body size of diurnal, surface active species is not related to environmental temperature. Our results indicate that lumping all species in a clade together is misleading, and that ecological traits profoundly affect the geographic variation of snake body size. Though environmental temperature generally does not exert a strong selective force on snake body size, this relationship differs for taxa exhibiting different ecological traits.     

The finely defined shift work schedule of dung beetles and their eye morphology

In nature, nothing is wasted, not even waste. Dung, composed of metabolic trash and leftovers of food, is a high‐quality resource and the object of fierce competition. Over 800 dung beetle species (Scarabaeinae) compete in the South African dung habitat and more than 100 species can colonize a single dung pat. To coexist in the same space, using the same food, beetles divide the day between them. However, detailed diel activity periods and associated morphological adaptations have been largely overlooked in these dung‐loving insects. To address this, we used a high‐frequency trapping design to establish the diel activity period of 44 dung beetle species in their South Africa communities. This allowed us to conclude that the dung beetles show a highly refined temporal partitioning strategy, with differences in peak of activity even within the diurnal, crepuscular, and nocturnal guilds, independent of nesting behavior and taxonomic classification. We further analyzed differences in eye and body size of our 44 model species and describe their variability in external eye morphology. In general, nocturnal species are bigger than crepuscular and diurnal species, and as expected, the absolute and relative eye size is greatest in nocturnal species, followed by crepuscular and then diurnal species. A more surprising finding was that corneal structure (smooth or facetted) is influenced by the activity period of the species, appearing flat in the nocturnal species and highly curved in the diurnal species. The role of the canthus—a cuticular structure that partially or completely divides the dung beetle eye into dorsal and ventral parts—remains a mystery, but the large number of species investigated in this study nevertheless allowed us to reject any correlation between its presence and the nesting behavior or time of activity of the beetles.     

Eye shape and the nocturnal bottleneck of mammals

Most vertebrate groups exhibit eye shapes that vary predictably with activity pattern. Nocturnal vertebrates typically have large corneas relative to eye size as an adaptation for increased visual sensitivity. Conversely, diurnal vertebrates generally demonstrate smaller corneas relative to eye size as an adaptation for increased visual acuity. By contrast, several studies have concluded that many mammals exhibit typical nocturnal eye shapes, regardless of activity pattern. However, a recent study has argued that new statistical methods allow eye shape to accurately predict activity patterns of mammals, including cathemeral species (animals that are equally likely to be awake and active at any time of day or night). Here, we conduct a detailed analysis of eye shape and activity pattern in mammals, using a broad comparative sample of 266 species. We find that the eye shapes of cathemeral mammals completely overlap with nocturnal and diurnal species. Additionally, most diurnal and cathemeral mammals have eye shapes that are most similar to those of nocturnal birds and lizards. The only mammalian clade that diverges from this pattern is anthropoids, which have convergently evolved eye shapes similar to those of diurnal birds and lizards. Our results provide additional evidence for a nocturnal ‘bottleneck’ in the early evolution of crown mammals.     

Testing the 'free radical theory of aging' hypothesis: physiological differences in long-lived and short-lived colubrid snakes

We test the 'free radical theory of aging' using six species of colubrid snakes (numerous, widely distributed, non-venomous snakes of the family Colubridae) that exhibit long (> 15 years) or short (< 10 years) lifespans. Because the 'rate of living theory' predicts metabolic rates to be correlated with rates of aging and oxidative damage results from normal metabolic processes we sought to answer whether physiological parameters and locomotor performance (which is a good predictor of survival in juvenile snakes) mirrored the evolution of lifespans in these colubrid snakes. We measured whole animal metabolic rate (oxygen consumption Vo2), locomotor performance, cellular metabolic rate (mitochondrial oxygen consumption), and oxidative stress potential (hydrogen peroxide production by mitochondria). Longer-lived colubrid snakes have greater locomotor performance and reduced hydrogen peroxide production than short-lived species, while whole animal metabolic rates and mitochondrial efficiency did not differ with lifespan. We present the first measures testing the 'free radical theory of aging' using reptilian species as model organisms. Using reptiles with different lifespans as model organisms should provide greater insight into mechanisms of aging.     

Sexual dimorphism, reproductive biology, and food habits of two species of African filesnakes (Mehelya, Colubridae)

The ecology and general biology of African snakes remains virtually unstudied, even in highly distinctive species such as the filesnakes (genera Mehelya and Gonionotophis ). Our measurements and dissections of preserved specimens provided information on body sizes, sexual dimorphism in size and bodily proportions, clutch sizes, and food habits of two Mehelya species. In both M. capensis and M. nyassae , females attain sexual maturity at the same size as conspecific males, but grow to much larger sizes. Mehelya capensis displays extreme differences in body shape between males and females at the same body length: females have longer and wider heads, thicker bodies, and larger eyes (relative to both head length and head width) than do conspecific males. Dimorphism in body proportions is less marked in M. nyassae. Female reproductive cycles are seasonal in M. capensis , and clutch sizes are larger in this species than in its smaller congener (5-11 eggs in M. capensis , 2-6 eggs in M. nyassae ).
Contrary to popular wisdom, Mehelya are not specialized ophiophages. Mehelya nyassae feeds primarily upon lygosomatine skinks, including many fossorial taxa. Mehelya capensis has a broader diet, feeding on a wide variety of terrestrial lizards (especially agamids and gerrhosaurids) and snakes. Toads are also common prey items. The diversity of prey types taken by M. capensis suggests that these snakes may use ambush predation as well as active foraging. Mehelya is strongly convergent with Asian elapids of the genus Bungarus in its morphology (triangular body shape; powerful jaws; visible interstitial skin), behaviour (nocturnality; reluctance to bite when harassed), and diet (feeding on elongate reptiles, including snakes). Observations of preyhandling and ingestion by captive snakes are needed to clarify possible selective forces for the evolution of the unusual traits shared by these taxa.     

Moving Day and Night: Highly Labile Diel Activity Patterns in a Tropical Snake

Most animals have well established diel activity patterns (e.g., diurnal, crepuscular, or nocturnal), and changes in behavior from diurnal to nocturnal are rare in single species. We radio tracked 50 keelback snakes in a single population, locating them up to four times a day, over five periods of the year in the Australian dry tropics to describe temporal variation in diel movement patterns. Snake body temperatures were also recorded to determine the relationship between activity patterns and body temperatures. Season influenced diel activity patterns significantly. Keelbacks were more likely to move, and moved further in the daytime in the mid‐dry (June–July), and late dry (Aug–Sep) seasons. In the mid‐dry season, 87 percent of movements were diurnal, whereas in the mid‐wet (Feb–March) season, although snakes were much more likely to move, only 43 percent of movements were diurnal. In the late dry season, snakes were slightly more likely to move at night than at any other time of day, and so at this time of the year, snakes could be classified as nocturnal. Thus, overall increased movements in the mid‐wet season (austral summer) were associated with more crepuscular and nocturnal movement. There was a significant relationship between individual snake body temperatures and movement rates in all seasons. Changes in movement patterns may be related to body temperature, and this diurnal species becomes cathemeral in the tropics in summer, when it is possible to maintain high body temperatures both day and night.     

Relationships between sexual dimorphism and niche partitioning within a clade of sea-snakes (Laticaudinae)

Previous studies in Fiji have shown that females of the amphibious sea-krait Laticauda colubrina are much larger than males, and have larger heads relative to body size. The dimorphism has been interpreted in terms of adaptation to a sex divergence in prey-size: females primarily eat large (conger) eels rather than smaller (moray) eels. The hypothesis that dimorphism is affected by niche divergence predicts that the degree of sex dimorphism will shift when such a species invades a habitat with a different range of potential prey sizes. On the island of Efate in Vanuatu, L. colubrina and a regionally endemic sibling species (L. frontalis) both consume smaller eels (in absolute terms, and relative to the snake's body size) than do the previously-studied Fijian snakes. Patterns of morphology and sexual dimorphism have shifted also. Both Vanuatu taxa are slender-bodied, and frontalis is smaller and less dimorphic than L. colubrina. Females grow larger than males in all taxa, and have larger heads (relative to body length), but the degree of sexual divergence is lower in Vanuatu (especially in frontalis). Dietary overlap (in prey species as well as size) is high between adult frontalis and juvenile colubrina, but the two taxa differ in prey size/predator size relationships. In particular, male frontalis eat very small prey and have very short heads. Our results are consistent with the hypothesis that sex differences in the mean adult body sizes and relative head sizes of laticaudine snakes are linked to sex differences in feeding biology.     

Species‐specific differences in relative eye size are related to patterns of edge avoidance in an Amazonian rainforest bird community

Eye size shows a large degree of variation among species, even after correcting for body size. In birds, relatively larger eyes have been linked to predation risk, capture of mobile prey, and nocturnal habits. Relatively larger eyes enhance visual acuity and also allow birds to forage and communicate in low‐light situations. Complex habitats such as tropical rain forests provide a mosaic of diverse lighting conditions, including differences among forest strata and at different distances from the forest edge. We examined in an Amazonian forest bird community whether microhabitat occupancy (defined by edge avoidance and forest stratum) was a predictor of relative eye size. We found that relative eye size increased with edge avoidance, but did not differ according to forest stratum. Nevertheless, the relationship between edge avoidance and relative eye size showed a nonsignificant positive trend for species that inhabit lower forest strata. Our analysis shows that birds that avoid forest edges have larger eyes than those living in lighter parts. We expect that this adaptation may allow birds to increase their active daily period in dim areas of the forest. The pattern that we found raises the question of what factors may limit the evolution of large eyes.     

Eye morphology in cathemeral lemurids and other mammals

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).     

Helminth infracommunity structure of the sympatric garter snakes Thamnophis eques and Thamnophis melanogaster from the Mesa Central of Mexico

Seventy-two Mexican garter snakes (Thamnophis eques) and 126 black-bellied garter snakes (T. melanogaster) were collected from 4 localities of the Mesa Central of Mexico between July 1996 and February 1998 and examined for helminths. Both species of garter snakes occurred sympatrically in every locality except in Lake Cuitzeo. Both species of snakes shared 9 helminth species, and in general, T. melanogaster hosted a larger number of species than T. eques. In each locality, a different helminth species showed the highest levels of prevalence and abundance (Spiroxys susanae in Ciénaga de Lerma, Telorchis corti in Lago de Pátzcuaro, Proteocephalus variabilis in Lago de Cuitzeo, and Contracaecum sp. in Lago de Chapala). Helminth communities in garter snakes of the Mesa Central are depauperate and dominated by a single parasite species. In those localities where the snakes occurred in sympatry, helminth communities were, in general, more diverse and species-rich in T. melanogaster. Differences in the ecology and physiology of these species of garter snakes may explain this pattern because black-bellied garter snakes (T. melanogaster) are more aquatic than Mexican garter snakes (T. eques) and primarily eat aquatic prey, potentially exposing themselves to a larger number of helminths transmitted by predator-prey infection. The helminth infracommunities of garter snakes in the Mesa Central of Mexico show a strong Nearctic influence because most of the species infecting these hosts have been recorded in other Nearctic colubrid snakes. However, the helminth infracommunities of these garter snakes are less species-rich and less diverse than those in colubrid snakes in more temperate latitudes. The widespread ecological perturbation of sampling sites in the Mesa Central because of human activity, and geographic differences in foraging ecology of the hosts and, thus, exposure to parasites transmitted by intermediate hosts may help to explain these patterns.     

Anatomical specializations for nocturnality in a critically endangered parrot, the Kakapo (Strigops habroptilus)

The shift from a diurnal to nocturnal lifestyle in vertebrates is generally associated with either enhanced visual sensitivity or a decreased reliance on vision. Within birds, most studies have focused on differences in the visual system across all birds with respect to nocturnality-diurnality. The critically endangered Kakapo (Strigops habroptilus), a parrot endemic to New Zealand, is an example of a species that has evolved a nocturnal lifestyle in an otherwise diurnal lineage, but nothing is known about its' visual system. Here, we provide a detailed morphological analysis of the orbits, brain, eye, and retina of the Kakapo and comparisons with other birds. Morphometric analyses revealed that the Kakapo's orbits are significantly more convergent than other parrots, suggesting an increased binocular overlap in the visual field. The Kakapo exhibits an eye shape that is consistent with other nocturnal birds, including owls and nightjars, but is also within the range of the diurnal parrots. With respect to the brain, the Kakapo has a significantly smaller optic nerve and tectofugal visual pathway. Specifically, the optic tectum, nucleus rotundus and entopallium were significantly reduced in relative size compared to other parrots. There was no apparent reduction to the thalamofugal visual pathway. Finally, the retinal morphology of the Kakapo is similar to that of both diurnal and nocturnal birds, suggesting a retina that is specialised for a crepuscular niche. Overall, this suggests that the Kakapo has enhanced light sensitivity, poor visual acuity and a larger binocular field than other parrots. We conclude that the Kakapo possesses a visual system unlike that of either strictly nocturnal or diurnal birds and therefore does not adhere to the traditional view of the evolution of nocturnality in birds.     

Osteological evidence for the evolution of activity pattern and visual acuity in primates

Examination of orbit size and optic foramen size in living primates reveals two adaptive phenomena. First, as noted by many authors, orbit size is strongly correlated with activity pattern. Comparisons of large samples of extant primates consistently reveal that nocturnal species exhibit proportionately larger orbits than diurnal species. Furthermore, nocturnal haplorhines (Tarsius and Aotus) have considerably larger orbits than similar-sized nocturnal strepsirrhines. Orbital hypertrophy in Tarsius and Aotus accommodates the enormously enlarged eyes of these taxa. This extreme ocular hypertrophy seen in extant nocturnal haplorhines is an adaptation for both enhanced visual acuity and sensitivity in conditions of low light intensity. Second, the relative size of the optic foramen is highly correlated with the degree of retinal summation and inferred visual acuity. Diurnal haplorhines exhibit proportionately larger optic foramina, less central retinal summation, and much higher visual acuity than do all other primates. Diurnal strepsirrhines exhibit a more subtle but significant parallel enlargement of the optic foramen and a decrease in retinal summation relative to the condition seen in nocturnal primates. These twin osteological variables of orbit size and optic foramen size may be used to draw inferences regarding the activity pattern, retinal anatomy, and visual acuity of fossil primates. Our measurements demonstrate that the omomyiforms Microchoerus, Necrolemur, Shoshonius, and Tetonius, adapiform Pronycticebus, and the possible lorisiform Plesiopithecus were likely nocturnal on the basis of orbit diameter. The adapiforms Leptadapis, Adapis, and Notharctus, the phylogenetically enigmatic Rooneyia, the early anthropoids Proteopithecus, Catopithecus, and Aegyptopithecus, and early platyrrhine Dolichocebus were likely diurnal. The activity pattern of the platyrrhine Tremacebus is obscure. Plesiopithecus, Pronycticebus, Microchoerus, and Necrolemur probably had eyes that were very similar to those of extant nocturnal primates, with a high degree of retinal summation and rod-dominated retinae. Leptadapis and Rooneyia likely had eyes similar to those of extant diurnal strepsirrhines, with moderate degrees of retinal summation, a larger cone:rod ratio than in nocturnal primates, and, more speculatively, well-developed areae centrales similar to those of diurnal strepsirrhines. Adapis exhibited uncharacteristically high degrees of retinal summation for a small-eyed (likely diurnal) primate. None of the adapiform or omomyiform taxa for which we were able to obtain optic foramen dimensions exhibited the extremely high visual acuity characteristic of extant diurnal haplorhines.     

Ontogenetic changes in retinal structure and visual acuity: a comparative study of coral-reef teleosts with differing post-settlement lifestyles

Changes in retinal structure during settlement were investigated in four species of tropical reef-associated teleost fishes with differing periods of planktonic duration and post-settlement lifestyles. They were: Apogon doederleini (Apogonidae), a nocturnal planktivore; Stethojulis strigiventer (Labridae), a diurnal microcarnivore; Upeneus tragula (Mullidae), a carnivore which uses chin barbels to disturb invertebrates from the sediment; and Pomacentrus moluccensis (Pomacentridae), a diurnal herbivorous planktivore. The densities of cones, rods, cells in the inner nuclear layer and cells in the ganglion cell layer were estimated in a size range of each species. Visual acuity was calculated using cone densities and lens diameter. The ontogenetic sequence of changes in cell density was similar in all species but interspecific variation in the timing and rates of change was found and could be related to lifestyle. For example, cone densities decreased and rod densities increased most rapidly in the nocturnal species, A. doederleini, during settlement. In contrast, high cone densities were maintained in the species adopting a diurnal lifestyle. Theoretical visual acuity was found to increase rapidly as lens size increased, but was similar for all species at similar lens sizes, indicating the importance of larger eye size as a means for improving resolution during early stages of eye growth. It was concluded that for the species undergoing abrupt lifestyle changes at settlement, structural re-organisation of the retina is important for the survival of the fish as they leave the pelagic environment and take up their reef-associated lifestyle.