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).     

Why be diurnal? Or, why not be cathemeral?

As a behavioural strategy, cathemerality is thought to confer considerable advantages by allowing animals to extend activity flexibly into either the diurnal or nocturnal phase in response to the prevailing ecological conditions. Factors such as temperature, access to food sources and minimising the risk of predation are all thought to be important in promoting cathemerality, although previous studies have produced inconsistent results. This paper adopts a different approach by first asking whether an obligate diurnal species, the chacma baboon (Papio hamadryas ursinus), exhibits seasonal variation in behavioural flexibility in response to annual cycles of day length. While short day lengths are an important constraint on the activity of the baboons at De Hoop Nature Reserve, South Africa, long summer days permit considerable flexibility in thermoregulatory response, diet selection and patterns of habitat choice. Given that baboons adapt flexibly in response to a relaxation of time constraints, the question thus arises as to why diurnal and nocturnal primates do not adopt cathemeral activity patterns when time is constrained? For baboons, the costs of predation appear to prohibit exploitation of the nocturnal phase and it is likely that such constraints are true of most primates. It thus follows that Madagascar's predatory environment must in some way permit or select for a cathemeral lifestyle. The importance of the predation by fossa (Cryptoprocta ferox) on the evolution of cathemerality is discussed.     

(Un‐)expected nocturnal activity in “Diurnal” Lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation

The ability to operate during the day and at night (i.e., cathemerality) is common among mammals but has rarely been identified in primates. Adaptive hypotheses assume that cathemerality represents a stable adaptation in primates, while nonadaptive hypotheses propose that it is the result of an evolutionary disequilibrium arising from human impacts on natural habitats. Madagascar offers a unique opportunity to study the evolution of activity patterns as there we find a monophyletic primate radiation that shows nocturnal, diurnal, and cathemeral patterns. However, when and why cathemeral activity evolved in lemurs is the subject of intense debate. Thus far, this activity pattern has been regularly observed in only three lemurid genera but the actual number of lemur species exhibiting this activity is as yet unknown. Here we show that the ring‐tailed lemur, Lemur catta, a species previously considered to be diurnal, can in fact be cathemeral in the wild. In neighboring but distinct forest areas these lemurs exhibited either mainly diurnal or cathemeral activity. We found that, as in other cathemeral lemurs, activity was entrained by photoperiod and masked by nocturnal luminosity. Our results confirm the relationship between transitional eye anatomy and physiology and 24‐h activity, thus supporting the adaptive scenario. Also, on the basis of the most recent strepsirrhine phylogenetic reconstruction, using parsimony criterion, our findings suggest pushing back the emergence of cathemerality to stem lemurids. Flexible activity over 24‐h could thus have been one of the key adaptations of the early lemurid radiation possibly driven by Madagascar's island ecology. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Diurnality and nocturnality in nonhuman primates: comparative chronobiological studies in laboratory and nature

Looking for differences in circadian clock characteristics of diurnal and nocturnal nonhuman primates, this article summarizes results of chronobiological studies carried out in various nocturnal, diurnal, and cathemeral prosimian and anthropoid primate species under controlled laboratory conditions, under seminatural conditions, and in the wild. In almost all circadian parameters investigated, no differences were discernible between the two main chrono-ecotypes, either in circadian period length and the influence upon it of after-effects, of light intensity, and ambient temperature, or in the PRC, re-entrainment behavior, rhythm splitting, and internal desynchronization. Diurnal and nocturnal or cathemeral species differed only in the phase of artificial or natural LDs to which their circadian activity phase was adjusted as well as in the characteristics of masking activity upon the rhythms produced by the direct inhibiting or enhancing effects of light. Pronounced lunar periodicity—observed in the activity rhythm of nocturnal neotropical owl monkeys, genus Aotus, in seminatural and natural environments as well as in wild cathemeral Malagasy lemurs, genus Eulemur—is shown to result from masking effects of moonlight. In captive Eulemur fulvus albifrons, a change from dark-active over cathemeral to light-active behavior, without concurrently changing the circadian phase-setting of activity to D, was produced by direct masking effects of a stepwise reduction of darktime luminosity on an LD 12:12 cycle. Long-term activity recordings carried out in wild diurnal Malagasy sifakas (Propithecus verreauxi) and cathemeral redfronted lemurs (Eulemur fulvus rufus), as well as in wild nocturnal owl monkeys (Aotus a. azarai) of the North Argentinean Chaco, yielded in all species distinct bimodal long- and short-day activity patterns with pronounced peaks during dusk and dawn. Applying Pittendrigh's two-oscillator concept to these results, it is hypothesized that the differences in chrono-ecotype behavior may result from variations in internal coupling and external phase-setting of morning and evening oscillators (m, e) to dawn and dusk, interacting with direct masking effects of light.     

Chronobiological background to cathemerality: circadian rhythms in Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea)

Cathemeral activity, in which the animals' motor activity is almost evenly distributed throughout the dark and the light portion of the day, has been described in various lemur genera (Eulemur, Hapalemur) and in the owl monkey Aotus azarai of the Argentinean Chaco. Proximate and ultimate factors responsible for this behaviour are still being debated. However, the chronobiological background of the behaviour has largely been ignored. We studied E. fulvus albifrons and A. a. boliviensis under controlled laboratory conditions to assess whether their activity rhythm is endogenously regulated by a circadian timing system that obeys general rules found in other mammals, or whether there are characteristic differences. To this end, we carried out long-term activity recordings on individuals of both subspecies kept under constant light and various light-dark cycles (LDs) using a PC-controlled electro-acoustic device in combination with telemetric body temperature measurements. Both subspecies developed free-running circadian activity and body temperature rhythms with periods deviating from 24 h in constant light, and LDs turned out to be the most efficient Zeitgeber synchronizing this endogenous rhythmicity to the external 24-hour day. The luminosity prevailing during the dark time of the LD had a decisive effect on levels of activity in the lemurs and induced strong masking effects on their circadian activity pattern. The results indicate that, from a chronobiological viewpoint, both species should be considered as dark active primates. Their diel activity rhythm is regulated by a normally responding circadian timing system and strong activity inhibiting or enhancing direct effects of light intensity. Thus, hypotheses on proximate and/or ultimate factors of cathemerality in primates must also consider its circadian background.     

Evolutionary disequilibrium and activity period in primates: a bayesian phylogenetic approach

Activity period plays a central role in studies of primate origins and adaptations, yet fundamental questions remain concerning the evolutionary history of primate activity period. Lemurs are of particular interest because they display marked variation in activity period, with some species exhibiting completely nocturnal or diurnal lifestyles, and others distributing activity throughout the 24-h cycle (i.e., cathemerality). Some lines of evidence suggest that cathemerality in lemurs is a recent and transient evolutionary state (i.e., the evolutionary disequilibrium hypothesis), while other studies indicate that cathemerality is a stable evolutionary strategy with a more ancient history. Debate also surrounds activity period in early primate evolution, with some recent studies casting doubt on the traditional hypothesis that basal primates were nocturnal. Here, we used Bayesian phylogenetic methods to reconstruct activity period at key points in primate evolution. Counter to the evolutionary disequilibrium hypothesis, the most recent common ancestor of Eulemur was reconstructed as cathemeral at ～9-13 million years ago, indicating that cathemerality in lemurs is a stable evolutionary strategy. We found strong evidence favoring a nocturnal ancestor for all primates, strepsirrhines and lemurs, which adds to previous findings based on parsimony by providing quantitative support for these reconstructions. Reconstructions for the haplorrhine ancestor were more equivocal, but diurnality was favored for simian primates. We discuss the implications of our models for the evolutionary disequilibrium hypothesis, and we identify avenues for future research that would provide new insights into the evolution of cathemerality in lemurs.     

The Social Systems of Gregarious Lemurs: Lack of Convergence with Anthropoids due to Evolutionary Disequilibrium?

The gregarious lemurs of Madagascar show a lack of convergence with anthropoid primates in several social, demographic, morphological and ecological features. They lack sexual dimorphism in canine and body size, and live in groups with equal adult sex ratios that can vary in composition from pairs to larger units. In most species, females dominate males, and have brief and often synchronized estruses. Finally, lemurs are often active during both day and night (i.e. cathemeral). Three hypotheses for this lack of convergence are discussed. The traditional explanation is that Madagascar's unique ecological pressures have forced females to exclude males from access to limiting resources, selecting for the other unique features as means to maintain female dominance over males. This idea is not logically consistent and is also poorly supported empirically. The second hypothesis claims that cathemerality imposes unique constraints on lemur social organization. The social behavior of cathemeral taxa is largely consistent with this idea. However, the social organization of the diurnal species is not. The third hypothesis claims that recent ecological changes, in particular the demise of large diurnal raptors, have produced a mismatch between current activity periods and adaptations to activity period. This idea is supported by a review of morphological adaptations to light conditions among lemurs, and, more generally, by a comparative analysis of cathemerality among tropical forest mammals. We conclude that the social systems of non-nocturnal lemurs are best considered as groups formed by species adapted to live in pairs. However, we cannot conclusively exclude the possibility that cathemeral activity is an old and stable activity pattern among lemurs. We indicate which data would decide the issue, and discuss the implications for views of social evolution of lemurs and other animals.     

Predation and cathemerality. Comparing the impact of predators on the activity patterns of lemurids and ceboids

The removal, or absence, of predatory species could be a contributing proximate factor to the rise of primate cathemerality. But predators themselves can also be cathemeral, so cathemerality could well be an evolutionary stable strategy. From a comparative perspective, it appears that the effect of predatory species cannot provide a unitary explanation for cathemerality. Varying distributions and population densities of predators, especially raptors, may be key factors in owl monkey (Aotus) cathemerality, but temperature and lunar cycle variation have also been implicated. In Madagascar, while raptors are potential predators of lemur species, the cathemerality of Eulemur species coincides with that of the fossa (Cryptoprocta ferox), a major predatory threat to lemurs. Thus, lemurid cathemerality may be more parsimoniously explained as an evolutionary stable strategy.     

A re-evaluation of the role of vision in the activity and communication of nocturnal primates

This paper examines the importance of vision in the lives of nocturnal primates in comparison to diurnal and cathemeral species. Vision is the major sense in all primates and there is evidence that the eyesight of nocturnal species is more acute and variable than has previously been recognized. Case studies of the behaviour of a galago and a loris in open woodland habitats in relation to ambient light show that Galago moholi males are more likely to travel between clumps of vegetation along the ground when the moon is up, and during periods of twilight, whereas they retreat to more continuous vegetation and travel less when the moon sets. This is interpreted as a strategy for avoiding predators that hunt on the ground when it is dark. The travel distances of Loris lydekkerianus are not affected by moonlight but this species reduces its choice of food items from more mobile prey to mainly ants when the moon sets, indicating the importance of light when searching for high-energy supplements to its staple diet. Evidence is presented for the first time to indicate key aspects of nocturnal vision that would benefit from further research. It is suggested that the light and dark facial markings of many species convey information about species and individual identity when animals approach each other at night. Differences in the colour of the reflective eye-shine, and behavioural responses displayed when exposed to white torchlight, point to different kinds of nocturnal vision that are suited to each niche, including the possibility of some degree of colour discrimination. The ability of even specialist nocturnal species to see well in broad daylight demonstrates an inherent flexibility that would enable movement into diurnal niches. The major differences in the sensitivity and perceptual anatomy of diurnal lemurs compared to diurnal anthropoids, and the emergence of cathemerality in lemurs, is interpreted as a reflection of evolution from different ancestral stocks in very different ecosystems, and not a recent shift towards diurnality due to human disturbance.     

Influence of abiotic factors on cathemeral activity: the case of Eulemur fulvus collaris in the littoral forest of Madagascar

The role environmental factors play in influencing circadian rhythms in natural habitats is still poorly described in primates, especially for those taxa with an activity cycle extended over the 24-hour cycle. In this paper, we elucidate the importance of abiotic factors in entraining the activity of cathemeral primates, focussing on results from a long-term study of Eulemur fulvus collaris (collared brown lemur) in south-eastern Malagasy littoral forest. Two groups of lemurs were followed for 60 whole-day and 59 whole-night observation periods over 14 months. Diurnal and nocturnal observations were equally distributed among moon phases and seasons. Temperature and humidity were recorded hourly by automatic data loggers. The littoral forest has a climatic environment where rainfall and humidity are uncorrelated with temperature and photoperiod. Diurnal and nocturnal activity varied seasonally, with the former increasing significantly with extended day length and the latter increasing significantly with shortened day length. Dusk seemed to act as a primary zeitgeber for these lemurs, coordinating the onset of evening activity throughout the entire year. Lunar phase and the nocturnal luminosity index correlated positively with the duration of nocturnal activity and negatively with the length of diurnal activity. Temperature was positively associated with diurnal activity but did not seem to influence lemur rhythms at night. Finally, lemur nocturnal activity significantly decreased when levels of humidity and rainfall were high. Cathemeral biorhythm is triggered by zeitgebers and influenced by masking factors. The activity of collared brown lemurs appears to be seasonally influenced by photoperiod and directly modulated by nocturnal ambient luminosity. These results are discussed by comparing data from other cathemeral species living in various climatic situations.     

Polyphasic activity patterns in small mammals

Cathemeral species are routinely active during the day, the night and at twilight. For the majority of species it is advantageous to specialize on the environmental conditions of a particular phase of the 24-hour day, so this rather uncommon type of activity must be a consequence of specific constraints. Good examples are the polyphasic activity patterns found in some small mammals. In shrews, with small body size and extremely high metabolic rate, polyphasic activity represents a simple short-term hunger cycle. In voles the short-term rhythm is triggered by an additional endogenous ultradian clock that interacts with the common circadian system, which probably is functionally related to endosymbiont digestion of cellulose-rich food. The activity bouts of individuals are synchronized on the population level to spread predation risk. As cathemeral species, voles are not specifically adapted to particular light conditions, but they are also not restricted to a particular activity phase. Therefore, the benefits from flexible responses in activity timing to environmental challenges may compensate for the disadvantages of not being specialized.     

Nocturnal activity in the cathemeral red-fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse

Several ecological and physiological factors have been suggested to structure circadian activity in cathemeral primates, i.e., those that are regularly active both day and night, but their relative importance remains controversial. We studied the nocturnal activity of a group of cathemeral redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest in Western Madagascar to examine its relationship with one environmental factor, ambient light levels, in detail. To this end, nightly travel distances and moon luminosity were determined between March and June 1996. During this transitional period between the wet and dry seasons these red-fronted lemurs were regularly active at night, and traveled significantly larger distances during full-moon nights compared to new-moon nights. The importance of ambient luminosity for nocturnal activity was highlighted by observations during a total lunar eclipse (i.e., during a full-moon night), which caused abrupt cessation of the animal's activity. Our results support the hypothesis that nocturnal activity of these cathemeral lemurs is regulated also by changes in ambient light levels.     

Opsin biosynthesis and trans-cis isomerization of aldehyde form chromophore in the blowfly Calliphora erythrocephala eye

The effect of eye carotenoid content, light conditions and retinoid supply on the biosynthesis of opsin, as well as the ability to isomerize of exogenous all-trans-retinal to 11-cis-retinal were investigated in the photoreceptors of blowfly Calliphora. SDS-PAGE of digitonin extracts from isolated rhabdom fractions of carotenoid-fortified and carotenoid-deficient animals revealed, on heavily loaded gels, that in both cases opsin forms faint minor bands similar to the patterns of “R⁻-flies” described as “vitamin A-deficient flies” (Paulsen and Schwemer, Biochim. biophys Acta 557, 358–390, 1979) or “carotenoid-deficient flies” (Paulsen and Schwemer, Eur. J. Biochem. 137, 609–614, 1983. Similar opsin patterns were obtained in flies subjected to continuous 72 h blue or yellow-green light or to a 12 h: 12 h white light:dark cycle, or total darkness, irrespective of the carotenoid content in their eyes. 11-cis-retinal and, to a lesser extent, all-trans-retinal, when included in the diet or painted on the cornea, were found to stimulate opsin biosynthesis in the dark. 11-cis-retinal in the dark or all-trans-retinal after illumination of the flies with blue light were the most effective, as compared with the effect of all-trans-retinal in the dark. Exogenous all-trans-retinal in the dark can be partially converted into a mixture of 11-cis-retinal (26%) and 13-cis-retinal (74%) by fly retina homogenate in vitro. It was concluded that Calliphora opsin biosynthesis is not strongly dependent on the carotenoid supply or on light: dark conditions and is triggered by the 11-cis aldehyde form of the chromophore, which can be produced in the fly retina either by an isomerase system in the dark or as a result of photoisomerization.     

Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)?

In group-living Malagasy primates (Lemuriformes), certain demographic and morphological traits deviate both from theoretical expectations derived from sexual selection theory and from patterns in better-known anthropoid primates. Lemurs lack sexual dimorphism in body and canine size and live in relatively small multimale-multifemale groups with, on average, even adult sex ratios, despite a polygynous mating system. In addition, the majority of gregarious lemurs are cathemeral, that is, they are regularly active both day and night. The social system of cathemeral lemurs has been considered an adaptation to their activity pattern. If so, groups should consist of multiple pairs that aggregate during diurnal activity and range separately at night in response to predation and infanticide risk, respectively. Moreover, mating privileges should exist between pair partners. We tested this hypothesis with data collected on two groups of wild redfronted lemurs in western Madagascar during 1023 focal animal hours spanning 4 months including the mating season. In addition, data on spatial relations were collected on 12 nights. We found no differences in group cohesion between day and night and no behavioural evidence for multiple male-female pairs. Instead, one male in each group monopolized social interactions with all females. However, females copulated with all resident males, although most often with the central male. Thus, basic predictions of the cathemerality hypothesis are unsupported. Multiple matings and indications of oestrous synchrony can be viewed as female counterstrategies against infanticide, whereas reproductive strategies of redfronted lemur males remain obscure. Copyright 1999 The Association for the Study of Animal Behaviour.     

Nocturnal ranging by a diurnal primate: are ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>) cathemeral?

Cathemerality, an activity pattern comprised of distinct periods of diurnal and nocturnal activity, is a trait found among several of the Malagasy strepsirhines and one species of Aotus. Because occasional anecdotal reports suggest that some diurnal primates can be active at night, I investigated the possibility of nocturnal ranging behavior in the ring-tailed lemur (Lemur catta) by using global positioning system (GPS) collars programmed to collect data across a 24-h period. Five individuals in a provisioned, free-ranging L. catta colony on St. Catherines Island, Georgia, USA, wore GPS collars across 1 week of the mating season. Results revealed that night ranging behavior occurred between the h of 1900 and 0530. An evaluation of the effect of moonlight on nocturnal activity showed that a greater rate of travel occurred during moonlit periods as opposed to periods when the moon had not yet risen. Distance travelled at night decreased across the deployment period, likely because of a decrease in available moonlight over time, as the lemurs were collared during a waning moon. Fewer mating opportunities over time may have also been responsible for the decrease in night ranging, because the number of females in estrus declined across the deployment period. Future research is needed to separate the effects of moonlight and mating activity on night ranging in this species, as well as to evaluate whether L. catta in Madagascar show night ranging similar to L. catta on SCI. These data raise the possibility that L. catta may be cathemeral, with an activity pattern fluctuating between diurnality and cathemerality in accordance with shifts in environmental conditions.     

Stratified activity: Vertical partitioning of the diel cycle by rainforest mammals in Borneo

Animal activity is driven by the environmental conditions and physical structure of a habitat, and the need to interact with, or avoid, other animals. Knowledge of the proportion of the 24-hour cycle spent active (activity level), and the time/s of day in which activity is concentrated (activity pattern), informs our understanding of species' ecology and community dynamics. In multidimensional habitats such as tropical rainforests, arboreal (canopy-dwelling) taxa comprise up to three-quarters of vertebrate assemblages; yet, wildlife surveys are typically limited to ground level. Terrestrial-only sampling can result in activity metrics that do not take account of species' full use of horizontal and vertical habitat space. We paired ground- and canopy-level camera traps to characterize mammal activity across vertical strata in Borneo. Additionally, we sampled unlogged and recovering-logged rainforest to evaluate whether this activity was impacted by logging. Activity across vertical strata varied substantially among 37 species. Arboreal mammals were predominantly nocturnal or diurnal but never cathemeral, terrestrial mammals were mostly nocturnal or cathemeral, and semi-arboreal mammals appeared to fill the temporal niches under-utilized by other groups. Differences in activity between unlogged and recovering-logged forest were minimal, with 92% of species found in both forest types retaining the same activity pattern. Our study demonstrates that the inclusion of canopy-based sampling provides much greater insights into overall rainforest mammal activity than terrestrial sampling alone. Our results suggest that the varying opportunities and constraints of each stratum act in concert to influence the diel patterns of tropical mammals. Abstract in Malay is available with online material.     

Further studies on the involvement of the circadian system in photoperiodic control of antifreeze protein production in the beetle Dendroides canadensis

The role of circadian rhythmicity in the photoperiodic time measuring processes regulating antifreeze protein production in the beetle Dendroides canadensis was further investigated. Using “T” experiments larvae were exposed to environmental light cycle periods close to the period length of the endogenous circadian oscillator. The following light cycles were employed: light/dark 8/13, 8/14, 8/16, 8/18 and 8/19 corresponding to period lengths of 21, 22, 24, 26 and 27 h. Larvae maintained in cycles equal to or less than 24 h displayed a characteristic short-day response, showing significantly (P < 0.01) greater antifreeze protein activity than did those measured on the day of collection in late summer. In contrast, a long-day response was observed in larvae maintained under a 26- or 27-h light cycle in that antifreeze protein activity did not differ from that measured on the initial collection date.

The role of photoperiod and temperature in influencing the photoperiodic timing processes were examined with a series of resonance experiments. The first group consisted of a 24, 36, 48, 60 or 72-h light cycle, each with an 8-h photophase at temperatures of 20 or 17°C. Rhythmic increases in antifreeze protein levels at intervals of 24 h occurred under both temperatures. However, the lower temperature displaced the resonance curve in the vertical direction (i.e. increasing % population response) and reduced the difference between peaks and troughs on the resonance curve. Resonance experiments incorporating a 14-h photophase resulted in low antifreeze protein activity under all conditions except a 36-h light cycle in which a 67% induction was observed.

Eight hour resonance experiments were also conducted with D. canadensis collected in early spring to determine whether the circadian system participates in the photoperiodic timing processes influencing the spring termination of antifreeze protein production. Positive resonance results were obtained in that only larvae maintained in cycles of 36 and 60 h displayed significantly (P < 0.01) lower antifreeze activity when compared to animals on the initial collection date.

The combined results emphasize the involvement of the circadian system in the photoperiodic control of antifreeze protein production by D. canadensis during the fall and spring. Furthermore, the induction of antifreeze protein production is a function of light cycle and its waveform (photoperiod). Temperature appears to modify the photoperiodic response in some manner involving the photoperiodic time measuring processes. It is concluded that the photoperiodic response of antifreeze protein production by D. canadensis is dependent upon the entrainment of the circadian system by the light cycle.     

Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap data and preliminary behavioral observations

Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered “strictly diurnal”. We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010–April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25 % of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5 % of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53 % nighttime, 43 % daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.     

Daily activity and light exposure levels for five species of lemurs at the duke lemur center

Light is the primary synchronizer of all biological rhythms, yet little is known about the role of the 24‐hour luminous environment on nonhuman primate circadian patterns, making it difficult to understand the photic niche of the ancestral primate. Here we present the first data on proximate light–dark exposure and activity–rest patterns in free‐ranging nonhuman primates. Four individuals each of five species of lemurs at the Duke Lemur Center (Eulemur mongoz, Lemur catta, Propithecus coquereli, Varecia rubra, and Varecia variegata variegata) were fitted with a Daysimeter‐D pendant that contained light and accelerometer sensors. Our results reveal common as well as species‐specific light exposure and behavior patterns. As expected, all five species were more active between sunrise and sunset. All five species demonstrated an anticipatory increase in their pre‐sunrise activity that peaked at sunrise with all but V. rubra showing a reduction within an hour. All five species reduced activity during mid‐day. Four of the five stayed active after sunset, but P. coquereli began reducing their activity about 2 hours before sunset. Other subtle differences in the recorded light exposure and activity patterns suggest species‐specific photic niches and behaviors. The eventual application of the Daysimeter‐D in the wild may help to better understand the adaptive evolution of ancestral primates. Am J Phys Anthropol 153:68–77, 2014. © 2013 Wiley Periodicals, Inc.     

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.