The Relationship between the Golden Spiny Mouse Circadian System and Its Diurnal Activity: An Experimental Field Enclosures and Laboratory Study

Examples of animals that switch activity times between nocturnality and diurnality in nature are relatively infrequent. Furthermore, the mechanism for switching activity time is not clear: does a complete inversion of the circadian system occur in conjunction with activity pattern? Are there switching centers downstream from the internal clock that interpret the clock differently? Or does the switch reflect a masking effect? Answering these key questions may shed light on the mechanisms regulating activity patterns and their evolution. The golden spiny mouse (Acomys russatus) can switch between nocturnal and diurnal activity. This study investigated the relationship between its internal circadian clock and its diurnal activity pattern observed in the field. The goal is to understand the mechanisms underlying species rhythm shifts in order to gain insight into the evolution of activity patterns. All golden spiny mice had opposite activity patterns in the field than those under controlled continuous dark conditions in the laboratory. Activity and body temperature patterns in the field were diurnal, while in the laboratory all individuals immediately showed a free‐running rhythm starting with a nocturnal pattern. No phase transients were found toward the preferred nocturnal activity pattern, as would be expected in the case of true entrainment. Moreover, the fact that the free‐running activity patterns began from the individuals' subjective night suggests that golden spiny mice are nocturnal and that their diurnality in their natural habitat in the field results from a change that is downstream to the internal clock or reflects a masking effect.     

The diversity of temporal niches in mammals

The division of animals into those that are diurnal (day-active) and those that are nocturnal (night-active) is widely recognized. However, closer examination of the selection of temporal niches by mammalian species reveals the existence of a gradient of diurnality between and within species, wherein “diurnal” and “nocturnal” are merely the opposite ends of a continuum. Evidence against a simple diurnal - nocturnal dichotomy includes the existence of species without any preference for time of day, species with a crepuscular pattern of activity, species containing both diurnal and nocturnal individuals, species containing individuals that spontaneously shift from a nocturnal to a diurnal activity pattern, species showing degrees of diurnality greater or smaller than those of other species, organismal variables exhibiting degrees of diurnality greater or smaller than those of other variables, and species having different temporal patterns under the effects of different environmental variables. Research on the neural processes responsible for temporal niche selection has revealed no fundamental difference between the circadian clocks of diurnal and nocturnal animals, but recent findings suggest that different output pathways from the clock in a given species may operate with different circadian phases, thus providing an explanation for why different body functions in the same individual are subjected to different temporal niche selections.     

The relationship between the golden spiny mouse circadian system and its diurnal activity: an experimental field enclosures and laboratory study

Examples of animals that switch activity times between nocturnality and diurnality in nature are relatively infrequent. Furthermore, the mechanism for switching activity time is not clear: does a complete inversion of the circadian system occur in conjunction with activity pattern? Are there switching centers downstream from the internal clock that interpret the clock differently? Or does the switch reflect a masking effect? Answering these key questions may shed light on the mechanisms regulating activity patterns and their evolution. The golden spiny mouse (Acomys russatus) can switch between nocturnal and diurnal activity. This study investigated the relationship between its internal circadian clock and its diurnal activity pattern observed in the field. The goal is to understand the mechanisms underlying species rhythm shifts in order to gain insight into the evolution of activity patterns. All golden spiny mice had opposite activity patterns in the field than those under controlled continuous dark conditions in the laboratory. Activity and body temperature patterns in the field were diurnal, while in the laboratory all individuals immediately showed a free-running rhythm starting with a nocturnal pattern. No phase transients were found toward the preferred nocturnal activity pattern, as would be expected in the case of true entrainment. Moreover, the fact that the free-running activity patterns began from the individuals' subjective night suggests that golden spiny mice are nocturnal and that their diurnality in their natural habitat in the field results from a change that is downstream to the internal clock or reflects a masking effect.     

Interspecific competition and torpor in golden spiny mice: two sides of the energy-acquisition coin

We studied the occurrence of torpor in golden spiny mice in a hot rocky desert near the Dead Sea. In this rodent assemblage, a congener, the nocturnal common spiny mouse, competitively excluded the golden spiny mouse from the nocturnal part of the diel cycle and forced it into diurnal activity; this temporal partitioning allows the two species to partition their prey populations, particularly in summer when the diet of the two species is comprised mainly of arthropods, and largely overlap. We studied the effect of the presence of the common spiny mice at two resource levels (natural food availability and food added ad libitum) on populations of golden spiny mice in four large outdoor enclosures: two with common spiny mice removed and two enclosures with populations of both species. We hypothesized that with interspecific competition and/or reduced resources, golden spiny mice will increase their use of torpor. As we expected, supplemented food reduced the total time spent torpid. In summer, when the different activity periods of the two species results in prey species partitioning, removal of the congener did not affect torpor in the golden spiny mouse. However, in winter, when insect populations are low and the two species of mice overlap in a largely vegetarian diet, removal of the common spiny mouse reduced torpor in golden spiny mice, whether food was supplemented or not. This result suggests that torpor, a mechanism that allows small mammals to sustain periods of low availability of resources or high energetic requirements, may also help them to tolerate periods of enhanced interspecific competition. This may be a significant short-term mechanism that reduces competition and hence increases fitness, in particular of individuals of the subordinate species whose accessibility to resources may be limited.     

Wheel-Running Activity Patterns of Five Species of Desert Rodents

In contrast to the extensive laboratory data on activity patterns in rodent species inhabiting temperate zones, much less is known about the activity patterns of desert rodents. In order to address this issue, we measured wheel-running activity patterns in males and females of five species of wild-trapped desert rodents (Dipodillus dasyurus, Gerbillus andersoni, Gerbillus pyramidum, Meriones shawi, and Acomys cahirinus) in long 'summer-like' and short, 'winter-like' day lengths. The specific goals of the present study were to characterize activity patterns in several desert rodent species in the laboratory and to determine if activity patterns are expressed in a seasonal or sexually dimorphic manner. Specifically, wheel-running was measured for 11 weeks in long days followed by 11 weeks in short days to test for photoperiodic entrainment as well as responsiveness to changes in the light-dark cycle. All animals exhibited rhythmic patterns of wheel-running with consistent onsets and offsets that had well-defined relations with the light-dark cycle. All individuals of G. andersoni showed nocturnal activity patterns. Most individuals of G. pyramidum had nocturnal activity patterns, but some individuals showed a short bout of activity at the beginning of the light period. Most individuals of D. dasyurus and M. shawi showed bimodal (i.e., nocturnal and diurnal) activity patterns, although some showed markedly nocturnal activity patterns. There was no sexual dimorphism in wheel running activity rhythms in any of the species examined. As expected, decreases in day length resulted in an overall increase in the duration of activity in all species. Collectively, these data provide an initial characterization of activity patterns within desert rodents in a controlled laboratory setting.     

Amplitude of the daily rhythm of body temperature in eleven mammalian species

The amplitude of the daily rhythm of body temperature was investigated in 11 species of small mammals. Recording equipment, housing and environmental conditions were identical for all species. Intraperitoneal temperature was measured by telemetry at 6 min intervals for 10 or more days. The results indicate that the amplitude of the body temperature rhythm is a species-specific trait in small mammals. Interspecies differences in amplitude are not a function of surface area (as determined by body size) but seem to relate to diurnality (nocturnal species displaying smaller amplitude than diurnal ones) and habitat (species from temperate habitats displaying smaller amplitude than species from desert and tropical habitats).     

Out of the dark: 350 million years of conservatism and evolution in diel activity patterns in vertebrates

Many animals are active only during a particular time (e.g., day vs. night), a partitioning that may have important consequences for species coexistence. An open question is the extent to which this diel activity niche is evolutionarily conserved or labile. Here, we analyze diel activity data across a phylogeny of 1914 tetrapod species. We find strong phylogenetic signal, showing that closely related species tend to share similar activity patterns. Ancestral reconstructions show that nocturnality was the most likely ancestral diel activity pattern for tetrapods and many major clades within it (e.g., amphibians, mammals). Remarkably, nocturnal activity appears to have been maintained continuously in some lineages for ～350 million years. Thus, we show that traits involved in local‐scale resource partitioning can be conserved over strikingly deep evolutionary time scales. We also demonstrate a potentially important (but often overlooked) metric of niche conservatism. Finally, we show that diurnal lineages appear to have faster speciation and diversification rates than nocturnal lineages, which may explain why there are presently more diurnal tetrapod species even though diurnality appears to have evolved more recently. Overall, our results may have implications for studies of community ecology, species richness, and the evolution of diet and communication systems.     

Activity Rhythms and Masking Response in the Diurnal Fat Sand Rat Under Laboratory Conditions

Daily rhythms are heavily influenced by light in two major ways. One is through photic entrainment of a circadian clock, and the other is through a more direct process, referred to as masking. Whereas entraining effects of photic stimuli are quite similar in nocturnal and diurnal species, masking is very different. Laboratory conditions differ greatly from what is experienced by individuals in their natural habitat, and several studies have shown that activity patterns can greatly differ between laboratory environment and natural condition. This is especially prevalent in diurnal rodents. We studied the daily rhythms and masking response in the fat sand rat (Psammomys obesus), a diurnal desert rodent, and activity rhythms of Tristram’s jird (Meriones tristrami), a nocturnal member of the same subfamily (Gerbillinae). We found that most sand rats kept on a 12?h:12?h light-dark (LD) cycles at two light intensities (500 and 1000?lux) have a nocturnal phase preferences of general activity and higher body temperature during the dark phase. In most individuals, activity was not as stable that of the nocturnal Tritram’s jirds, which showed a clear and stable nocturnal activity pattern under the same conditions. Sand rats responded to a 6-h phase advance and 6-h phase delay as expected, and, under constant conditions, all tested animals free ran. In contrast with the nocturnal phase preference, fat sand rats did not show a masking response to light pulses during the dark phase or to a dark pulse during the light phase. They did, however, have a significant preference to the light phase under a 3.5?h:3.5?h LD schedule. Currently, we could not identify the underlying mechanisms responsible for the temporal niche switch in this species. However, our results provide us with a valuable tool for further studies of the circadian system of diurnal species, and will hopefully lead us to understanding diurnality, its mechanisms, causes, and consequences.     

Mammalian diurnality: some facts and gaps

A major factor contributing to the evolution of mammals was their ability to be active during the night, a niche previously underused by terrestrial vertebrates. Diurnality subsequently reemerged multiple times in a variety of independent lineages. This paper reviews some recent data on circadian mechanisms in diurnal mammals and considers general themes that appear to be emerging from this work. Careful examination of behavioral studies suggests that although subtle differences may exist, the fundamental functions of the circadian system are the same, as seems to be the case with respect to the molecular mechanisms of the clock. This suggests that responses to signals originating in the clock must be different, either within the SCN or at its targets or downstream from them. Some features of the SCN vary from species to species, but none of these has been clearly associated with diurnality. The region immediately dorsal to the SCN, which receives substantial input from it, exhibits dramatically different rhythms in nocturnal lab rats and diurnal grass rats. This raises the possibility that it functions as a relay that transforms the signal emitted by the SCN and transmits different patterns to downstream targets in nocturnal and diurnal animals. Other direct targets of the SCN include neurons containing orexin and those containing gonadotropin-releasing hormone, and both of these populations of cells exhibit patterns of rhythmicity that are inverted in at least one diurnal compared to one nocturnal species. The patterns that emerge from the data on diurnality are discussed in terms of the implications they have for the evolution and neural substrates of a day-active way of life.     

Diurnality and Nocturnality in Primates: An Analysis from the Rod Photoreceptor Nuclei Perspective

Diurnality, associated with enhanced visual acuity and color vision, is typical of most modern Primates. However, it remains a matter of debate when and how many times primates re-acquired diurnality or returned to nocturnality. We analyzed the features specific to nocturnal and diurnal vision that were recently found in the nuclei of mammalian rod photoreceptor cells in 11 species representing various groups of the Primates and related tree shrew and colugo. In particular, heterochromatin in rod nuclei of nocturnal mammals is clustered in the center of rod nuclei (inverted architecture), whereas rods of diurnal mammals retain rods with peripheral heterochromatin (conventional architecture). Rod nuclei of the nocturnal owl monkey have a state transitional to the inverted one. Surprisingly, rod nuclei of the tarsier have a conventional nuclear architecture typical for diurnal mammals, strongly implying that recent Tarsiiformes returned to nocturnality from the diurnal state. Diurnal lemurs retain inverted rod nuclei typical of nocturnal mammals, which conforms to the notion that the ancestors of all Lemuroidea were nocturnal. Data on the expression of proteins indispensable for peripheral heterochromatin maintenance (and, respectively, conventional or inverted nuclear organization) in rod cells support the view that the primate ancestors were nocturnal and transition to diurnality occurred independently in several primate and related groups: Tupaia, diurnal lemurs, and, at least partially independently, in Simiiformes (monkeys and apes) and Tarsiiformes.     

The effect of the lunar cycle on fecal cortisol metabolite levels and foraging ecology of nocturnally and diurnally active spiny mice

We studied stress hormones and foraging of nocturnal Acomys cahirinus and diurnal A. russatus in field populations as well as in two field enclosures populated by both species and two field enclosures with individuals of A. russatus alone. When alone, A. russatus individuals become also nocturnally active. We asked whether nocturnally active A. russatus will respond to moon phase and whether this response will be obtained also in diurnally active individuals. We studied giving-up densities (GUDs) in artificial foraging patches and fecal cortisol metabolite levels. Both species exhibited elevated fecal cortisol metabolite levels and foraged to higher GUDs in full moon nights; thus A. russatus retains physiological response and behavioral patterns that correlate with full moon conditions, as can be expected in nocturnal rodents, in spite of its diurnal activity. The endocrinological and behavioral response of this diurnal species to moon phase reflects its evolutionary heritage.     

Adaptive thermoregulation in golden spiny mice: the influence of season and food availability on body temperature

We studied the effect of food supplementation during summer and winter in seminatural field conditions on thermoregulation of a desert rodent, the golden spiny mouse Acomys russatus. We hypothesized that (a) under natural food availability (control conditions), mice will use less precise thermoregulation (i.e., an increase in the variance of body temperature [T(b)]) during winter because of low ambient temperatures (T(a)'s) and low food availability and during summer because of low food and water availability; (b) food supplementation will result in more precise thermoregulation during winter, but the effect will be smaller during summer because variation in T(b) in summer is also driven by water availability during that period. We found that under natural food availability, spiny mice thermoregulated more precisely during summer than during winter. They spent more time torpid during summer than during winter even when food was supplemented (although summer nights are shorter), allowing them to conserve water. Supplementing food resulted in more precise thermoregulation in both seasons, and mice spent less time torpid. In summer, thermoregulation at high T(a)'s was less precise, resulting in higher maximum T(b)'s in summer than in winter and when food was supplemented, in accord with the expected effect of water shortage on thermoregulation. Our results suggest that as expected, precise thermoregulation is beneficial when possible and is abandoned only when the costs of homeothermy outweigh the benefits.     

Effect of plant cover on seed removal by rodents in the Monte Desert (Mendoza,Argentina)

Abstract In desert areas, predation risk is one of the highest costs of foraging and is a major influence on animal behaviour. Several strategies are used by foragers for surviving and reproducing in desert areas. The foraging strategies of the small mammals of South American deserts are still poorly known. In this study, we investigated the foraging strategies of rodents of the Monte Desert in response to distance from seed sources to sheltered sites (i.e. shrubs) during two different seasons (wet and dry). We evaluated the relative rates of removal of two species of seeds (millet and sunflower) by rodents at two sites by establishing 80 seed sources, 40 in unsheltered microhabitats and 40 in sheltered microhabitats. We recorded both the number of caches and seed consumption for each source. We found that plant cover affected the foraging activity of rodents of the sand dunes in the Monte Desert because both consumption and numbers of caches constructed from sheltered seed sources were higher than those from unsheltered ones. Consumption of sunflower was higher in the wet season than it was in the dry season, when millet consumption increased. Sunflower was the preferred seed both from sheltered or unsheltered sources. We discuss the possible causes of the different foraging strategies used by rodents of the Monte Desert.     

Variability of diurnality in laboratory rodents

The locomotor activity rhythms of domestic mice, laboratory rats, Syrian hamsters, Siberian hamsters, Mongolian gerbils, degus, and Nile grass rats were compared. Running-wheel activity was monitored under a light–dark cycle with 12 h of light and 12 h of darkness per day. Nile grass rats were found to be reliably diurnal, whereas laboratory rats, Siberian hamsters, domestic mice, and Syrian hamsters were reliably nocturnal. Both diurnal and nocturnal subgroups were observed in Mongolian gerbils and degus. A downward gradient of diurnality was observed from Mongolian gerbils classified as diurnal, degus classified as diurnal, gerbils classified as nocturnal, and degus classified as nocturnal. Nocturnal degus remained nocturnal when tested with an infrared motion detector without running wheels. Thus, although the diurnal–nocturnal dichotomy could be applied to some of the species, it was not appropriate for others. The dichotomy may reflect researchers’ needs for systematization more than a natural distinction between species. Through mechanisms as yet poorly understood, the balance between entraining and masking processes seems to generate a gradient of temporal niches that runs from predominantly diurnal species to predominantly nocturnal species with many chronotypes in between, including species that exhibit wide intra-species gradients of temporal niche.     

Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice

Diurnally active golden spiny mice (Acomys russatus) and nocturnal common spiny mice (Acomys cahirinus) coexist in hot rocky deserts of Israel. Diurnal and nocturnal activities expose these species to different climatic conditions. Nonshivering thermogenesis (NST) capacity of individuals of both species immediately upon removal from the field exhibited seasonal changes, with no significant interspecific difference. Colony-reared mice of either species transferred in the laboratory from long to short photoperiod increased NST capacity, though to a lesser extent than observed in the seasonal acclimatization. The underlying biochemical mechanisms of short photoperiod acclimation differed between the species. In both Cytochrome-c oxidase (Cox) activity was higher in short as compared to long photoperiod. In short-photoperiod-acclimated A. cahirinus uncoupling protein (UCP) content in brown adipose tissue (BAT) was significantly higher than in long photoperiod, while in A. russatus there was no significant change. In A. russatus there was a significant increase in lipoprotein lipase (LPL) activity in BAT in short-photoperiod-acclimated individuals, while in A. cahirinus LPL activity was high under both acclimations. The low LPL activity in brown adipose tissue of desert-adapted A. russatus may facilitate lipid uptake in white adipose tissue, an advantage in desert conditions where food is scarce and irregularly distributed in space and time.     

Plasticity of Circadian Activity and Body Temperature Rhythms in Golden Spiny Mice

Most animals can be categorized as nocturnal, diurnal, or crepuscular. However, rhythms can be quite plastic in some species and vary from one individual to another within a species. In the golden spiny mouse (Acomys russatus), a variety of rhythm patterns have been seen, and these patterns can change considerably as animals are transferred from the field into the laboratory. We previously suggested that these animals may have a circadian time‐keeping system that is fundamentally nocturnal and that diurnal patterns seen in their natural habitat reflect mechanisms operating outside of the basic circadian time‐keeping system (i.e., masking). In the current study, we further characterized plasticity evident in the daily rhythms of golden spiny mice by measuring effects of lighting conditions and access to a running wheel on rhythms in general activity (GA) and body temperature (Tb). Before the wheel was introduced, most animals were active mainly during the night, though there was considerable inter‐individual variability and patterns were quite plastic. The introduction of the wheel caused an increase in the level of nighttime activity and Tb in most individuals. The periods of the rhythms in constant darkness (DD) were very similar, and even slightly longer in this study (24.1±0.2 h) than in an earlier one in which animals had not been provided with running wheels. We found no correlation between the distance animals ran in their wheels and the period of their rhythms in DD. Re‐entrainment after phase delays of the LD cycle occurred more rapidly in the presence than absence of the running wheel. The characteristics of the rhythms of golden spiny mice seen in this study may be the product of natural selection favoring plasticity of the circadian system, perhaps reflecting what can happen during an evolutionary transition as animals move from a nocturnal to a diurnal niche.     

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.     

Seed predation by birds and small mammals in semiarid Chile

We studied spatial and temporal patterns in foraging activity among diurnal birds and nocturnal mammals at a semiarid site in northern Chile using artificial foraging trays. Small mammals foraged more extensively under shrubs than in open microhabitats, but birds showed no such selection. Moreover, avian foraging was more extensive than that by small mammals in all seasons and both microhabitats. Avian foraging was highly seasonal, as many birds at our site migrate to the Andean prepuna or to Patagonia during the austral summer. Birds have tended to be overshadowed by small mammals and ants in studies of granivory, but this study suggests that their importance may be underestimated in some systems.     

Are rainforest owl monkeys cathemeral? Diurnal activity of black-headed owl monkeys, Aotus nigriceps, at Manu Biosphere Reserve, Peru

Members of the genus Aotus are traditionally considered strictly nocturnal, however, in recent years cathemeral habits have been described in a single species of owl monkey, Aotus azarai, which occur in the highly seasonal habitat of the Argentinean Chaco. This finding raises the question as to whether other species of Aotus exhibit cathemeral activity in less seasonal habitats. In this study, we observed the diurnal activity of one group of A. nigriceps living in the Manu Biosphere Reserve, Peru over 65 days. The data collected indicate that A. nigriceps has only sporadic diurnal bouts of activity. In addition, nocturnal luminosity of the previous night, rainfall, and temperature did not correlate with the minor diurnal activity exhibited. This suggests that for A. nigriceps the potential costs of shifting to diurnality may outweigh its prospective advantages in this rainforest environment.