Temporal Dissociation Between Activity and Body Temperature Rhythms of a Subterranean Rodent (Ctenomys famosus) in Field Enclosures.

Several wild rodents, such as the subterranean tuco-tucos (Ctenomys famosus), switch their time of activity from diurnal to nocturnal when they are transferred from field to the laboratory. Nevertheless, in most studies, different methods to measure activity in each of these conditions were used, which raised the question of whether the detected change in activity timing could be an artifact. Because locomotor activity and body temperature (Tb) rhythms in rodents are tightly synchronized and because abdominal Tb loggers can provide continuous measurements across field and laboratory, we monitored Tb as a proxy of activity in tuco-tucos transferred from a semi-field enclosure to constant lab conditions. In the first stage of this study ("Tb-only group," 2012-2016), we verified high incidence (55%, n = 20) of arrhythmicity, with no consistent diurnal Tb rhythms in tuco-tucos maintained under semi-field conditions. Because these results were discrepant from subsequent findings using miniature accelerometers (portable activity loggers), which showed diurnal activity patterns in natural conditions (n = 10, "Activity-only group," 2016-2017), we also investigated, in the present study, whether the tight association between activity and Tb would be sustained outside the lab. To verify this, we measured activity and Tb simultaneously across laboratory and semi-field deploying both accelerometers and Tb loggers to each animal. These measurements (n = 11, "Tb + activity group," 2019-2022) confirmed diurnality of locomotor activity and revealed an unexpected loosening of the temporal association between Tb and activity rhythms in the field enclosures, which is otherwise robustly tight in the laboratory.

Telling the Seasons Underground: The Circadian Clock and Ambient Temperature Shape Light Exposure and Photoperiodism in a Subterranean Rodent.

Living organisms anticipate the seasons by tracking the proportion of light and darkness hours within a day-photoperiod. The limits of photoperiod measurement can be investigated in the subterranean rodents tuco-tucos (Ctenomys aff. knighti), which inhabit dark underground tunnels. Their exposure to light is sporadic and, remarkably, results from their own behavior of surface emergence. Thus, we investigated the endogenous and exogenous regulation of this behavior and its consequences to photoperiod measurement. In the field, animals carrying biologgers displayed seasonal patterns of daily surface emergence, exogenously modulated by temperature. In the laboratory, experiments with constant lighting conditions revealed the endogenous regulation of seasonal activity by the circadian clock, which has a multi-oscillatory structure. Finally, mathematical modeling corroborated that tuco-tuco's light exposure across the seasons is sufficient for photoperiod encoding. Together, our results elucidate the interrelationship between the circadian clock and temperature in shaping seasonal light exposure patterns that convey photoperiod information in an extreme photic environment.

Maximising survival by shifting the daily timing of activity.

Maximising survival requires animals to balance the competing demands of maintaining energy balance and avoiding predation. Here, quantitative modelling shows that optimising the daily timing of activity and rest based on the encountered environmental conditions enables small mammals to maximise survival. Our model shows that nocturnality is typically beneficial when predation risk is higher during the day than during the night, but this is reversed by the energetic benefit of diurnality when food becomes scarce. Empirical testing under semi-natural conditions revealed that the daily timing of activity and rest in mice exposed to manipulations in energy availability and perceived predation risk is in line with the model's predictions. Low food availability and decreased perceived daytime predation risk promote diurnal activity patterns. Overall, our results identify temporal niche switching in small mammals as a strategy to maximise survival in response to environmental changes in food availability and perceived predation risk.

Acute effects of light and darkness on the activity and temperature rhythms of a subterranean rodent, the Anillaco tuco-tuco.

Tuco-tucos from Anillaco (Ctenomys aff. knighti), are subterranean rodents that run vigorously on laboratory wheels during the night but are active during the day in semi-natural enclosures, where they surface for foraging and burrow maintenance, under intense sunlight. Several studies have shown that light causes opposite, inhibitory and stimulatory, "masking" effects on the activity levels between nocturnal and diurnal species, respectively. Because of the alternating subterranean/surface activity of tuco-tucos in nature during the day and their ability to shift from diurnal to nocturnal patterns in field-to-lab transitions, we assessed the acute effects of light and darkness on running wheel activity, general activity and body temperature. Adult males and females were kept in a LD 12:12 h regimen and exposed to light and dark pulses to verify masking effects in their rhythms. A first experiment consisted in submitting animals to light pulses of different illuminance during the dark phase. Clear inhibition of wheel-running activity occurred, being the response more pronounced as illuminance of the pulse increased, a response typically seen in nocturnal rodents. A second experiment consisted in submitting animals to light pulses during the dark phase, and later to dark pulses during the light phase. This protocol occurred three times in the conditions: 1) without a wheel, 2) with free access to a wheel, and 3) with a blocked wheel. Wheel running was inhibited and body temperature decreased in most animals during the light pulse, with little to no inhibition on general activity. Dark pulses during the light phase had no effect on wheel-running activity nor on general activity but did affect body temperature. Interestingly, there was a single individual that switched from nocturnal to diurnal when kept without a running wheel, offering an opportunity to test nocturnal and diurnal masking patterns to light in the same individual.

The Interplay of Energy Balance and Daily Timing of Activity in a Subterranean Rodent: A Laboratory and Field Approach.

The tuco-tuco (Ctenomys aff. knighti) is among the rodent species known to be nocturnal under standard laboratory conditions and diurnal under natural conditions. The circadian thermoenergetics (CTE) hypothesis postulates that switches in activity timing are a response to energetic challenges; daytime activity reduces thermoregulatory costs by consolidating activity to the warmest part of the day. Studying wild animals under both captive and natural conditions can increase understanding of how temporal activity patterns are shaped by the environment and could serve as a test of the CTE hypothesis. We estimated the effects of activity timing on energy expenditure for the tuco-tuco by combining laboratory measurements of metabolic rate with environmental temperature records in both winter and summer. We showed that, in winter, there would be considerable energy savings if activity is allocated at least partially during daylight, lending support to the CTE hypothesis. In summer, the impact of activity timing on energy expenditure is small, suggesting that during this season other factors, such as predation risk, water balance, and social interaction, may have more important roles than energetics in the determination of activity time.

Nocturnal to Diurnal Switches with Spontaneous Suppression of Wheel-Running Behavior in a Subterranean Rodent.

Several rodent species that are diurnal in the field become nocturnal in the lab. It has been suggested that the use of running-wheels in the lab might contribute to this timing switch. This proposition is based on studies that indicate feed-back of vigorous wheel-running on the period and phase of circadian clocks that time daily activity rhythms. Tuco-tucos (Ctenomys aff. knighti) are subterranean rodents that are diurnal in the field but are robustly nocturnal in laboratory, with or without access to running wheels. We assessed their energy metabolism by continuously and simultaneously monitoring rates of oxygen consumption, body temperature, general motor and wheel running activity for several days in the presence and absence of wheels. Surprisingly, some individuals spontaneously suppressed running-wheel activity and switched to diurnality in the respirometry chamber, whereas the remaining animals continued to be nocturnal even after wheel removal. This is the first report of timing switches that occur with spontaneous wheel-running suppression and which are not replicated by removal of the wheel.

Rhythmic 24 h variation of core body temperature and locomotor activity in a subterranean rodent (Ctenomys aff. knighti), the tuco-tuco.

The tuco-tuco Ctenomys aff. knighti is a subterranean rodent which inhabits a semi-arid area in Northwestern Argentina. Although they live in underground burrows where environmental cycles are attenuated, they display robust, 24 h locomotor activity rhythms that are synchronized by light/dark cycles, both in laboratory and field conditions. The underground environment also poses energetic challenges (e.g. high-energy demands of digging, hypoxia, high humidity, low food availability) that have motivated thermoregulation studies in several subterranean rodent species. By using chronobiological protocols, the present work aims to contribute towards these studies by exploring day-night variations of thermoregulatory functions in tuco-tucos, starting with body temperature and its temporal relationship to locomotor activity. Animals showed daily, 24 h body temperature rhythms that persisted even in constant darkness and temperature, synchronizing to a daily light/dark cycle, with highest values occurring during darkness hours. The range of oscillation of body temperature was slightly lower than those reported for similar-sized and dark-active rodents. Most rhythmic parameters, such as period and phase, did not change upon removal of the running wheel. Body temperature and locomotor activity rhythms were robustly associated in time. The former persisted even after removal of the acute effects of intense activity on body temperature by a statistical method. Finally, regression gradients between body temperature and activity were higher in the beginning of the night, suggesting day-night variation in thermal conductance and heat production. Consideration of these day-night variations in thermoregulatory processes is beneficial for further studies on thermoregulation and energetics of subterranean rodents.

Modeling natural photic entrainment in a subterranean rodent (Ctenomys aff. knighti), the Tuco-Tuco.

Subterranean rodents spend most of the day inside underground tunnels, where there is little daily change in environmental variables. Our observations of tuco-tucos (Ctenomys aff. knighti) in a field enclosure indicated that these animals perceive the aboveground light-dark cycle by several bouts of light-exposure at irregular times during the light hours of the day. To assess whether such light-dark pattern acts as an entraining agent of the circadian clock, we first constructed in laboratory the Phase Response Curve for 1 h light-pulses (1000lux). Its shape is qualitatively similar to other curves reported in the literature and to our knowledge it is the first Phase Response Curve of a subterranean rodent. Computer simulations were performed with a non-linear limit-cycle oscillator subjected to a simple model of the light regimen experienced by tuco-tucos. Results showed that synchronization is achieved even by a simple regimen of a single daily light pulse scattered uniformly along the light hours of the day. Natural entrainment studies benefit from integrated laboratory, field and computational approaches.

Field and laboratory studies provide insights into the meaning of day-time activity in a subterranean rodent (Ctenomys aff. knighti), the tuco-tuco.

South American subterranean rodents (Ctenomys aff. knighti), commonly known as tuco-tucos, display nocturnal, wheel-running behavior under light-dark (LD) conditions, and free-running periods >24 h in constant darkness (DD). However, several reports in the field suggested that a substantial amount of activity occurs during daylight hours, leading us to question whether circadian entrainment in the laboratory accurately reflects behavior in natural conditions. We compared circadian patterns of locomotor activity in DD of animals previously entrained to full laboratory LD cycles (LD12:12) with those of animals that were trapped directly from the field. In both cases, activity onsets in DD immediately reflected the previous dark onset or sundown. Furthermore, freerunning periods upon release into DD were close to 24 h indicating aftereffects of prior entrainment, similarly in both conditions. No difference was detected in the phase of activity measured with and without access to a running wheel. However, when individuals were observed continuously during daylight hours in a semi-natural enclosure, they emerged above-ground on a daily basis. These day-time activities consisted of foraging and burrow maintenance, suggesting that the designation of this species as nocturnal might be inaccurate in the field. Our study of a solitary subterranean species suggests that the circadian clock is entrained similarly under field and laboratory conditions and that day-time activity expressed only in the field is required for foraging and may not be time-dictated by the circadian pacemaker.