Synchronization of biological rhythms to the 24-hour day/night has long been studied with model organisms, under artificial light/dark cycles in the laboratory. The commonly used rectangular light/dark cycles, comprising hours of continuous light and darkness, may not be representative of the natural light exposure for most species, including humans. Subterranean rodents live in dark underground tunnels and offer a unique opportunity to investigate extreme mechanisms of photic entrainment in the wild. Here, we show automated field recordings of the daily light exposure patterns in a South American subterranean rodent, the tuco-tuco (Ctenomys aff. knighti ). In the laboratory, we exposed tuco-tucos to a simplified version of this natural light exposure pattern, to determine the minimum light timing information that is necessary for synchronization. As predicted from our previous studies using mathematical modeling, the activity rhythm of tuco-tucos synchronized to this mostly simplified light/dark regimen consisting of a single light pulse per day, occurring at randomly scattered times within a day length interval. Our integrated semi-natural, lab and computer simulation findings indicate that photic entrainment of circadian oscillators is robust, even in face of artificially reduced exposure and increased phase instability of the synchronizing stimuli.

While most studies of the impacts of climate change have investigated shifts in the spatial distribution of organisms, temporal shifts in the time of activity is another important adjustment made by animals in a changing world. Due to the importance of light and temperature cycles in shaping activity patterns, studies of activity patterns of organisms that inhabit extreme environments with respect to the 24-hour cyclicity of Earth have the potential to provide important insights into the interrelationships among abiotic variables, behaviour and physiology. Our previous laboratory studies with Argentinean tuco-tucos from the Monte desert (Ctenomys aff. knighti) show that these subterranean rodents display circadian activity/rest rhythms that can be synchronized by artificial light/dark cycles. Direct observations indicate that tuco-tucos emerge mainly for foraging and for removal of soil from their burrows. Here we used bio-logging devices for individual, long-term recording of daily activity/rest (accelerometry) and time on surface (light-loggers) of six tuco-tucos maintained in outdoor semi-natural enclosures. Environmental variables were measured simultaneously. Activity bouts were detected both during day and night but 77% of the highest values happened during the daytime and 47% of them coincided with time on surface. Statistical analyses indicate time of day and temperature as the main environmental factors modulating time on surface. In this context, the total duration that these subterranean animals spent on surface was high during the winter, averaging 3 h per day and time on surface occurred when underground temperature was lowest. Finally, transport of these animals to the indoor laboratory and subsequent assessment of their activity rhythms under constant darkness revealed a switch in the timing of activity. Plasticity of activity timing is not uncommon among desert rodents and may be adaptive in changing environments, such as the desert where this species lives.

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.

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.