Day and night in the subterranean: measuring daily activity patterns of subterranean rodents (Ctenomys aff. knighti) using bio-logging

Abstract

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.

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

“…Light-logger data indicated when the subterranean tucotucos were on surface during daylight and, consequently, the timing of their exposure to light. Daily surface emergences and light exposure occurred near the twilights during mid and late summer (Figure 1 and Supplementary Figure 3), contrasting with the pattern in winter (Flôres et al, 2016;Jannetti et al, 2019), when both were concentrated in the middle of the day (Figures 1, 2A). The two animals with longer deployment duration (Figure 1 #177 and #193) show the gradual transition between these two contrasting patterns during autumn.…”

“…We named field-activity duration the interval between activity onset and offset measured in the field. Field-activity duration was measured in the accelerometry data from 3 animals recaptured in summer in the current work and another 3 animals in autumn/winter from Jannetti et al (2019). The fourth summer animal with activity data did not show stable activity rhythms during the field condition, thus its data could not be used in this analysis.…”

“…Soil temperature was recorded by a buried temperature logger (HOBO R , Onset Computer Corporation, Bourne, MA; accuracy ± 0.5 • C from 0 to 50 • C) at 20 cm deep (T soil ). Data from external temperature at the surface (Jannetti et al, 2019) were obtained using a temperature logger inserted inside a taxidermied tuco-tuco exposed to the sun, to account for radiation and convection effects. This measurement is called operative temperature (T e ) (Chappell and Bartholomew, 1981).…”

“…The variables included had variance inflation factors (VIF) (Zuur et al, 2009) lower than 5. A total of 20 extreme values of T soil and T sur (more than 2 standard deviations or less than −2) were underrepresented in the datasets and were excluded to avoid bias, resulting in a sample size of 973 observations from 12 animals in the current summer data and 227 observations from 9 animals in the winter data published previously (Jannetti et al, 2019).…”

“…Four of the recaptured tuco-tucos (169.7 ± 46 g; 2 males; 2 females) had collars containing accelerometers. Data from 9 animals in winter and 1 animal in autumn were taken from Jannetti et al (2019) and used for comparisons between seasons.…”