Research Article: Seasonal Patterns of Body Temperature Daily Rhythms in Group-Living Cape Ground Squirrels Xerus inauris

Date Published: April 27, 2012

Publisher: Public Library of Science

Author(s): Michael Scantlebury, Marine Danek-Gontard, Philip W. Bateman, Nigel C. Bennett, Mary-Beth Manjerovic, Kenneth E. Joubert, Jane M. Waterman, Mark Briffa. http://doi.org/10.1371/journal.pone.0036053

Abstract

Organisms respond to cyclical environmental conditions by entraining their endogenous biological rhythms. Such physiological responses are expected to be substantial for species inhabiting arid environments which incur large variations in daily and seasonal ambient temperature (Ta). We measured core body temperature (Tb) daily rhythms of Cape ground squirrels Xerus inauris inhabiting an area of Kalahari grassland for six months from the Austral winter through to the summer. Squirrels inhabited two different areas: an exposed flood plain and a nearby wooded, shady area, and occurred in different social group sizes, defined by the number of individuals that shared a sleeping burrow. Of a suite of environmental variables measured, maximal daily Ta provided the greatest explanatory power for mean Tb whereas sunrise had greatest power for Tb acrophase. There were significant changes in mean Tb and Tb acrophase over time with mean Tb increasing and Tb acrophase becoming earlier as the season progressed. Squirrels also emerged from their burrows earlier and returned to them later over the measurement period. Greater increases in Tb, sometimes in excess of 5°C, were noted during the first hour post emergence, after which Tb remained relatively constant. This is consistent with observations that squirrels entered their burrows during the day to ‘offload’ heat. In addition, greater Tb amplitude values were noted in individuals inhabiting the flood plain compared with the woodland suggesting that squirrels dealt with increased environmental variability by attempting to reduce their Ta-Tb gradient. Finally, there were significant effects of age and group size on Tb with a lower and less variable Tb in younger individuals and those from larger group sizes. These data indicate that Cape ground squirrels have a labile Tb which is sensitive to a number of abiotic and biotic factors and which enables them to be active in a harsh and variable environment.

Partial Text

Organisms respond to cyclical variation in environmental conditions by entraining their endogenous biological rhythms [1], [2]. One such rhythm in endothermic species is that of body temperature (Tb), which is considered to be a consequence of the balance between heat production and heat dissipation [3]. In many taxa, Tb daily rhythms are influenced by diel and seasonal changes in photoperiod and ambient temperature (Ta) [4]–[9]. Indeed, the primary cues for seasonal acclimatization of the thermoregulatory system, which include changes in Tb daily rhythms, are photoperiod and temperature [10], [11]. Interestingly, little is known about which selective pressures may affect the evolution of heterothermy in endotherms. Indeed, it is unclear whether one should examine the effects of environmental variation on raw Tb data or use some index which can be comparable across species (e.g. ‘Heterothermy Index’, ‘HI’ [12]). Angilletta et al. (2010) [13] suggest that future empirical work should examine the potential “selective pressures imposed by regional and temporal heterothermy”. They identify several potential candidates which might cause Tb variations to evolve which include food and water availability, Ta and social huddling. For example, restricted food and water supplies and low Ta values should favor energy-saving reductions in Tb and temporal heterothermy. Implicit in their arguments is the fact that extremes of variation in Ta and in particular cyclical variations in Ta may result in adaptive variation in Tb daily rhythms [13]–[16]. For group-living animals, behaviors such as social huddling may be one mechanism to conserve water and energy [17], [18]. Minimization of thermoregulatory costs and water loss are thus seen as a possible selective pressure for aggregation [19]–[21]. For instance, huddling in newborn rabbit (Oryctolagus cuniculus) pups not only saves energy but also affects Tb daily rhythms [22]. Hence, Tb daily rhythms are likely to be affected by group size in social animals.

Of the 20 individuals originally implanted with dataloggers, eight were recaptured; six from the flood plain (two adults, four sub adults) and two from the woodland (two adults). Group sizes (i.e. the sizes of groups in which the eight animals lived) ranged from one to nine individuals. The implanted animals were regularly observed during the two weeks following implantation and no mortality or immigration was observed. We observed no signs of different behavior of the implanted squirrels compared to the others. There were significant daily rhythms of Tb in all of the eight individuals measured (Table 1, Fig. 1) with mean ±SD values of the mesor, amplitude and acrophase for the 23 week measurement period of 37.51±0.15°C, 1.13±0.08°C and 12∶33±2 min, respectively.

Living in hot arid environments can be stressful for small diurnal mammals since the availability of free water necessary to reduce body heat by evaporation is limited [49]. Consequently, evaporative cooling is often accompanied by behavioral and physiological mechanisms to dissipate heat such as the use of a thermal refuge or substrate [50] or heterothermy [13], [51]–[53]. In the current study, Cape ground squirrels were exposed to a wide seasonal and daily range of Ta and the Tbmesor of all individuals increased significantly as the season progressed. This indicates that Tb values, including both maximal and minimal Tb’s were higher on average when Ta values were higher. This will presumably serve to conserve their water and energy as a reduced Ta-Tb temperature gradient minimizes the need to keep cool by evaporation [15], [54], [55]. In addition, acrophase values became earlier over the measurement period, indicating that activity periods also became earlier [28], [56]. Ground squirrels in general have labile Tb’s [2], [5], [57]–[61], Tbamplitudes of different species may vary by 4–5°C and be accompanied by bouts of torpor or hibernation. This compares with Tb amplitude values of up to 4.1°C in Arabian oryx (Oryx leucoryx) [51] and 2.6°C in Arabian sand gazelles (Gazella subgutturosa marica) [52]. We found no evidence of torpor and recorded daily variation in Tb, of 5–6°C, which is greater than that noted in most other species and greater than noted by Wilson et al. (2010) [33] for Cape ground squirrels in a more mesic area (3.8°C amplitude); hence this probably reflects adaptation to an environment with high Ta values and large daily variations in Ta.

Source:

http://doi.org/10.1371/journal.pone.0036053