Fasting-Induced Daily Torpor in Desert Hamsters (Phodopus Roborovskii)
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Comparative Biochemistry and Physiology, Part A 199 (2016) 71–77 Contents lists available at ScienceDirect Comparative Biochemistry and Physiology, Part A journal homepage: www.elsevier.com/locate/cbpa Fasting-induced daily torpor in desert hamsters (Phodopus roborovskii) Qing-Sheng Chi a, Xin-Rong Wan a,FritzGeiserb, De-Hua Wang a,⁎ a State Key Laboratory of Integrated Management for Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China b Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, New South Wales 2351, Australia article info abstract Article history: Daily torpor is frequently expressed in small rodents when facing energetically unfavorable ambient conditions. Received 4 December 2015 Desert hamsters (Phodopus roborovskii, ~20 g) appear to be an exception as they have been described as homeo- Received in revised form 12 May 2016 thermic. However, we hypothesized that they can use torpor because we observed reversible decreases of body Accepted 18 May 2016 temperature (T ) in fasted hamsters. To test this hypothesis we (i) randomly exposed fasted summer-acclimated Available online 20 May 2016 b hamsters to ambient temperatures (Tas) ranging from 5 to 30 °C or (ii) supplied them with different rations of Keywords: food at Ta 23 °C. All desert hamsters showed heterothermy with the lowest mean Tb of 31.4 ± 1.9 °C (minimum, Ambient temperature 29.0 °C) and 31.8 ± 2.0 °C (minimum, 29.0 °C) when fasted at Ta of 23 °C and 19 °C, respectively. Below Ta 19 °C, Body temperature the lowest Tb and metabolic rate increased and the proportion of hamsters using heterothermy declined. At Ta Desert hamster (Phodopus roborovskii) 5 °C, nearly all hamsters remained normothermic by increasing heat production, suggesting that the Food shortage heterothermy only occurs in moderately cold conditions, perhaps to avoid freezing at extremely low Tas. During Heterothermy heterothermy, Tbs below 31 °C with metabolic rates below 25% of those during normothermia were detected in Torpor four individuals at Ta of 19 °C and 23 °C. Consequently, by definition, our observations confirm that fasted desert hamsters are capable of shallow daily torpor. The negative correlation between the lowest Tbs and amount of food supply shows that heterothermy was mainly triggered by food shortage. Our data indicate that summer- acclimated desert hamsters can express fasting-induced shallow daily torpor, which may be of significance for energy conservation and survival in the wild. © 2016 Elsevier Inc. All rights reserved. 1. Introduction et al., 2007, 2013). Desert hamsters are active year-round and usually hoard food to cope with the fluctuation of food availability Torpor is defined as a state of profound but controlled reductions of (Feoktistova and Meschersky, 2005; Wan et al., 2007; Müller et al., metabolic rate and body temperature (Tb) in endotherms. Many small 2015). They are known to be non-hibernating animals and daily torpor mammals can reduce their energy expenditure by expressing torpor could not be confirmed in a previous study, neither under summer- nor to cope with daily or seasonal fluctuations of environmental conditions under winter-like conditions (Jefimow, 2007). In contrast, we observed like low ambient temperature (Ta) or low food availability (McNab, reversible decrease of Tb below 30.0 °C in fasted hamsters at Ta 23 °C 2002; Geiser, 2004). Torpor is traditionally divided into two categories: under long photoperiod (Chi and Wang, 2011). Similarly, Ushakova daily torpor and hibernation. Compared to the multiday duration and et al. (2012) reported substantially decreased Tbs in winter-acclimated profound reduction of metabolic rate during hibernation, daily torpor individuals under semi-natural conditions. Thus, desert hamsters lasts less than one day, is usually less profound and closely related to might be a potentially heterothermic species, but their pattern of torpor the circadian rhythm (Ruf and Geiser, 2015). Mammals capable of has never been quantified. torpor are widely distributed in most recent mammalian orders and Siberian hamsters (Phodopus sungorus), an intensely studied the number of heterothermic species is likely to be higher than known congener, express spontaneous daily torpor mainly as a response to at present (Geiser and Ruf, 1995; Ruf and Geiser, 2015). prolonged short photoperiod exposure even when food is available ad Desert hamsters (Phodopus roborovskii SATUNIN) mainly inhabit the libitum (Heldmaier and Steinlechner, 1981; Kirsch et al., 1991; Ruf desert regions of north Asia, characterized by harsh and cold winters and Heldmaier, 1992). In long photoperiod, Siberian hamsters display (Ross, 1994). They are small, nocturnal, granivorous rodents with fasting-induced daily torpor after severe food restriction and a reduc- body mass around 20 g (Bao et al., 2002; Zhan and Wang, 2004; Wan tion in body mass of about 25% (Ruby and Zucker, 1992; Diedrich et al., 2015). A further congener named Campbell hamsters (Phodopus campbelli) was also found to be heterothermic (Ushakova et al., 2012; ⁎ Corresponding author at: Institute of Zoology, Chinese Academy of Sciences, 1 BeichenXilu, Chaoyang, Beijing 100101, China. Müller et al., 2015). In several other heterotherms, such as small rodents E-mail address: [email protected] (D.-H. Wang). and marsupials, daily torpor often occurs when food is restricted under http://dx.doi.org/10.1016/j.cbpa.2016.05.019 1095-6433/© 2016 Elsevier Inc. All rights reserved. 72 Q.-S. Chi et al. / Comparative Biochemistry and Physiology, Part A 199 (2016) 71–77 moderate cold conditions (Geiser, 2004; Hudson and Scott, 1979; 2.4. Metabolic trials Tannenbaum and Pivorun, 1987; Nespolo et al., 2010; Geiser and Martin, 2013). Metabolic rates were measured as oxygen consumption with an Because the profound and reversible decrease of Tb in fasted desert open flow respirometry system (Sable Systems, TurboFOX Complete hamsters, we hypothesized that they are able to express daily torpor Field System, including a mass-flow meter) by placing each animal when facing food shortage at certain Tas. To test this hypothesis and to into a transparent plastic chamber (TSE, type I for mice, Volume 2.7 L) quantify the thermal energetics of desert hamsters under different ther- with small pieces of paper to absorb animal wastes. An incubator mal and trophic conditions, we exposed fasted hamsters to different Tas (Yiheng Model LRH-250, Shanghai, China) was used to maintain and investigated the effects of food availability at Ta 23 °C, at which the constant ambient conditions within the animal chamber during the maximum decreases of Tb were previously detected and the hamsters measurement intervals at a series of Tas from 5 °C to 30 °C (±0.5 °C) were routinely maintained. Tb and/or metabolic rate were monitored (Thermal neutral zone, TNZ, 25–33 °C, Zhan and Wang, 2004). Fresh continuously during the experiments. air from outside was pumped through the chamber at 500– 600 ml/min. Before entering the chamber, air passed through a copper 2. Material and methods coil to ensure that its temperature was adjusted to that inside the incu- bator. After passing through the chamber, the gas was subsampled and 2.1. Animals and housing dried using a non-chemical gas drier (Sable Systems, ND-2); approxi- mately 100 ml/min at a stable flow rate was analyzed. Baseline mea- Adult hamsters (12 to 18 months old) used in this study were off- surements of reference air outside the animal chamber were carried spring of 30 pairs, live-trapped in Hunshandake sandy land (43°11′N, out every 4 h to compensate for the drift of the oxygen sensor during 116°10′E, minimum Ta −30.3 °C, field observation with iButton, long-term metabolic rate monitoring. Maxim Model DS1922L) of Inner Mongolia. According to our records, Oxygen consumption was calculated using the equation: the life span of desert hamsters in laboratory conditions was around 36 months. They were raised individually in standard plastic cages FR Â ðÞFiO2‐FeO2 −FR Â FeO2 Â ðÞFeCO2−FiCO2 VO2 ¼ (30 cm × 15 cm × 20 cm) with saw dust and wood shavings under 1−FeO2 photoperiod conditions of 16 h light and 8 h darkness at Ta 23 ± 1 °C. Hamsters had ad libitum access to standard rodent maintenance pellets (FR = mass flow rate, FiO2 = input fractional concentration of O2 to the (crude protein, ≥18%; crude fat, ≥4%; coarse fiber, ≤5%; ashes, ≤8%; chamber, FeO2 = excurrent fractional concentration of O2 from the moisture, ≤10%) (Beijing HFK Bio-Technology Co. Ltd.) and water. The chamber, FiCO2 = input fractional concentration of CO2, FeCO2 =excur- use of these animals in this study was permitted by the Animal Care rent fractional concentration of CO2 from the chamber) (Hill, 1972; and Use Committee of Institute of Zoology, the Chinese Academy of Withers, 1977). We took the 5-min least variable and lowest VO2 Sciences. average as resting metabolic rate (RMR) after the animal had been at rest for at least 30 min (Li et al., 2010; Chi and Wang, 2011). 2.2. Surgery 2.5. Body mass and daily food intake determination About two weeks before the beginning of the experiments, each of the 34 desert hamsters (16 males and 18 females) was implanted intra- Animals were provided with a pre-weighed quantity of food in ex- peritoneally with a battery-free temperature-sensitive transponder cess. Uneaten food together with feces was collected after 3 days. (15.5 mm × 6.5 mm; 1.1 g) (Mini Mitter, Model G2 E-Mitter, made of Daily food intake was calculated for each animal. Feeding trials always biocompatible materials). Transponders had been calibrated by the started at around 1700 h and ended at the same time 3 days later. At company using a two point calibration (to the nearest of ±0.1 °C) and the beginning and end of each trial, body mass was measured with an an accuracy of ±0.15 °C over a temperature range of 20 °C–45 °C was electronic balance (Sartorius Model BL1500, to the nearest 0.1 g).