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Torpor Capability in Two Gerbil Species, Meriones Unguiculatus and Tatera Indica

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Torpor Capability in Two Gerbil Species, Meriones Unguiculatus and Tatera Indica Jpn. J. Environ. Entomol. Zool. 27（1）：9－16（2016） 環動昆 第 27 巻 第 1 号：9－16（2016） Original Article Torpor capability in two gerbil species, Meriones unguiculatus and Tatera indica Daisuke Watanabe1,2)*, Mihoko Hatase3)*, Shinsuke H. Sakamoto3), Chihiro Koshimoto4), Akio Shinohara4) and Tetsuo Morita3) 1) Interdisciplinary Graduate School of Agriculture and Engineering, University of Miyazaki, Miyazaki 889-2192, Japan 2) Miyazaki City Phoenix Zoo, Miyazaki 880-0122, Japan 3) Faculty of Agriculture, University of Miyazaki, Miyazaki 889-2192, Japan 4) Divisions of Bio-Resources, Frontier Science Research Center, University of Miyazaki, Miyazaki 889-1692, Japan (Received : July 17, 2015 ; Accepted : February 3 ,2016) Abstract To determine whether or not gerbils possess a capability for torpor, we examined the effects of temperature, photoperiod and food availability on torpor expression in two species, the Mongolian gerbil, Meriones unguiculatus (Milne-Edwards, 1867) and the Indian gerbil, Tatera indica (Hardwicke, 1807). Some M. unguiculatus subjected to food deprivation became torpid only under short photoperiod conditions, while in T. indica, fasting lead to daily torpor under both long and short photoperiods. This demonstrated that both gerbils have the capability for fasting-induced torpor although incidences of torpor were low. In addition, the findings for M. unguiculatus suggest that short-day exposure may be a prerequisite for the expression of fasting-induced torpor in this species. On the other hand, only one instance of torpor was found under prolonged exposure to short photoperiods with ample food, in a female of M. unguiculatus. This is insufficient evidence to support the conclusion that spontaneous daily torpor occurs in these species. Key words : daily torpor, food deprivation, Meriones unguiculatus, short photoperiod, Tatera indica Introduction torpor on the other hand, was reported relatively recently by Tucker (1962), and is still rather poorly reported. Indeed, the Chronic shortages of water and food and large daily expression of daily torpor in many species is so subtle that it is fluctuations in ambient temperature make deserts and arid often overlooked and the list of species known to possess the lands particularly harsh environments for endotherms to capability remains far from complete. Previous studies suggest survive. That they do so at all is largely due to the development that among small mammals in arid habitats daily torpor may be of adaptations including mechanisms to conserve body water much more common than hibernation (Buffenstein, 1985; (Schmidt-Nielsen and Schmidt-Nielsen, 1952), food hoarding Buffenstein and Jarvis, 1985; Barfod and Wünnenberg, 1990; (Vander Wall, 1990), variable activity level (Gutman et al., Ehrhardt et al., 2005; Grimpo et al., 2013, 2014). 2007), and torpor (Barfod and Wünnenberg, 1990; Ehrhardt et Many small mammals with distribution ranges from mid to al., 2005; Grimpo et al., 2013, 2014). high latitudes in the northern hemisphere are known to display Torpor is normally defined as a sustained drop in metabolic daily torpor in response to short photoperiod (SP). As this rate and body temperature. This definition includes both torpor occurs regardless of abundance of food, it is referred as hibernation, in which bouts of torpor last more than 1 day, and spontaneous daily torpor (SDT). In general, SDT has been daily torpor, which occurs in shorter bouts lasting less than 24 regarded as a winter adaptation specific to seasonal climates hours. Thus the energy savings achieved due to depressed (Heldmaier et al., 1989). SDT is known to occur in the metabolism are more pronounced during hibernation than Djungarian hamster Phodopus sungorus (Pallas, 1773) during daily torpor (Geiser and Ruf, 1995; Geiser, 2004). (Heldmaier et al., 1989), the deer mouse Peromyscus Hibernation in endotherms has been known well biologically maniculatus (Wagner, 1845) (Lynch et al., 1978), the Korean since the 19th century (Dubois, 1896). The occurrence of daily field mouse Apodemus peninsulae (Thomas, 1906) (Masaki et Corresponding author:[email protected] - 9 - Watanabe et al. al., 2005) and the large Japanese field mouse Apodemus Experiment 1: Effects of photoperiod, food shortage and cold speciosus (Temminck, 1844) (Eto et al., 2014). On the other on body temperature (Tb) patterns of M. unguiculatus hand, daily torpor triggered by food shortage in any season is A total of 30 individuals of M. unguiculatus were assigned known as fasting-induced torpor (FIT) (Diedrich and to two experimental groups and exposed to different light Steinlechner, 2012). In contrast to SDT, FIT is deemed an regimes. The first group, comprising 9 males (87.8 ± 3.8 g: adaptation to unpredictable environments. FIT is known in the mean ± SE) and 9 females (76.9 ± 3.5 g) were maintained house mouse Mus musculus (Linnaeus, 1758) (Hudson and under long photoperiod (LP) conditions, whereby the ratio of Scott, 1979) and the pouched mouse Saccostomus campestris light to dark hours (L: D) was 16: 8 (lights on at 06:00 a.m.), (Peters, 1846) (Lovegrove and Raman, 1998), among others. for 2 weeks. The second group, of 7 males (89.4 ± 34.7 g) and The murid subfamily Gerbillinae includes at least 15 genera 5 females (69.8 ± 2.9 g) were acclimatized to a short and more than 80 extant species of gerbil, known to inhabit photoperiod (SP) (L: D = 8: 16, lights on at 10:00 a.m.) for 12 mainly deserts and arid lands. Knowledge relating to torpor weeks. Ta for both groups was regulated at 23 ± 2°C. Animals in gerbils is limited to findings in two species from the same were housed individually in aluminum cages (200×300×260 genus, namely the smallest African gerbil, Gerbillus pusillus mm) and fed a commercial laboratory rodent diet (CE-2: CLEA (Peters, 1878) (Buffenstein, 1985; Buffenstein and Jarvis, Japan, Inc., Tokyo). Under the each light regime, after a 1985) and the pale gerbil, Gerbillus perpallidus (Setzer, 1958) week-long control period of ad libitum feeding, animals were (Morita et al., 2004). In order to understand the torpor profile subjected to a further week of chronic food deprivation (FD) of gerbils generally, it is important to begin characterizing during which food was withdrawn for 14 hours of each day. torpidity in other members of the group. In this study, two Water continued to be supplied ad libitum. The animals were gerbil species originally inhabiting mid to high latitudes in the then allowed to recover for one week during which ad libitum northern hemisphere were subjected to food shortage, short feeding was re-instated, and then deprived of food for a full 48 photoperiod and/or cold in order to assess effects on hours (48h FD), after which they were allowed for a further thermoregulation and torpor capability. week-long recovery period again, with ad libitum feeding. Food deprivation started at 08:30 p.m. under LP, and at 06:00 Material and Methods p.m. under SP. In the next phase of the experiment, Ta was sharply reduced and the animals were exposed to 4 ± 2°C for The experimental procedures used in this study were 10 days. Food was provided ad libitum during this period of examined and approved by the Animal Experimentation cold exposure. Tb of all 30 animals was recorded throughout Committee at the University of Miyazaki (Permission No. the experimental period as described below. 2002-055). Experiment 2: Effects of photoperiod and food shortage on Tb in T. indica Experimental animals 16 experimental individuals of T. indica comprising 7 males The two gerbil species, the Mongolian gerbil, Meriones (130.5 ± 8.7 g) and 9 females (89.5 ± 4.5 g) were housed unguiculatus (Milne-Edwards, 1867) and the Indian gerbil, individually in plastic cages (276×445×204 mm) at 25 ± 3°C Tatera indica (Hardwicke, 1807) used in this study were raised of Ta and supplied with water and pelleted herbivore feed (ZF: to adulthood at the Department of Bio-resources, Division of Oriental Yeast Co., Ltd., Tokyo, Japan) ad libitum. All 16 Biotechnology, Frontier Science Research Center, University animals were exposed to LP conditions (L: D = 16: 8, lights on of Miyazaki, Japan. Animals were housed individually in at 06:00 a.m.) for a week during which ad libitum feeding plastic or aluminum cages, supplied with water and continued then placed on a chronic FD regime for a week when commercial laboratory rodent diet (CE-2: CLEA Japan, Inc., food was withdrawn for 14 hours per day. Subsequently, the Tokyo) or herbivore diet (ZF: Oriental Yeast Co., Ltd., Tokyo, same individuals (7 males and 9 females) were acclimatized to Japan) ad libitum under a 12L: 12D photoperiod and ambient SP conditions (L: D = 8: 16, lights on at 10:00 a.m.) with ad temperature (Ta) of 23°C. As a welfare consideration, it was libitum feeding for 12 weeks. A further one week control decided that a loss of more than 30% of initial body mass period with ad libitum was followed by a one week FD period, would terminate the experiment. with food withdrawn for 14 hours per day. Water was provided ad libitum throughout the experimental period. Tb was Experimental protocol recorded as described below. - 10 - Daily torpor in two gerbil sprcies Measurement of body temperature (Tb) Pharmaceutical Co. Ltd., Osaka, Japan). Prior to implantation, Body temperatures were recorded using Thermochron the data loggers were programmed to record Tb to the nearest iButtonTM data loggers (DS1921L-F51: Dallas Semiconductor 0.5°C every 30 minutes. The animals were allowed to recover Co., Dallas). The devices were coated with a thin layer of a from the surgery for 7 days before experimental recording paraffin-Evaflex mixture according to Eto et al. (2015), began. At the end of the experiment, the data loggers were whereby 1 part Evaflex vinyl resin (ethylene-vinyl acetate removed and the data retrieved to a personal computer using an copolymers: Du Point Mitsui Polychemical Co., Tokyo, Japan) adapter (DS1402D-DR8: Dallas Semiconductor Co., Dallas).
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