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 , 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 , Meriones unguiculatus (Milne-Edwards, 1867) and the , 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 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 Phodopus sungorus (Pallas, 1773) during daily torpor (Geiser and Ruf, 1995; Geiser, 2004). (Heldmaier et al., 1989), the deer 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. in gerbils is limited to findings in two species from the same were housed individually in aluminum cages (200×300×260 , namely the smallest African gerbil, pusillus mm) and fed a commercial laboratory 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 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). was mixed with 5 parts paraffin to provide a coating with adequate plasticity at temperatures near 0°C. The coated data Definition of daily torpor and data handling loggers weighed approximately 3.1g and were surgically Torpor was defined as a reduction in body temperature implanted into the abdominal cavity of each animal under below 31°C according to Ruf and Heldmaier (1992). Tb traces anesthesia with pentobarbital (Nembutal: Dainippon were examined carefully in order to discriminate unintended bouts of mild hypothermia from torpor. The minimum Tb (A) (Tbmin) was the lowest Tb obtained during each experimental period. Torpor incidence was determined as the number of torpid animals / the number of animals observed.

Statistical analysis Statistical analyses were performed using JMP Ver.7.0.1a, (SAS Institute Inc. Cary NC, USA). Incidence of torpor was

compared between treatments using Fisher’s exact test. Tbmin in Experiment 1 was compared between treatments and between photoperiods using the Steel-Dwass test and the

Wilcoxon rank sum test, respectively. In Experiment 2, Tbmin was compared between treatments and between sexes using the Wilcoxon rank sum test.

(B)

Fig. 2 Transient hypothermia observed in a LP (Long photoperiod) female (M-f6) in M. unguiculatus during cold exposure. FD: food deprivation. M-f6: Animal ID.

Fig. 1 Tb patterns of a SP (short photoperiod) female (M-f5) (A) and a LP (long photoperiod) female (M-f8) (B) in M.

unguiculatus. Representative Tb traces in a torpid individual

(M-f5) (A) and a non-torpid individual (M-f8) (B). FD: food deprivation. M-f5; M-f8: Animal ID.

- 11 - Watanabe et al.

Results recovery period. In females, torpor incidence was 2/3 (Table 1). Under SP conditions, one female expressed torpor when Some individuals of M. unguiculatus and T. indica did subject to chronic FD and 48h FD and the other became torpid display episodes of daily torpor. during 48h FD. Among males, only one animal became torpid, under SP, during 48h FD. However, Fisher’s exact test Experiment 1: revealed no statistically significant effects of environmental Two of five females exposed to SP conditions died from conditions and sex on the torpor incidence (p > 0.05). seizures during routine cage changing, reducing the total Because of the small sample size for SP females and no number of SP females to three. Figs.1A and B compare the significant effect of sex, data of Tbmin from both sexes were Tb traces of torpid and non-torpid females under SP and LP pooled and analyzed by the Steel-Dwass test or the Wilcoxon conditions, respectively. Daily torpor was observed during rank sum test. Tbmin showed a significant decrease during chronic and 48h FD, and in one SP animal also during the chronic FD and 48h FD under both SP and LP conditions (Steel-Dwass test, p < 0.05). However the drop under LP was

never enough to constitute torpor. Tbmin was significantly (A) lower under SP than that under LP during chronic FD and 48h 40 FD (Wilcoxon rank sum test, p < 0.05). Furthermore, Tbmin was 38 significantly (Steel-Dwass test, p < 0.05) reduced by cold

36 exposure (Ta = 4 ± 2°C; Table 1) and one LP female exhibited an isolated episode of hypothermia at 30.5°C during the 10 day 34 period of cold exposure. However, unlike the repeatable bouts 32 of torpor elicited by FD (Fig. 1A), the Tb trace during the

Tb(°C) Tb(°C) 30 hypothermic episode lacked a smooth transition during cooling

28 and rewarming phases (Fig. 2). Thus, it appeared to be a relatively mild case of accidental hypothermia and was not 26 Chronic FD considered true daily torpor. 24 22 Experiment 2: 0 4 8 12 Day In this trial, one female did not recover well from surgery and three more showed substantial weight loss under food (B) deprivation. Furthermore, data from a fifth female was lost due 40 to a fault in the data logger. No data pertaining to these five 38 animals was used in the analysis.

36 Only female gerbils were observed expressing daily torpor during chronic FD under both SP and LP photoperiods, despite 34 the number of males in the study being greater. In females,

C) C) 32

° overall torpor incidence was 2/4. During chronic FD, one

Tb( 30 female exhibited torpor under SP conditions whereas the other became torpid under both light regimes (Table 2, Fig. 3). 28 None of the seven males in the study group showed any Chronic FD 26 incidence of daily torpor. No statistically significant effects of 24 environmental conditions and sex were found on the torpor

22 incidence (Fisher’s exact test, p > 0.05). Because of the small 0 4 8 12 sample size for females and no significant effect of Day photoperiod, Tbmin data from both photoperiods were pooled

Fig. 3 Tb patterns of a female T. indica (T-f9) acclimatized and analyzed by the Wilcoxon rank sum test. Tbmin was then to SP (short photoperiod) (A) and to LP (long photoperiod) found to decrease significantly (p < 0.05) during FD in females, (B). Representative Tb traces of torpid states in the same animal (T-f9) (A, B). FD: food deprivation. T-f9: Animal ID. but not in males.

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Table 1 Effect of environmental conditions on torpor parameters in M. unguiculatus Items Sex Photoperiod n Control Chronic FD 48h FD Cold exposure Torpor incidence Male Long 9 0/9 0/9 0/9 0/9 Short 7 0/7 0/7 1/7 0/7 Female Long 9 0/9 0/9 0/9 0/9 Short 3 0/3 1/3 2/3 0/3 Minimum Tb (°C) Male Long 9 35.0 (35.0-36.0) 34.5 (34.0-35.5) 34.5 (33.5-35.0) 34.0 (33.0-34.5) Short 7 35.0 (34.5-35.5) 33.5 (32.5-34.5) 33.0 (30.5-34.0) 33.5 (33.0-34.0) Female Long 9 35.0 (34.5-36.0) 34.5 (33.5-35.5) 34.0 (32.5-35.0) 33.5 (30.5-35.5) Short 3 34.5 (32.5-35.0) 32.5 (31.0-34.0) 29.5 (26.0-33.5) 33.0 (32.5-34.0)

Long 18 aX bX bX bX 35.0 (34.5-36.0) 34.5 (33.5-35.5) 34.0 (32.5-35.0) 34.0 (30.5-35.5) Short 10 aX bY bY bX 35.0 (32.5-35.5) 33.5 (31.0-34.5) 32.8 (26.0-34.0) 33.3 (32.5-34.0)

FD: food deprivation. Torpor incidence is shown as the number of torpid gerbils / the number of gerbils observed. Fisher’s

exact test revealed no statistically significant effects of environmental conditions and sex on the torpor incidence (p >

0.05). Tb values are shown as medians of ranges given in parentheses. a,b: different superscripts in the same row indicate

statistical difference (Steel-Dwass test, p < 0.05). X,Y: different superscripts in the same column indicate statistical

difference (Wilcoxon rank sum test, p < 0.05). Ranges with underscores include Tb drop below 31°C.

Table 2 Effect of environmental conditions on torpor parameters in T. indica

Items Sex Photoperiod n Control Chronic FD Torpor incidence Male Long 7 0/7 0/7 Short 7 0/7 0/7 Female Long 4 0/4 1/4 Short 4 0/4 2/4 Minimum Tb (°C) Male Long 7 34.0 (33.5-34.5) 33.5 (32.5-34.0) Short 7 34.0 (33.5-35.0) 35.0 (34.0-35.0) Female Long 4 33.3 (32.5-33.5) 29.5 (27.0-32.0) Short 4 34.0 (33.5-34.5) 31.8 (30.0-34.5)

Male 14 34.0 (33.5-35.0) aX 34.0 (32.5-35.0)aX aX bY Female 8 33.5 (32.5-34.5) 30.8 (27.0-34.5)

FD: food deprivation. Torpor incidence is shown as the number of torpid gerbils / the number of gerbils observed.

Fisher’s exact test revealed no statistically significant effects of environmental conditions and sex on the torpor

incidence (p > 0.05). Tb values are shown as medians of ranges given in parentheses. a,b: different superscripts in the

same row indicate statistical difference (Wilcoxon rank sum test, p < 0.05). X,Y: different superscripts in the same

column indicate statistical difference (Wilcoxon rank sum test, p < 0.05). Ranges with underscores include Tb drop

below 31°C.

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history of laboratory rearing. Thus, the low incidence is Discussion thought unlikely to be a solely a result of laboratory breeding. Torpor capability is known to differ between strains of inbred In M. unguiculatus, FD appeared to trigger daily torpor in mice (Dikic et al., 2008), suggesting that intra-species two females and one male under SP conditions as shown in variation in daily torpor may have a genetic basis. Table 1. In T. indica, FD also lead to daily torpor in two As previously indicated by Hudson (1978), the expression of females under SP and a single female under LP, as shown in daily torpor exhibits interindividual variation, and the two Table 2. These findings suggest that food shortage is an species of Gerbillinae used in this study included a environmental factor triggering torpor in these species, and considerable number of non-torpid individuals. In contrast, also that the torpor of T. indica is FIT, which manifests itself golden spiny mice Acomys russatus (Wagner, 1840), which as irrespective of season. Conversely, for M. unguiculatus, SP xeric-adapted share certain adaptations to hostile dry appears to be a pre-requisite for the expression of FIT. This habitats with gerbils, respond readily to food shortage with seems to be the first documentation of significant seasonality daily torpor (Grimpo et al., 2013). However, A. russatus in FIT. neither digs nor stores food (Shkolnik, 1966), leaving Meriones unguiculatus are originally distributed in daily torpor as one of its most important strategies for coping northeastern China and ranging from 35 to 52°N with unexpected food shortage and cold. By contrast, the two (Corbet, 1978; Corbet and Hill, 1991). Likewise, T. indica Gerbillinae species in this study routinely use burrows and originated from wild individuals caught in Pakistan, most of hoard food (Tanimoto, 1943; Kumari and Khan, 1979; Ågren et which is located in mid-latitudes of the northern hemisphere. al., 1989; Goyal and Ghosh, 1993; Waiblinger and König, Thus it was expected that the both species might exhibit SDT. 2004). Burrowing and food hoarding behavior are both likely However we were unable to find convincing evidence for daily to attenuate the impact of thermal stress and seasonal food torpor under SP conditions in well-fed gerbils, except for one shortage. Furthermore, T. indica and another species, the incidence of torpor in a female of M. unguiculatus during the Indian desert gerbil Meriones hurrianae (Jerdon, 1867), are recovery period (Fig. 1A). Cold exposure did not result in known to vary the depths of their burrows seasonally, most daily torpor in any SP M. unguiculatus although a low likely as a strategy to escape high temperatures in summer temperature facilitator for SDT expression has been reported in (Goyal and Ghosh, 1993). M. unguiculatus is colonial and the Korean field mouse, A. peninsulae (Masaki et al., 2005). typically lives in family units (Shilova and Orlenev, 2004). Nevertheless, the possibility of SDT in these gerbils should not Individuals huddle in the and hoard food, presumably be excluded, because threshold Ta levels for inducing SDT in order to optimize energy budgets. Thus despite the torpor differ between species and the single episode of torpor capability demonstrated in this study, it seems clear that both obtained for one female of M. unguiculatus on the third day of species are also able to endure environmental difficulties the recovery period with abundant food lends support to the without torpor. theory that SDT is possible (Fig. 1A). Further investigation is Further studies are needed to confirm the relationships needed in order to determine whether or not SDT occurs in between the environmental factors and torpor expression, and both study species. reveal the full torpor use profile of the Gerbillinae in detail. We successfully demonstrated that both M. unguiculatus and T. indica are capable of FIT, though the incidence under the Acknowledgements conditions of this study was low (Table 1 and 2), and it appears that FIT occurs infrequently in these species. The low We wish to express our cordial thanks to Dr Kimiyuki incidence of daily torpor in M. unguiculatus in this study may Tsuchiya for providing animals. be partly explained by our use of laboratory-bred animals descended from 11 pairs collected in China in 1954 References (Schwentker, 1963). However, torpor capability is well retained in highly inbred laboratory mice, Mus musculus (Dikic Ågren G., Q. Zhou and W. Zhong (1989) Territoriality, et al., 2008) with a long history of domestication, and our cooperation and resource priority: hoarding in the experimental specimens of T. indica showed a similarly low Mongolian gerbil, Meriones unguiculatus. Anim. Behav. incidence of torpor to M. unguiculatus despite a much shorter 37: 28-32.

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２種のスナネズミ（Meriones unguiculatus と Tatera indica）の休眠能力

渡部大介 1),2)*・畑瀬美穂子 3)*・坂本信介 3)・篠原明男 4)・越本知大 4)・森田哲夫 3)

1) 宮崎大学大学院農学工学総合研究科

2) 宮崎市フェニックス自然動物園

3) 宮崎大学農学部

4) 宮崎大学フロンティア科学実験総合センター生物資源分野

スナネズミ類が休眠能力を有するかどうかを確定するために，スナネズミ M. unguiculatus とインドオオアレチネ

ズミ T. indica の２種で光周期，食物欠乏および低温が休眠発現に及ぼす影響を調べた．T. indica では食物欠乏が短

日と長日の両条件下で日内休眠を引き起こしたが，M. unguiculatus では食物欠乏・短日条件下でのみ数個体が休眠し

た．これは，休眠発生率は低いものの両種が絶食誘導性休眠の能力を有することを示している．さらに，M. unguiculatus

の知見は長期短日曝露が本種で絶食誘導性休眠を発現させる上での必須前提条件であることを示唆する．一方，長期

短日曝露された M. unguiculatus の雌１個体で，不断給餌下において１回のみの日内休眠が認められた．しかし，これ

は本種が自発日内休眠すると結論づける証拠としては不充分であった．

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