Physiology & Behavior 84 (2005) 739–745
Seasonal energetics of the Hottentot golden mole at 1500 m altitude
M. Scantleburya,T, M.K. Oosthuizena, J.R. Speakmanb, C.R. Jacksona, N.C. Bennetta
aMammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa bAberdeen Centre for Energy Regulation and Obesity (ACERO), School of Biological Sciences, University of Aberdeen, Aberdeen AB24 2TZ, Scotland, UK, and Rowett Research Institute, Bucksburn, Aberdeen, AB21 9SB, Scotland, UK
Received 10 November 2004; received in revised form 15 February 2005; accepted 23 February 2005
Abstract
Winter is an energetically stressful period for small mammals as increasing demands for thermoregulation are often coupled with shortages of food supply. In sub-tropical savannah, Hottentot golden moles (Ambysomus hottentottus longiceps) forage throughout the year and for long periods of each day. This may enable them to acquire sufficient resources from an insectivorous prey base that is both widely dispersed and energetically costly to obtain. However, they also inhabit much cooler regions; how their energy budgets are managed in these areas is unknown. We measured the daily energy expenditure (DEE), resting metabolic rate (RMR) and water turnover (WTO) of free-living golden moles during both winter and summer at high altitude (1500 m). We used measurements of deuterium dilution to estimate body fat during these two periods. DEE, WTO and body mass did not differ significantly between seasons. However, RMR values were higher during the winter than the summer and, in the latter case were also lower than allometric predictions. Body fat was also higher during the winter. Calculations show that during the winter they may restrict activity to shorter, more intense periods. This, together with an increase in thermal insulation, might enable them to survive the cold. D 2005 Elsevier Inc. All rights reserved.
Keywords: Energetics; Doubly labelled water; Resting metabolic rate; Water turnover; Afrotheria; Amblysomus; Ecophysiology; Seasonality
1. Introduction conditions prevail, such as low ambient temperatures or a shortage of food [8]. Daily or more protracted periods of Living conditions for fossorial mammals (those that live torpor are often used in other groups, such as tropical and forage underground) are quite different from those that mouse lemurs (Microcebus sp.), especially during periods inhabit the surface. Relatively constant burrow temper- of low rainfall when food supply is depressed [9,10]. atures, hypoxic and hypercapnic gas concentrations and However, measurements of daily energy demands of this high humidity necessitate specialised physiological capa- strategy using doubly labelled water [11] indicate that the bilities. Fossorial mammals have evolved reduced meta- energy savings on a daily basis are quite small, while bolic and heart rates, low and labile body temperatures and savings in water turnover are significant [12]. Hence, the high thermal conductances [1–6] to deal with these torpor may actually serve as a mechanism to conserve water conditions. These characteristics are thought to minimise or avoid heat stress. overheating in burrow systems where opportunities for Golden moles (Chrysochloridae) belong to an ancient evaporative water loss and convective cooling may be African superordinal clade containing six orders of extant constrained [1,2,7]. It has also been suggested that they placental mammals, the Afrotheria [13]. All golden moles may use torpor as means to conserve energy when harsh occur in sub-Saharan Africa and are solitary [14]. Of the 21 species currently recognised, 14 appear in the 2004 IUCN Red List of Threatened Species [15]. Despite their vulner- T Corresponding author. ability, little is known about their biology since they are E-mail address: [email protected] (M. Scantlebury). elusive and difficult to catch. Anatomically, they are ideally
0031-9384/$ - see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2005.02.022 740 M. Scantlebury et al. / Physiology & Behavior 84 (2005) 739–745 equipped for a fossorial existence: they lack external eyes 2.2. Daily energy expenditure (DEE) and water turnover and ear pinnae, they have a streamlined body with a low (WTO) body carriage, and they have a conical nose shield and modified forefeet to excavate soil [14]. Burrow systems are We measured the daily energy expenditure (DEE) of 10 often extensive and may be up to 200 m in length; they have adult golden moles (5 in summer and 5 in winter; although been known to excavate over 20 m of superficial runs per we injected 17 animals, 8 in summer and 9 in winter, we day [16]. only recaptured 10) using the doubly labelled water (DLW) The Hottentot golden mole (Amblysomus hottentotus technique [11,21]. On day 1, the animals were weighed longiceps) (hereafter Amblysomus) occurs in the south- (F0.1 g Sartorius balance) and a 0.2 ml blood sample was eastern regions of South Africa, from sub-tropical coastal obtained from the cephalic vein in the foot to estimate the areas to mountainous regions inland (up to 3000 m) [17]. background isotope enrichments of 2H and 18O. Blood It has been demonstrated that, in contrast to the expected samples were taken after RMR had been determined (see low values of fossorial mammals, the basal metabolic rate below). Blood samples were immediately heat-sealed in 50 of laboratory-acclimated Amblysomus was not signifi- AL glass capillaries. Afterwards, a known mass of DLW cantly different from the general mammalian predictions [100 g 95% APE enriched 18O water (Rotem Industries Ltd, [16,18]. In the laboratory, they spend a large part of their Beer Sheva, Israel) and 50 g 99.9% APE enriched 2H water total daily time (70%) inactive; and some of this time is (Isotec Inc. Miamisburg OH, USA) mixed with 342 g 1 16 spent in torpor. Torpor can be readily induced when H2 O] was administered (IP, 0.3 g/100 g body weight). ambient temperatures fall below the thermoneutral zone Syringes were weighed before and after administration (22.7–33 8C) [8]. However, free-ranging Amblysomus in (F0.0001 g, Sartorius balance) to calculate the mass of coastal savannah are active for more than 40% of each DLW injected. Blood samples were taken after 1 h to day. We were interested in how the pattern of energy use estimate initial isotope enrichments [11] after which animals in golden moles might vary in a very different part of were returned to the field at the site of capture. Final blood their geographical range –the Drakensburg mountains– samples were taken when moles were recaptured on a day where nocturnal outside temperatures fall below freezing between days 2 and 5 post dose, after whole 24 h periods, to during the winter. As the region is one of summer estimate isotope elimination rates [22]. Animals were then rainfall, prey supply is also likely to be limited during the released back to the site of capture. Capillaries that dry winter months. We propose two alternative hypoth- contained the blood samples were then vacuum distilled eses that might help understand how energy use might [23] and water from the resulting distillate was used to 18 16 differ during the winter: First, that golden moles might produce CO2 and H2 [11,24]. The isotope ratios O: O follow an energy-minimisation strategy; in which case, and 2H:1H were then analysed using gas source isotope they are likely to be inactive for much of the time, have ratio mass spectrometry (Optima, Micromass IRMS and low daily energy expenditure (DEE) and resting metabolic Isochrom uG, Manchester, UK), prior to calculation of DEE rate (RMR) values, and make extensive use of torpor. [25]. Upon initial capture, we took animals back to the Second, that they might use an energy-maximisation laboratory where their RMR was immediately measured. strategy; therefore, they may forage for longer or more Sustained metabolic scope (SusMS=DEE/RMR, [26]) was intensively to meet the additional energy demands of determined for each animal. Water turnover (WTO) values thermoregulation and associated costs of digging in drier (ml/day) were calculated using the measured deuterium and harder soils [19]. In this latter case, we would expect elimination rates (kd) and deuterium dilution spaces (Nd) higher DEE and RMR values during the cold dry winter [21,27] using the equation: months. WTOðÞ¼ ml=day kdNd  F ð1Þ where F is the fractionation factor of the isotope (=0.941; 2. Materials and methods 15). We estimated body fat content using the equation: %fat ¼ ½Â1 À ðÞN =0:78  body mass 100 ð2Þ 2.1. Study site and animals d [28,29]. Fieldwork took place during summer (December– February) and winter (June–August) at 1500 m altitude 2.3. Resting metabolic rate (RMR) in the Drakensburg mountain range, 64 km west of Mooi Rivier, South Africa (25858V S; 21849V E). The study area RMR was determined as minimal oxygen consumption consisted of a 40 ha golf course surrounded by montane for 17 animals (8 in the summer and 9 in the winter), when grassland. Mole tunnels were located underneath and they were seen to be at rest, for approximately 20 min, adjacent to fresh molehills. Tunnels were exposed, and after an initial hour in which they were habituated to the modified Hickman traps [20] were set at the entrance to the respirometry chamber. Measurements were carried out exposed tunnels. during the period of minimal activity (approx. 0900– M. Scantlebury et al. / Physiology & Behavior 84 (2005) 739–745 741
1300) [8]. We used an open circuit respirometry system Table 1 [30,31]. A metabolic chamber (1610 cm3 volume) was Mass, energy expenditure, water turnover and percent body fat immersed in a temperature-controlled water bath (Labotec) Summer Winter and maintained at 26–27 8C (LAUDA, Kfnigshofen, n 89 Germany). This was the temperature at which minimal mass (g) 65.5 68.1 sd 12.3 11.1 resting VO2 was measured previously, within the thermo- RMR (mlO2/h) 73.5 114.8 neutral zone of 22.7–33 8C [16]. Dried air was pumped sd 22.7 18.7 into the chamber at a rate of 500 ml/min. Flow rate was RMR (mlO2/g h) 1.02 1.56 controlled by a mass-flow controller (F900, Applied sd 0.29 0.33 Electrochemistry, AEI Technologies Inc. USA) that was n 55 placed upstream of the metabolism chamber. Measure- DEE (kJ/day) 108.5 98.5 sd 24.2 35.0 ments of VO2 were taken using an oxygen analyser (S-2A DEE (kJ/g day) 1.46 1.70 Applied Electrochemistry, AEI Technologies, Inc. USA). sd 0.25 0.46 The analyser was calibrated to an upper value (20.95% O2) WTO (ml/day) 36.7 30.4 sd 10.1 10.4 prior to the measurement of each animal and to a lower a value (0% O in N gas, AFROX, South Africa) every 2 SusMS 3.73 2.17 2 2 sd 0.67 0.41 weeks. Results were corrected to standard temperature and % fat 4.9 13.8 pressure. RMR values were compared with allometrically sd 2.9 2.6 predicted values [18,32]. Mean and standard deviations (sd) of body mass (mass, g), resting
metabolic rate (RMR; mlO2/h and mlO2/g h), daily energy expenditure 2.4. Analysis (DEE; kJ/day and kJ/g day), water turnover (WTO; ml/day), sustained metabolic scope (SusMS) and percent body fat (% fat) of Hottentot golden We used analysis of covariance (ANCOVA) to examine moles (Amblysomus hottentotus longiceps) during both summer and winter. n denotes sample sizes. differences in DEE (kJ/day), DEE (kJ/g day), Nd (ml), WTO a RMR in kJ/day used to estimate SusMS was calculated using an
(ml/day), WTO (ml/100 g day), SusMS (no units) and % oxygen-equivalent of 20.51 kJ/l O2 [60]. body fat between moles from winter and summer [33]. Body mass was included as a covariate and season as a categorical factor. must have been different at the different TAs. Using previous information on the energy costs of torpor and rest at different ambient temperatures [16], we determined 3. Results the energy costs of activity for different amounts of torpor. If we assume that there are three activity states; F Body mass averaged 66.9 g ( 11.4 sd) throughout the torpor, rest and activity; then the time spent in these three year. There was no significant difference in body mass, DEE activities must sum to 24 h. Similarly, the product of the or WTO between seasons ( P =0.66, 0.66 and 0.68 times spent in these activities with their respective energy respectively); these averaged 65.5 g, 108.5 kJ/day and costs must sum to the DEE. Therefore we have two 36.7 ml/day in summer and 68.1 g, 98.5 kJ/day and 30.4 ml/ relationships: day in winter respectively (Table 1). In marked contrast, RMR values and percent body fat were higher during the tTORPOR þ tREST þ tACTIVITY ¼ 24 h ð3Þ winter ( F1,14 =16.97, P =0.001 for RMR and F1,7 =12.65, P =0.024 for % fat) and sustained metabolic scope was and higher during the summer ( P =0.036) (Table 1). Previous studies suggest that there is a negative ðÞþt  E ðÞt  E correlation between ambient temperature and the daily TORPOR TORPOR REST REST time spent in torpor —Amblysomus spend more time in þ ðÞ¼tACTIVITY  EACTIVITY DEE ð4Þ torpor at lower temperatures [16]. It is likely that under the cooler environmental conditions of our study, in which where tTORPOR, tREST and tACTIVITY; and ETORPOR, EREST ambient temperature (TA) ranged from À5to208C (M. and EACTIVITY are the times and the energy costs of Scantlebury et al. unpublished data), Amblysomus spent torpor, rest and activity, respectively. The relationship more time in torpor than proposed in those populations between EACTIVITY and tACTIVITY is shown in Fig. 1. This previously studied in subtropical coastal areas. In the shows that as tACTIVITY decreases or tTORPOR increases, current study, winter burrow temperatures were approx- EACTIVITY increases (assuming that ETORPOR and EREST imately 15 8C lower than in summer (10 and 26 8C, in are both less than EACTIVITY); i.e. animals must expend winter and summer respectively, CR Jackson, unpublished more energy on activity if their activity periods are data). However, because DEE values were not signifi- shorter. Similarly, as TA increases, EACTIVITY increases. cantly different between seasons, the costs of activity This is because ETORPOR and EREST both decrease with 742 M. Scantlebury et al. / Physiology & Behavior 84 (2005) 739–745
1000 subterranean mammals adjust their physiological capabil- ities accordingly to deal with seasonal differences in 800 microclimate. In the Natal mole-rat, Cryptomys hottentottus natalensis, a sympatric, herbivorous rodent that may share burrow systems with Amblysomus,RMRvalueswere 600
kJ/day significantly higher during the winter than during the summer [44]. 400 We found that the DEE of Amblysomus did not differ ACTIVITY
E between seasons, and that it was not significantly different
200 from predicted values for similarly sized insectivores (Table 2). This is in contrast to Namib desert golden moles Eremitalpa granti namibensis andCapegoldenmoles 0 Chrysochloris asiatica, which both have energy require- 0 6 12 18 24 ments that are lower than allometric predictions [45,46]. tACTIVITY (hrs) Low energy budgets of E. granti namibensis are thought to Fig. 1. Calculated energy expenditure whilst active (EACTIVITY, kJ/day) as a stem from their very low RMR values, associated with low function of time spent active (tACTIVITY) during a 24 h period for o body temperatures and metabolic depression, which enable Amblysomus. !, n, E, D and represent values of EACTIVITY at am- bient temperatures of 10, 15, 20, 25 and 30 8C respectively, with zero them to conserve energy in an arid environment with low torpor. Dotted lines without symbols show increasing values of EACTIVITY productivity [45]. Low energy budgets of C. asiatica are for increasing amounts of torpor (6, 12 and 18 h) at an ambient temperature also thought to be associated with metabolic depression, of 10 8C. tACTIVITY cannot reach 24 h when tTORPOR is greater than zero as which may be an adaptation to a subterranean lifestyle [46]. the assumption is tTORPOR +tREST +tACTIVITY=24 h. Low RMR values are thought to prevent overheating in closed burrow systems [1,47], or to compensate for the high increasing TA; hence EACTIVITY must increase to sum to energy demands of subterranean foraging [48,49]. Reasons the DEE. why Amblysomus do not appear to show similar levels of metabolic suppression remain unclear; they may have higher RMR values because they inhabit colder environments. 4. Discussion Other insectivorous species of similar size, such as tenrecs (Microgale), commonly have reduced metabolic rates [50]. Maintenance of body temperature in the cold is energeti- However, higher RMR values have been recorded in some cally expensive [7]. For small mammals that inhabit cold species [50–52]. This was suggested to be a consequence of and temperate regions, winter is the most stressful season as certain species inhabiting cooler, more mesic environments. they are faced with increasing energy demands for thermo- Bearing in mind that the energy costs of rest increase regulation as well as shortages of food supply [34,35]. with decreasing TA [16], we can presume that there must be Various behavioural, anatomical and physiological strat- some form of behavioural compensation (of tACTIVITY)as egies are implemented to deal with this period. For example, DEE values were not significantly different between seasons animals may huddle in communal nests to reduce heat loss (see Fig. 1). This is consistent with the notion of a [36], build thicker and warmer nests [37] or reduce dreallocation hypothesisT [53,54], that subterranean mam- aboveground activity. They may also insulate themselves mals manage their overall energy balance seasonally by by getting fatter [38] or increase pelage or fur thickness minimising energy expenditure [55]. We can use this model [39]. Endogenous heat production may also be increased by to calculate the energy budget for a typical 70 g animal of non-shivering thermogenesis (NST) [40]. An alternative average mass: Laboratory studies suggest that at 10 8C, solution is to allow body temperature to drop, which Amblysomus are torpid for 75% of the total time and are eliminates the energetic cost of keeping warm [7]. This active for the remaining 25%. However, at 26 8C, they are mechanism can be employed for short periods of, for only torpid for 5% and are active for 35% of the total time example, 3–4 h/day, or for longer periods of several months [16]. Therefore, at 10 8C in the winter, EACTIVITY would be [41]. 335 kJ/day. This compares with a calculated EACTIVITY of Subterranean mammals are a special case. They live in 208 kJ/day at 26 8C in the summer. Hence, the costs of conditions that are buffered from outside temperature activity are potentially 50% greater during the winter. It fluctuations [42,43]. Mean maximum and minimum burrow should be noted that behaviour in the field cannot always be temperatures of Amblysomus occurring in coastal Natal, accurately extrapolated from laboratory observations, and South Africa, were 27 and 23.9 8C, in summer and 18.4 and any assumptions should be interpreted with caution. In 18.1 8C, in winter, respectively [16]. This compares with subtropical regions, Amblysomus spend a greater proportion corresponding outside ambient temperatures of 33 and 17 of total time active during winter (40.5%), than summer 8C during the summer and 26 and 12 8C, during the winter, (31.5%). This is in contrast to laboratory observations, respectively (South African Weather Bureau). Nevertheless, where activity periods were shorter at colder ambient M. Scantlebury et al. / Physiology & Behavior 84 (2005) 739–745 743
Table 2 Comparisons of measured values of resting metabolic rate, daily energy expenditure, sustained metabolic scope and water turnover with values predicted by allometry Species Body RMR % expected DEE % expected SusMS % expected WTO ml % expected Source a b c d mass (g) (mlO2/g h) RMR (kJ/day) DEE SusMS H2O/g day WTO Eremitalpa granti 26.1 0.50 22*** 12.5 24*** 1.95 59 2.3 49*** 1 namibensis Chrysochloris 44.0 1.17 68*** 33.0e 45*** 1.30 39*** 6.6 92** 2 asiatica Amblysomus 69.8 1.37 103 – – – – – – 3 hottentottus Amblysomus 65.5 1.02 74* 108.5 115 3.28 110 36.7 368*** 4 hottentottus (summer) Amblysomus 68.1 1.56 105 98.5 102 2.17 73*** 30.4 295*** 4 hottentottus (winter) Body mass (g), resting metabolic rate (RMR), percent of expected resting metabolic rate (% expected RMR), daily energy expenditure (DEE), percent of expected DEE (% expected DEE), sustained metabolic scope (SusMS), percent of expected sustained metabolic scope (% expected SusMS), water turnover (WTO) and percent of expected water turnover (% expected WTO) of three southern African species of golden mole from (1) Seymour et al. [45], (2) Bennett and Spinks [46], (3) Kuyper [16], (4) This study. *, ** and *** indicate the results of t-tests at significance levels of P b0.05, P b0.01 and P b0.001, respectively, of the measured value from the predicted value. a Expected RMR from the equation: RMR=15.67WÀ0.582 for 26 species of insectivores [61]. b Expected DEE from the equation: DEE=6.98W0.622 for 14 species of insectivores [62]. c Expected SusMS for eutherian mammals from the equation: log y =0.680À0.113 log W [63]. d Expected WTO for non-desert eutherians in the field from the equation: log y =À0.487+0.818 log W [64]. e Calculated from energy intake of captive moles [59]. temperatures and the total duration of these activities was In conclusion, Amblysomus does not appear to follow less [16]. It was proposed that the extra time required for either an energy minimisation or maximisation strategy. activity in the wild was necessary to forage for food. Our Moles survive the winter by maintaining average DEE at golden moles also had significantly higher proportions of approximately the same value as the summer. We suggest body fat in winter than summer, but in all seasons were that this is may be due to a restriction of their daily activities relatively lean. The fact that animals were leaner during the to a shorter, more intense period of the day, coupled by an summer, when more food was available [56], suggests that increase in thermal insulation. One possibility is a shift in fat storage is not necessarily limited by food supply. More the times of activity, perhaps from a nocturnal to a diurnal fat may be stored during the winter to buffer the effects of mode. Future research should measure the daily rhythms of low ambient temperature, and perhaps allow for longer body temperature in free-living animals in order to gain periods of activity. Increased levels of fat have been insights into patterns of activity and bouts of torpor. associated with higher predation risks and energy costs of transport in birds [57,58]. Carrying excess fat might increase the costs of locomotion in Amblysomus, but it is unclear Acknowledgements whether this may affect predation risks or mortality. This study has also highlighted the high water turnover (WTO) in This research was funded by a NRF grant (GUN this species, which was 3.4–3.7 times higher than allometric 2053801) R.S.A. to NCB and a University of Pretoria predictions for free ranging eutherians (Table 2). This might PDRF to MS. These experiments in this study complied be due to the amount of water contained in their food, that with the current laws and regulations in RSA. primarily comprises oligochaetes. 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