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Seasonal Energetics of the Hottentot Golden Mole at 1500 M Altitude

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Seasonal Energetics of the Hottentot Golden Mole at 1500 M Altitude 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).
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