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Buoyancy Does Not Affect Diving Metabolism During Shallow Dives in Steller Sea Lions Eumetopias Jubatus

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Buoyancy Does Not Affect Diving Metabolism During Shallow Dives in Steller Sea Lions Eumetopias Jubatus Vol. 3: 147–154, 2008 AQUATIC BIOLOGY Published online July 29, 2008 doi: 10.3354/ab00074 Aquat Biol OPENPEN ACCESSCCESS Buoyancy does not affect diving metabolism during shallow dives in Steller sea lions Eumetopias jubatus A. Fahlman1,*, G. D. Hastie1, 3, D. A. S. Rosen1, Y. Naito2, A. W. Trites1 1Marine Mammal Research Unit, Fisheries Centre, Room 247, AERL—Aquatic Ecosystems Research Laboratory, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada 2National Institute of Polar Research, 1-9-10 Kaga, Itabashi, Tokyo 173-8515, Japan 3Present address: Sea Mammal Research Unit, Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife KY16 8LB, UK ABSTRACT: Changes in buoyancy due to seasonal or abnormal changes in body composition are thought to significantly affect the energy budget of marine mammals through changes in diving costs. We assessed how changes in body composition might alter the foraging efficiency of Steller sea lions Eumetopias jubatus by artificially adjusting the buoyancy of trained individuals. PVC tubes were attached to harnesses worn by Steller sea lions that had been trained to feed at fixed depths (10 to 30 m) and to resurface inside a metabolic dome. Buoyancy was altered to simulate the naturally occurring differences in body composition reported in adult females (~12 to 26% subcutaneous fat). Diving characteristics (transit times and time at depth) and aerobic energy expenditure (gas exchange) were measured. We found that foraging cost decreased with the duration of the dive and increased with dive depth. However, changes in body composition did not affect the diving metabolic rate of Steller sea lions for dives between 10 and 30 m. We propose that Steller sea lions may adjust their diving lung volume to compensate for changes in buoyancy to avoid additional metabolic costs. KEY WORDS: Body composition · Diving physiology · Marine mammal · Diving lung volume Resale or republication not permitted without written consent of the publisher INTRODUCTION eral blood flow and by using thick subcutaneous fat to limit heat loss in water. Increasing total body fat (body Marine birds and mammals spend considerable time composition) reduces the thermal challenge posed by (>50%) underwater during foraging trips and must cold water and serves as a reserve for future energetic optimize the physiological effects of conflicting de- challenges. However, increased subcutaneous fat also mands. Most notably, they must maximize the time increases buoyancy, which may in turn affect the they spend at a prey patch to increase prey acquisition metabolic cost of ascending, descending and staying at while minimizing the time they spend on the surface to depth—thereby increasing the costs of foraging. Alter- exchange metabolic gases. natively, diving animals may increase their metabolic Diving birds and mammals have developed sophisti- rate using physiological (shivering) or behavioural pro- cated physiological processes to increase the depths cesses (increased activity) to compensate for increased they can attain and prolong the time they can spend heat loss in water (Kvadsheim et al. 2005, Bostrom underwater. For example, animals may conserve oxy- & Jones 2007). While logic suggests that increasing gen and thereby increase foraging times by reducing metabolism (O2 consumption rate) to cover thermoreg- or terminating certain physiological processes while ulatory needs will reduce aerobic DD (Rosen et al. diving to increase the aerobic dive duration (DD) 2007), no study has assessed this in foraging marine (digestion and thermoregulation; Zapol et al. 1979, mammals. In fasting king penguins (Fahlman et al. Crocker et al. 1997, Schmidt et al. 2006). Metabolic 2005), complex changes in metabolic and thermoregu- costs of diving may also be reduced by reducing periph- latory processes were observed, and it is possible that *Email: [email protected] © Inter-Research 2008 · www.int-res.com 148 Aquat Biol 3: 147–154, 2008 marine mammals exhibit similar plasticity in their levels). We focused on one aspect of body composition thermoregulatory ability. (buoyancy) and examined how it affects energy expen- The relationship between buoyancy, diving behav- diture (metabolism) during shallow dives. However, iour and energetics is complicated. An animal that is we wanted to measure only the effect of changes positively buoyant at the surface will have to swim in buoyancy in the absence of other physiological actively to depth, but will be aided by the buoyant lift changes that would have occurred if lipid composition during ascent. Variation in diving behaviour, suppos- were artificially altered (i.e. thermoregulation, meta- edly related to differences in body composition, has bolic depression, etc.). We therefore measured the been previously documented in wild pinnipeds (Webb metabolic rates of Steller sea lions that were trained to et al. 1998, Beck et al. 2000, Watanabe et al. 2006). In dive while carrying buoyancy tubes, and adjusted grey seals, for example, both descent and ascent rates buoyancy to assess the possible consequence for wild increased with increasing negative buoyancy, while animals that experience changes in body composition. DD and surface interval (SI) duration remained unchanged (Beck et al. 2000). However, in northern elephant seals, buoyancy was negatively correlated MATERIALS AND METHODS with descent rate, but did not affect the ascent rate (Webb et al. 1998). All experiments were conducted under permits from Whether or not altered buoyancy and its concurrent Animal Care Committees of the University of British effect on underwater swimming behaviour have ener- Columbia and the Vancouver Aquarium. getic consequences in otariids is not known. Sato et al. Sea lions. Experiments were conducted between (2002) showed that the inhaled air volume before a April 26 and June 21, 2006 with 3 female Steller sea dive correlated with the dive depth in penguins, pre- lions Eumetopias jubatus housed in a specially de- sumably a strategy to adjust buoyancy according to the signed floating pen located in a coastal inlet in British depth of the dive. As lung capacities of marine mam- Columbia, Canada. The sea lions freely chose to co- mals are generally larger than those of terrestrial operate with all data collection and were never re- mammals, Kooyman suggested that adjustment of strained or confined during any of the experimental lung volume provides a useful way to alter buoyancy trials. Two of the sea lions (F97HA and F97SI) were 9 yr (Kooyman 1973). Consequently, marine mammals old, and the third was 6 yr old (F00BO). Body mass of could adjust their diving lung volume to compensate each sea lion was measured on a daily basis and aver- for changes in buoyancy—a strategy that would be aged (±SD) 170.2 ± 1.8 kg for F97HA (n = 14), 211.6 ± particularly useful during shallow dives. Alternatively, 1.3 kg for F97SI (n = 16) and 135.7 ± 0.8 kg for F00BO the additional cost incurred by descending with addi- (n = 13). tional buoyancy may equal the energetic saving Body composition, buoyancy and buoyancy adjust- reaped during ascent, and vice versa. For this reason, it ment. Total body water (TBW) was estimated once is important to assess diving costs in animals with midway through the trial (mid-May) using the deu- simulated variation in buoyancy to understand how terium dilution method. TBW values were reduced by changes in body composition may affect foraging costs 4% to correct for overestimation by this method (Nagy and ultimately survival. & Costa 1980). Total body lipid mass (TBL, kg) was Body composition of female Steller sea lions Eume- determined from the predictive equation reported for topias jubatus varies seasonally (Pitcher et al. 2000). Antarctic fur seals (Arnould 1995). The proportions of They are known to have the highest percentage body TBL and TBW were used to estimate the buoyancy of fat (and hence buoyancy) in the spring, before the each animal from Eq. (2) in Webb et al. (1998). Buoy- summer pupping season, and are leanest in the fall. ancy was adjusted to simulate the maximal naturally However, sea lions may also experience unpredictable occurring differences in body composition, or the level changes in body composition induced by negative of lipid mass, reported in adult female Steller sea lions environmental changes that affect rates of energy (~26 to ~12% subcutaneous fat, age 6 to 9 yr; Fig. 3 expenditure (e.g. inclement weather, dispersed and in Pitcher et al. 2000, see Table 1). Buoyancy was difficult to find prey) or energy intake (e.g. reduced adjusted by attaching 2 matched PVC tubes (diameter: quality or quantity of prey). Changes in body composi- 7.5 cm, length: 30 cm) of various buoyancies to the har- tion will affect the foraging abilities of adult females, nesses routinely worn by the sea lions during open- and will also have implications for the growth and water sessions. For positive buoyancy (B+) trials, the survival of offspring (Iverson et al. 1993). tube was closed off at both ends and the internal air Changes in body composition affect a number of volume was adjusted to result in an overall buoyancy physiological and behavioural processes (scope of that represented the upper limit of subcutaneous fat thermoregulation, reduction in metabolic rate, activity (27%). Each tube gave a maximum B+ of 12.7 N. For Fahlman et al.: Metabolic cost of diving in Steller sea lions 149 Table 1. Eumetopias jubatus. Body mass (Mb), total body lipid (TBL), initial (B),
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