Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Fasting metabolism in Antarctic fur seal (Arctocephalus gazella) pups
Introduction
The growth and development of young mammal infants is dependent on the adequate delivery of milk and/or solid food. The regular supply of nutrients enables the continued deposition of lean tissue mass and skeletal growth while meeting maintenance metabolic costs, with any surplus nutrients being incorporated into body lipid stores (Martin, 1984, Oftedal, 1984, Blaxter, 1989). Where the rate of food supply to offspring is low or irregular, the rate of offspring development is reduced as a greater proportion of nutrition is diverted from deposition into growing tissues to maintenance metabolism (Spray and Widdowson, 1950, Derrickson, 1988).
Otariid seals (fur seals and sea lions) have a lactation pattern characterised by short (1–2 days) nursing periods ashore alternating with long (3–30 days) maternal foraging trips to sea (Gentry and Kooyman, 1986, Francis et al., 1998, Georges and Guinet, 2000a). For the majority of lactation, fur seal pups are entirely dependent on their mother for nutrition (Bonner, 1984). Consequently, while their mother is at sea foraging, pups must fast and lose mass which reduces their overall growth rates. Numerous studies have shown that, in years of low food availability, increases in maternal foraging trip durations lower pup growth rates and can lead to increased pup mortality from starvation (e.g. Gentry and Kooyman, 1986, Boness et al., 1991, Lunn et al., 1993). The magnitude of the fasting durations, however, is not the only determinant of overall pup growth rate, with a recent study showing that the degree in the variability of maternal foraging trip duration has a strong influence on pup growth and survival (Georges and Guinet, 2000a, Georges and Guinet, 2000b).
A wide range of vertebrate species undergo periods of prolonged food restriction or fasting throughout their life history (Mrosovsky and Sherry, 1980, Nelson, 1980, Dawson et al., 1983, Cherel et al., 1988, Oftedal, 1993). Numerous studies of adult mammals and birds that undertake extended fasts associated with annual migrations, hibernation, breeding cycles or moults have revealed that a common physiological response is a reduction in basal metabolic rate, the reliance on stored body lipid reserves for the majority of metabolic energy expenditure and the conservation of lean tissue through a reduction in protein catabolism and/or urea recycling (Nelson et al., 1975, Le Maho et al., 1981, Le Maho et al., 1988, Groscolas, 1986, Boyd and Duck, 1991, Cherel et al., 1992, Boyd et al., 1993, Atkinson et al., 1996).
While long-term fasts are a natural component of adult life in many mammal and bird species, extended fasting is less common in infants which, because of the nutritional and energetic demands of growth, are generally less able to survive periods of severe food restrictions (Spray and Widdowson, 1950, Adolph and Heggeness, 1971, Blaxter, 1989, Sikes, 1996). An exception to this is the king penguin (Aptenodytes patagonica) where chicks undergo a fast of 4–6 months during the subantarctic winter when their parents are unable to adequately provision them (Cherel and Le Maho, 1988). Similarly, grey seal (Halichoerus grypus), harp seal (Phoca groenlandica) and northern elephant seal (Mirounga angustirostrus) pups all undertake long post-weaning fasts (2–12 weeks) on land or ice before commencing active foraging (Bowen, 1991, Costa, 1991). Studies of these phocid seal (Phocidae) species and king penguins have shown that they employ the same strategies of energy conservation, protein sparing and lipid utilisation as observed in adults during extended fasts (Ortiz et al., 1978, Pernia et al., 1980, Cherel et al., 1987, Condit and Ortiz, 1987, Worthy and Lavigne, 1987, Le Ninan et al., 1988, Reilly, 1991, Adams and Costa, 1993, Nordøy et al., 1993). However, infants of these species generally experience just one extended period of fasting during their development. In contrast, with their intermittent pattern of lactation, otariid seal pups do so regularly (Costa, 1991). Few studies have investigated the fasting metabolism of otariid seals and little is known of their physiological adaptations for the frequent long fasts they experience (Boyd and Duck, 1991, Castellini et al., 1993, Donohue et al., 2000, Rea et al., 2000).
The Antarctic fur seal (Arctocephalus gazella) has a 4-month lactation period coinciding with the brief but productive polar summer (McCann and Doidge, 1987, Boyd, 1991). Pups have a short period in which to grow and develop before they wean and have to forage independently. Consequently, Antarctic fur seal pups have one of the fastest mass-specific growth rates of any otariid seal (Costa, 1991, Lunn et al., 1993). In years of normal food availability, Antarctic fur seal females make foraging trips of 4–5 days, such that pups spend up to 71% of the lactation period in repeated fasting episodes (Boyd et al., 1991, Lunn et al., 1993).
The aim of this study was to determine the physiological responses (in particular, changes in resting metabolic rate and metabolic fuel use) of Antarctic fur seal pups to fasting durations normally experienced throughout the period of maternal dependence.
Section snippets
Materials and methods
The study was conducted on Bird Island (54°00′ S, 38°02′ W), South Georgia, during January and February 1999. All pups were born during the December 1998 breeding season and, for the purposes of this study, the mean pupping date of 4 December for the season (British Antarctic Survey unpublished data) is taken as the birth date for the study animals. Twenty healthy pups (10 male, 10 female), aged between 52 and 73 days that had been suckling naturally were captured as their mother departed the
Mass loss, body composition and water flux
The body mass of pups decreased exponentially in both sexes during the fasting period (Fig. 1). The elevations of the curves were significantly different (t18=3.06, P<0.01) with male pups (12.8±0.4 kg) being heavier than females (11.1±0.4 kg) at the beginning of the fasting period. The difference in the coefficient of the exponent approached significance (P=0.069) with proportional daily mass loss being slightly greater in females (3.8±0.1%) than males (3.5±0.1%). Average absolute daily mass
Mass loss and metabolic rate
The mean percentage daily mass loss by pups reported in the present study (3.5–3.8%) is within the range of means previously reported for Antarctic fur seals during fasting at this colony (3.4–4.9%; Arnould et al., 1996a) but higher than in fasting captive Steller sea lion (Eumetopias jubatus) pups (2.5%; Rea et al., 2000). This difference may reflect the greater initial body mass (24–37 kg), and thus potentially lower mass-specific metabolic rates of the Steller sea lion pups (Rea et al., 2000
Acknowledgements
We are grateful to Angela Gibson (Howard Florey Institute) for kindly conducting the plasma metabolite assays.
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