Polar Biol (2005) 28: 769–775 DOI 10.1007/s00300-005-0004-6

ORIGINAL PAPER

A. R. Carlini Æ G. A. Daneri Æ M. E. I. Ma´rquez H. Bornemann Æ H. Panarello Æ R Casaux S. Ramdohr Æ J. Plo¨tz Food consumption estimates of southern elephant seal females during their post-breeding aquatic phase at King George Island

Received: 4 November 2004 / Revised: 5 April 2005 / Accepted: 8 April 2005 / Published online: 26 August 2005 Springer-Verlag

Abstract Changes in mass and body composition, mea- fish and squid consumed by the breeding group, sured with labelled water, were used to quantify the assuming a diet composed of 75% cephalopods and energy expenditure during lactation and energy replen- 25% fish, was estimated to be 521 and 174 metric ton- ishment during the post-breeding aquatic phase in nes, respectively, for the period examined. Southern elephant seal females at Stranger Point, King George Island. During lactation females spent a mean of 6,021±1,365 MJ, which resulted in a loss of 35% of the initial mass, comprising 63% of initial body fat and 20% of initial body protein. During the 58±5.4 day post- breeding foraging period, females gained 135±39 Kg, Introduction which allowed them to recover an average of 55% of the mass, including 46% of the fat, 71% of the protein and Southern elephant seals (Mirounga leonina) have a cir- 47% of the energy lost during lactation. Neither the cumpolar distribution, breeding mainly on subantarctic mass nor the energy lost during lactation were related to islands (Laws 1994). They are major predators of pelagic those replenished while at sea. However, protein loss squid and fish in the Southern Ocean marine ecosystem expressed in absolute terms or as a proportion of that (Laws 1977). The annual cycle of adult southern ele- present at the beginning of lactation explained about phant seal females has two distinct periods on land: one 50% of the variation in the protein gained during the for breeding and one for moulting. Breeding takes place post-breeding phase. This might indicate the presence of on subantarctic islands between September and a mechanism favouring an increase in lean tissue during November. After giving birth, females nurse their pups post-breeding. Daily energy requirements for an average daily for about 3 weeks while fasting, losing up to 40% sized female, during the post-breeding aquatic phase percent of mass and 50% of body energy reserves (Fe- were estimated at 96 MJ. Estimation of prey consump- dak et al. 1996; Carlini et al. 2004). After weaning their tion varies according to assumptions about diet com- pups, they return to sea to feed during an intermediate position. On a basis of 450 females, the total biomass of offshore period: the post-breeding phase. Diving studies suggest that this aquatic phase is a period of intensive feeding (Boyd and Arnbom 1991; Hindell et al. 1991; A. R. Carlini (&) Æ M. E. I. Ma´rquez Æ R Casaux Slip et al. 1994) when females gain mass at rates of 1 to 1 Depto. de Ciencias Biolo´gicas, Instituto Anta´rtico Argentino, 2.5 kg day (Boyd et al. 1993; Carlini et al. 1997). The Cerrito 1248, C1010 AAZ Buenos Aires, Argentina recovery of body mass during this time could be crucial, E-mail: [email protected] because after this period females come ashore for mo- G. A. Daneri ulting, a process which requires protein for growing the Divisio´n Mastozoologı´a, Museo Argentino de Cs. Naturales new integument and fat for metabolic demands. ‘‘B. Rivadavia’’, Av. Angel Gallardo 470, C1405 DJR Knowledge of food and energy requirements is Buenos Aires, Argentina important for assessing the impact of southern ele- H. Bornemann Æ S. Ramdohr Æ J. Plo¨ tz phant seal populations on marine resources and also Alfred - Wegener- Institut fu¨ r Polar-und Meeresforschung, 27515 Bremerhaven, Germany to provide clues as to potential effects that changes in prey abundance could have on population size and H. Panarello distribution. In this study data, on the energy gain Instituto de Geocronologı´a y Geologı´a Isoto´pica (INGEIS), Pabello´n INGEIS, Ciudad Universitaria, 1428 Buenos Aires, during the post-breeding aquatic phase was used to Argentina estimate food consumption and foraging efficiency for 770 females that breed at Stranger Point, King George subsequently thawed before liquid nitrogen freezing, and Island. the water was separated from the serum by sublimation under vacuum. HDO concentration was measured at the INGEIS laboratories on hydrogen obtained by Zn Materials and methods reduction at 500C from a subsample (5 ll) of the water obtained, according to the technique described in Study area and sampling protocol (Coleman et al. 1982). Isotope ratios were determined with a gas-isotope-ratio mass spectrometer (Finningan The study was conducted at Stranger Point, King Delta-s, McKinney). George Island (6214¢S, 5840¢W) during the 1995/1996 austral spring and summer. During lactation, 18 females were immobilised on the parturition day using an Body composition intramuscular dose of ketamine hydrochloride (2.63– 5.34 mg/kg body weight). Mothers were weighed in a net Total body water (TBW) was calculated from the dilu- stretcher suspended from a load cell (Challenger AZM, tion of D2O measured in the blood sample after a 4-h 1,000±0.5 kg) attached to an aluminium tripod and a equilibration period according to the equations provided blood sample (20 ml) was taken to measure background by Schoeller et al. (1980). levels of deuterium oxide. Then a pre-weighed dose Measuring TBW by isotope dilution overestimates water mass, because some isotope atoms become incor- (0.043±0.013 g/kg) of deuterium oxide (D2O, 99.8% purity) was administered via intramuscular injection. porated into body tissues and thereby give an errone- After equilibration of the injected deuterium for 3–4 h ously high estimate of TBW (Pinson 1952; Nagy and (Costa 1987), females were recaptured and a second Costa 1980; Oftedal and Iverson 1987). Reilly and Fe- blood sample was taken. An average of 2.9±1.6 (range dak (1990) gave this overestimate as 2.8±0.9% with 0–8) days before females departed to sea for the post- D2O for gray seals, and estimates of TBW were therefore breeding foraging period, mothers were recaptured, corrected using their regression equation. Body composition was calculated from total mass weighed and a blood sample was taken to measure D2O levels. Final total body water was then obtained by and TBW to give total body fat, total body protein, and total body gross energy (TBGE), using equations pro- reinjection of D2O (0.042±0.009 g/kg) followed by blood sampling 4 h later. We estimated the additional vided by Reilly and Fedak (1990) derived from analyses mass loss by females from this sampling point to the end of whole-body chemical composition of gray seals. of lactation as in a previous work (Carlini et al. 1999), Calculation of TBGE assumed energy densities of while the composition of this mass loss was assumed to 39.5 kJ/g for fat and 23.5 kJ/g for protein (Reilly and be similar to that effectively measured between the two Fedak 1990). sampling points during lactation. Detailed information on body material loss during lactation for the complete Dietary composition and energy content set of data (n=18) is given in another paper (Carlini et al. 2004). Here, we include data on loss during lac- To calculate total biomass consumption, the different tation for females, which returned to Stranger Point for energy densities of each prey item consumed must be moulting (see below) to examine possible relationships considered. Following Boyd et al. (1994) cephalopod between lactation costs during breeding and energy species were divided into muscular squid, gelatinous gained while at sea. squid and cranchiid squid with an energy density of 4.0, From December 1995, daily checks were made to 2.0 and 1.7 MJ kg1, respectively. Thus, considering the search for marked females that returned to Stranger percentage by mass of each cephalopod species at King Point to moult. Of the 18 females sampled during George Island given in Table 1, an average energy breeding nine returned to Stranger Point to moult. The density of 3.93 MJ kg1 of cephalopods consumed was complete set of body composition data were available assumed. Regarding the fish species consumed, Daneri for eight of these females. and Carlini (2002) stated that myctophids and the not- On the day of arrival, moulting animals were immo- otheniid Pleuragramma antarcticum were the most bilised, weighed and the blood sampling protocol was important fish prey for females during their post- repeated as described for animals during the lactation breeding aquatic phase at Stranger Point. Energetic period. The deuterium dose injected at the beginning of 1 1 values of 7.0 MJ kg for myctophids and 4.84 MJ moulting was (0.036±0.005 g kg ). kg1 for P. antarcticum were assumed (Cherel and Ridoux 1992; VNIRO 2000). Blood sample analysis Estimation of energy requirements All blood samples were left to clot in sealed vials for 8 h, then centrifuged and the serum was drawn off by pipette Daily energy requirements (ER) during the foraging and stored in airtight vials at 14 C. The samples were period at sea were estimated as 771

Table 1 Biomass (%) of the total cephalopods present in the diet of female southern elephant seals at King George Island. Diet data for Stranger Point from Daneri et al. 2000

Species Percentage of total Type Energy density cephalopod mass in diet (MJ/kg)

Psychroteuthis glacialis 81.4 Muscular 4.0 Gonatus antarticus 3.4 Muscular 4.0 Moroteuthis knipovitchi 3.9 Muscular 4.0 Kandakovia longimana 3.0 Cranchiid 1.7 Alluroteuthis antarcticus 7.8 Muscular 4.0 Chiroteuthis veranyi 0.2 Gelatinous 2.0 Brachioteuthis · picta 0.3 Muscular 4.0

ERðMJ=dayÞ ¼ FMR þðEG=DÞ; assimilation efficiency of the digestible portion. We as- sume that 78.3% of squid and 90% of fish energy is where FMR is the estimated field metabolic rate while at actually available to the seals (Costa 1988 quoted in sea defined as the energy cost a wild animal pays during Costa and Williams 1999). Thus, for the estimations the course of a day including basal metabolism, ther- given in Table 3, the total prey intake (TPI) in kg day1 moregulation, and voluntary activity (Nagy 1994), EG is for the different potential diets by mass was calculated as the difference in total body energy reserves between the follows: end of lactation and the beginning of the moult and D is 1 the duration of the post-breeding aquatic phase in days. TPI ¼ ERðPcAcaC þ PmAmam þ PnAnanÞ ; We assumed that energy for reproduction is near zero 1 during this period at sea. where ER is the daily energy requirement (MJ day ), P Field metabolic rate of free ranging southern ele- is the proportion by mass for a given prey item in a given phant seals has not been measured but, for phocid seals, diet, A is the assimilation efficiency (expressed as a proportion) for a given prey item and a is the energetic it appears to be one to three times the basal metabolic 1 rate (BMR) predicted by Kleiber’s (1975) equation density (MJ kg ) of a given prey item. The subscripts (Costa 1991, 1993). Thus, (c, m and n) indicate cephalopods, myctophids and nototheniids. Finally, the contribution of each prey item 0:75 BMRðMJ=dayÞ ¼ 0:293 M ; (PI) to the TPI was calculated as PI=TPI·P where M is female body size in kilograms. In this study, (M) was taken as the arithmetic mean mass between the end of lactation and the beginning of moult, while FMR Statistical analyses was assumed to be equal to 1.5 times the basal metabolic rate, i.e. FMR= 1.5·BMR. Values are given as means ± SD except where otherwise indicated and results were considered to be significant at the P<0.05 level. All percentage data were arcsine- Prey consumption transformed before statistical testing. The Kolmogorov– Smirnov test was used to determine whether data were The total prey energy consumed must account for that normally distributed, and the Levene median test was portion of the prey, which is indigestible, and the actual employed to confirm homogeneity of variances.

Table 2 Energy and body materials used during lactation and gained during the post-breeding foraging trip for females sampling at King George Island

Lactation period Post-breeding foraging period

Initial mass Mass loss Fat loss Protein loss Energy loss Time spent Mass gained Fat gained Protein gained Energy gained (kg) (kg) (kg) (kg) (MJ) at sea (day) (kg) (kg) (kg) (MJ)

688.5 278.1 178.9 19.3 7,595 52 137.0 14.2 30.6 1,290 730.0 222.5 139.7 16.4 5,961 51 114.5 97.5 1.1 3,916 600.0 210.1 132.1 15.4 5,635 54 174.0 109.1 12.9 4,657 717.0 277.5 111.5 38.5 5,357 60 204.0 36.1 41.4 2,419 688.5 259.8 160.2 20.0 6,866 65 108.5 72.2 6.8 3,041 529.0 180.5 66.1 26.9 3,272 65 94.0 13.4 20.0 1,008 847.5 264.6 173.1 17.5 7,319 59 97.0 61.9 6.9 2,634 795.5 273.0 136.6 30.1 6,161 60 153.5 69.8 18.9 3,235 Mean 699.5 245.8 137.3 23.0 6,021 58.2 135.3 59.3 17.3 2,775.1 SD 101.5 36.7 36.5 8.1 1,365 5.4 39.4 35.7 13.5 1,230.4 772

Fig. 1 Total protein gained during the post-breeding aquatic phase as a function of protein lost during lactation

absolute terms and as a proportion of that present at the Results beginning of lactation, tended to gain more protein 2 while at sea (F(1,6)=7.8, P<0.05, r =0.57; F(1,6)=7.6, Mass and energy loss over lactation and gain while at P<0.05, r2=0.56, respectively) (Fig. 1). sea for individual females are shown in Table 2.On Estimation of prey intake during the post–breeding average, females spent 6,021 MJ during lactation. The phase varies according to the assumptions made in the energy expenditure resulted in losses of 63% of initial calculations (see Discussion). On a basis of 450 females body fat and 20% of initial body protein. During the present at the peak haul out during this season, the total post-breeding, foraging phase females spent biomass of fish and squid consumed by the breeding 58.2±5.4 days at sea. During this period they gained a group, assuming a diet constituted by 75% cephalopods mean of 135±39 Kg composed of 12% protein, 46% fat and 25% fish, was estimated at 521 tonnes and and 41% water. There was a wide variation in mass gain 174 tonnes, respectively, for the period examined. Ta- as well as in the compositions of that mass (Table 2). ble 3 shows estimation of food consumption while at sea Mass or energy gained expressed in absolute terms or as taking into account different potential diets. a percentage of that lost over lactation was not related to time spent at sea. During the post-breeding foraging phase females recovered, on average, 55% of the mass including 71% protein, 43% fat and 47% of the energy Discussion lost during lactation. Foraging success [measured as total mass gain (kg) or total energy gain (MJ) while at The post-breeding phase occurs in a period of seasonally sea] was not related to female mass or body energy re- abundant food supply and may be of overriding impor- serves at the end of the lactation period (P>0.05 both tance for females to compensate for the energy costs in- cases). Moreover, foraging success (as defined above) curred during the previous lactation period. During was not related to the mass or energy lost throughout lactation, losses of 40% of arrival mass and 50% of en- the lactation period (P>0.05 both cases). Although ergy reserves were observed at South Georgia (Fedak greater use of fat by females during lactation was not et al. 1996). For the eight females recaptured at the related to the fat gained while at sea, those females that beginning of moulting, the energy loss varied between spent more protein during the lactation period both in 3,272 MJ and 7,595 MJ (Table 2), which represented

Table 3 Estimation of biomass consumption of different food items under different assumptions on diet compositions by mass and energy expenditure while at sea equal to 1.5 times BMR

Diet composition expressed as proportion Daily prey intake Estimated biomass consumed during the entire post- by a female breeding foraging phase, on a basis of 450 females (tonnes)

Cephalopods Myctophids P. antarcticum TPI(Kg/day) Cephalopods Myctophids P. antarcticum

0 0.5 0.5 18.1 0 237 237 0.25 0.5 0.25 19.3 126 252 126 0.33 0.33 0.33 21.3 184 184 184 0.5 0.25 0.25 22.9 301 150 150 0.75 0.125 0.125 26.5 521 87 87 1 0 0 31.4 822 0 0 773 between 42% and 66%, respectively, of the body energy value not significantly different from that reported by reserves at the beginning of lactation. Due to the wide Boyd et al. (1993) for females at South Georgia range of absolute and relative expenditure throughout 2,111±840 (t-test, P>0.05, one tailed). However, al- lactation, females with greater expenditures might be though females at King George spent significantly less expected to compensate during post-breeding for their time at sea between breeding and the moult (58.2±5.4 vs greater losses. One might then also expect a positive 72.0±2.7, respectively; t test P<0.001 one tailed), they relationship between the mass and/or energy lost and gained energy at significantly higher rates (48.6±23.6 vs that gained over the post-breeding foraging period. This, 28.9±12.9 MJ/day respectively; t test P<0.05 one however, was not the case at King George Island, where tailed). By tracking females from King George, Borne- females showed a wide variation in their foraging success mann et al. (2000) showed that most of them travelled (Table 2), which was not related to their expenditure southwest along the coast of the Antarctic Peninsula. during lactation or to their final mass or energy reserves They suggested that the use of this potential feeding area at the end of the breeding period. However, protein loss may result in an energetic advantage for females at King during lactation, both in absolute terms and as a pro- George compared with females that breed at South portion of that present at parturition, was related to Georgia because of the relatively shorter distances to the protein gain while at sea, which explained more than potential feeding grounds, which might in turn explain 50% of the variability observed (Fig. 1). This suggests the differences in the rates of energy gained. that there might be some mechanism to allow females to compensate during the post-breeding phase for the losses incurred as protein during lactation, delaying at least in Estimation of prey intake some degree, the building of fat reserves when their body protein reserves have been compromised to a high degree In food consumption estimates that there are naturally during lactation. The lack of a relationship between sources of error associated with the assumptions made. energy or mass gain in absolute terms or in relation to the Among these, diet composition and metabolic rate while losses incurred by females during lactation and time at sea could be of overriding importance. The cephalo- spent at sea suggests that the duration of the post- pod portion of the diet of females at King George after breeding phase is constrained by the haul-out for mo- their post-breeding aquatic phase was described by ulting. If females are unable to increase time at sea in Daneri et al. (2000), who gave an overall picture of the relation to their foraging success, a possible solution to relative importance of each species in terms of biomass, build up the necessary protein reserves for moulting while the fish portion of the diet was informed by Daneri could be to favour the increase in lean body during this and Carlini (2002). It is known that the diet of southern aquatic phase. The fact that mass gained while at sea elephant seals varies with locations (Green and Burton showed a positive relation (although no longer significant 1993). Since data on the diet of the Stranger Point at P<0.05) to protein gain (R=0.65, P=0.07) but not to population were used in the estimates of biomass con- fat gain (R=0.11, P=0.8) suggests that the above sug- sumption in our study, it is expected that biases associ- gested mechanism could take place. The recovery of body ated with the consideration of overall diets for the protein during the post-breeding aquatic phase could be species would be minimised. On the other hand, since crucial, because after this period, females return to land females feed far from their moulting sites, it is more for their annual moulting. This process requires protein difficult to quantify the relative importance of these two to grow the new integument and fat for their metabolic main components, i.e. cephalopods versus fish because demands. For female southern elephant seals at South of the differential rates of digestion and retention of the Georgia losses have been estimated as 24% of initial hard parts (beaks and otoliths) used for the identifica- protein and 27% of body fat reserves upon arrival for tion of prey species. While Laws (1977), from exami- moulting (Boyd et al. 1993). If losses during moulting nation of stomach contents of southern elephant seals, were similar at King George, this would imply a loss of estimated that their diet consisted of 75% cephalopods about 24 kg of body protein throughout the moulting and 25% fish by weight, a more recent publication, using period. It might therefore be necessary to build up body fatty acid signature analysis (Brown et al. 1999), con- protein reserves during post-breeding to allow the mo- sidered that fish is more important in the southern ele- ulting process. In the northern elephant seal, fed wean- phant seal diet than previously assumed. Even bearing in lings preferentially lay down protein after the post- mind the potential limitations of stomach lavage as a weaning fast, which allowed them to maintain weight method for determining diet, in the present work we and store protein even when energy intake was below assume that prey items found by means of this technique their metabolic demands (Condit and Ortiz 1987). (Daneri et al. 2000; Daneri and Carlini 2002) are broadly Additionally, the critical role of protein as a limiting fuel indicative of overall diet. However, we have little justi- during lactation was stated by Crocker et al. (2001)in fication for deciding in favour of a given proportion of female northern elephant seals and also observed in the fish and cephalopods by mass in the diet of the southern southern species (Carlini et al 2004). elephant seal. In an attempt to overcome this limitation, During the post-breeding aquatic phase, females at Table 3 was drawn up to give an indication of what King George gained an average of 2,775±1,230 MJ, a amounts of different types of prey would be consumed, 774 taking into account different proportions of squid and In the northern elephant seal, Le Boeuf et al. (1988) fish by mass in the diet of southern elephant seal fe- observed an average mass gain of 1.05 Kg day1 and males. estimated that females consume around 6.2% of their Regarding metabolic rate, we used, in our estimates, mass daily during the post-breeding aquatic phase. a metabolic rate while at sea of 1.5 times the predicted From our figures, considering a diet composed com- basal level. Although there are no measurements of pletely of cephalopods, daily prey consumption was metabolic rates in southern elephant seals while at sea, estimated to be around 31 Kg day1 (Table 3) or 6.8% Kooyman et al. (1973) reported, for Weddell seals diving of their mass per day. Considering that the average mass from a hole in the ice, measurements of 1.5–3 times the of cephalopods recovered from stomach samples at BMR. Moreover, for diving northern elephant seals, Stranger Point was 180 g (Daneri et al. 2000), an average metabolic rates as low as 0.7 times the BMR were esti- female would capture around 174 cephalopods per day mated for long dives, assuming that dives were aerobic or 3 per dive, assuming 2.5 dives per hour and 90% of (Le Boeuf et al. 1988), while estimations of around 1.5 the total time spent diving at sea (Slip et al 1994). If so, times the BMR (considering the daily maintenance en- working at 1.5 times BMR while diving, the ratio of ergy and daily cost of transport) were made for female energy acquired to energy expended for an average sized northern elephant seals during the post-breeding aquatic female at King George (average mean mass 521 kg) phase (Sakamoto et al. 1989). Additionally, in captive would be approximately 2.12 MJ/0.72 MJ, i.e., three juvenile northern elephant seals, Webb et al. (1998) times for each dive, which is similar to the ratio esti- measured a mean oxygen consumption of 3.32 ml mated for the northern congener (4.0) by Costa (1993). 1 1 O2kg min , which is similar to the BMR predicted by Foraging success could be then examined by prey catch Kleiber (1975) equation. For southern elephant seals instead of energy gained during the foraging period. Hindell and Lea (1998), on the assumption that almost Taking into account the different energy requirements all dives were aerobic, estimated a total consumption of for the different females sampled at Stranger Point but about 120,409 l O2 during the 80 day post-breeding assuming the same diet constituted by 100% cephalo- aquatic phase for a female whose initial mass was pods, the equation given in methods can be simplified to 396 kg. This results in a metabolic rate slightly higher TPI(Kg/day)=ER (MJ)/(3.93(MJ/kg)·0.783). From the fig- than the BMR for a similarly sized female. In the cal- ures employed in this work, the most successful female culation made in our study, an overestimation of met- during the post-breeding aquatic phase must acquire, on abolic rate while at sea would lead us to overestimate average, 2.4 times more prey per dive than the least food consumption, while the opposite would be true if successful female, showing an efficiency in energy we assumed a lower metabolic rate than the actual one. acquisition (defined here as ratio of energy acquired to If female southern elephant seals worked at three times energy expended per dive) twice as great. The differences the BMR while at sea, instead of the 1.5 times assumed could be related to individual diving strategies and/or in this work, we would be underestimating female con- foraging locations, a question which is not possible to sumption by a factor of 1.5 (34.3 kg day1 vs answer from our data. However, the data reinforce the 22.9 kg day1 calculated in our study from a diet of necessity to couple studies of diving behaviour and 50% fish and 50% cephalopods). On the other hand, if movements at sea with energy gain to allow a much females worked while at sea at the BMR we would be more comprehensive analysis of foraging behaviour. overestimating actual consumption by a factor of 1.2 Although many assumptions must be made to esti- (22.9 kg day1 vs 19.2 kg day1) (Table 3). In other mate prey consumption, many of these were confirmed words, if all other parameters were constant, for each in other works. We therefore think that ours could be a increase of 0.5 times the predicted BMR, daily food reliable overall estimation of food consumption for consumption (considering the above diet) would in- southern elephant seals at King George. The total bio- crease by 3.8 kg for an average sized female. As pointed mass consumption by the 450 breeding females at King out previously, although no direct measurements of George during the breeding peak haul-out (A. Carlini, metabolic rate were made in free-diving elephant seals, it unpublished data), considering a diet by mass of 50% seems that diving for this species must be mostly aerobic cephalopods, 25% myctophids and 25% P.antarcticum, (Hindell et al. 1992; Slip et al. 1994; Hindell and Lea was estimated to be approximately 300 tonnes of ceph- 1998). To make it possible, since the amount of oxygen alopods, 150 tonnes of myctophids and 150 tonnes of that a female can carry is finite, females would use a P.antarcticum during their post-breeding aquatic phase. number of mechanisms collectively known as the dive response (Elsner and Gooden 1983). These mechanisms Acknowledgements We want to thank S. Poljak, R. Conde, M. would allow them to depress their metabolism while Alcalde, R. Montiel and G. Moreira for field assistance and S. diving to a level below the values of the field metabolic Valencio and J.L.Nogueira for technical assistance. We thank rate predicted for their body size by Nagy’s (1994) Empresa Neuquina de Servicios de Ingenierı´a – Sociedad del Es- equation. For the above mentioned reasons, it is ex- tado (ENSI), who provided the D2O to perform this study, and Holliday-Scott, who provided some of the anaesthetics used in this pected that metabolic requirements while at sea would study. We also wish to thank two anonymous reviewers for their not be very different from the 1.5 times BMR used in our helpful comments on the manuscript. This work was funded by the study. Direccio´n Nacional del Anta´rtico and the Secretarı´a de Ciencia y 775

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