Physiological implications of continuous, prolonged, and deep dives of the southern elephant seal (Mirounga leonina)

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1 Physiological implications of continuous, prolonged, and deep dives of the southern elephant seal (Mirounga leonina) MARK A. HINDELL~ Department of Zoology, University of Queensland, St. Lucia, Queensland 4067, Australia DAVID J. SLIP AND HARRY R. BURTON Antarctic Division, Channel Highway, Kingston, Tasmania 7050, Australia AND MICHAEL M. BRYDEN Department of Veterinary Anatomy, University of Sydney, New South Wales 2006, Australia Received January 3, 1991 Accepted August 7, 1991 HINDELL, M. A., SLIP, D. J., BURTON, H. R., and BRYDEN, M. M Physiological implications of continuous, prolonged, and deep dives of the southern elephant seal (Mirounga leonina). Can. J. Zool. 70: The diving behaviour of 14 adult southern elephant seals was investigated using time depth recorders. Each of the seals performed some dives that were longer than its theoretical aerobic dive limit. Forty-four percent of all dives made by postmoult females exceeded the calculated limit compared with 7% of those made by postbreeding females and less than 1 % of those made by adult males. The extended dives displayed characteristics that suggested that they were predominantly foraging dives, although some were apparently rest dives. Dives longer than the calculated aerobic limits often occurred in bouts; the longest consisted of 63 consecutive dives and lasted 2 days. Postmoult females performed longer bouts of extended dives than postbreeding females. Extended surface periods (longer than 30 min) were not related to the occurrence of extended dives or bouts of extended dives. The possible physiological mechanisms that permit such prolonged continuous dives are discussed. Southern elephant seals may increase the aerobic capacity of dives by lowering their metabolism to approximately 40% of the resting metabolic rate on long dives. There is substantial interseal variability in the methods used to cope with long dives. Some animals appear to use physiological strategies that allow them to prolong the time available to them at the bottom of a dive, while others use alternative strategies that may limit the time available at the bottom of their dives. HINDELL, M. A., SLIP, D. J., BURTON, H. R., et BRYDEN, M. M Physiological implications of continuous, prolonged, and deep dives of the southern elephant seal (Mirounga leonina). Can. J. Zool. 70 : Le comportement de plongce a CtC CtudiC par utilisation d'appareils enregistreurs du temps et de la profondeur chez 14 individus adultes de 1'Clkphant de mer du Sud. Tous les animaux ont fait des plongces plus longues que la limite de temps acrobique thkorique estimke pour cette espkce. Quarante-quatre pourcent de toutes les plongkes effectukes par les femelles aprks la mue ont dcpassc la limite calculke, alors que seulement 7% des femelles post-parturiantes et moins de 1 % des miles adultes ont dcpassc cette limite. Les plongkes prolongkes avaient certaines caractkristiques qui indiquaient qu'il s'agissait surtout de plongkes de recherche de nourriture, mais certaines de ces plonogkes Ctaient apparemment des plongces de repos. Les plongces de durce au-dela des limites akrobiques estimces Ctaient regroupces; les plongces les plus longues ont CtC 63 plongces consccutives rcparties sur 2 jours. Les femelles en pkriode de post-mue se sont adonnces a des pcriodes de plongces prolongces plus Ctendues que les femelles post-parturiantes. Les pcriodes prolongces de repos en surface (plus de 30 min) n'ctaient relikes ni a des plongces prolongces, ni a des Cpisodes de plongces prolongces. Les mccanismes physiologiques qui peuvent permettre de telles plongces prolongces continues sont examinks. 11 est possible que les ElCphants de mer du Sud soient capable d'augmenter leur capacitc akrobique de plongce en diminuant leur mctabolisme jusqu'a environ 40% du taux de mctabolisme de repos au cours de leurs plongces prolongces. Les animaux utilisent des mcthodes varices pour effectuer leurs plongces prolongces; certains semblent utiliser des stratkgies physiologiques qui leur permettent d'avoir plus de temps en eau profonde, d'autres utilisent des strategies alternatives qui peuvent limiter le temps dont ils disposent en eau profonde. [Traduit par la rcdaction] Introduction Recent studies on the diving behaviour of deep-diving phocids have changed traditional ideas about mammalian diving physiology (Le Boeuf et al. 1988; Le Boeuf et al. 1989; Kooyman 1989a). Elephant seals in particular are capable of extremely deep dives, over 1500 m in northern elephant seals, Mirounga angustirostris (De Long and Stewart 1989) and over 1200 m in southern elephant seals, Mirounga leonina (Hindell et al ). Dives lasting up to 2 h have been reported for southern elephant seals (Hindell et al ). Deep-diving mammals have to contend with the large hydrostatic pressures encountered during a deep dive. During dives 'Present address: Department of Zoology, University of Tasmania, P.O. Box 252C, Hobart, Tasmania 7001, Australia. in excess of 1000 m, elephant seals are subjected to pressures of over 100 atmospheres ( 1 atm = kpa). Even during dives to average depths of m (Le Boeuf et al. 1988), the seals are exposed to pressures of atm and experience pressure changes of 5-6 atmlmin during descent and ascent. The mechanisms that seals use to overcome many of these problems are still poorly understood, involving as they do such high pressures, rapid pressure changes, and compression of the body, along with consequent decreases in lung volume and rate of gas exchange and the accumulation of blood gases in the tissues (Kooyman 1988; discussed more fully in Kooyman 1988, and Gooden 1990). Another major problem facing deep-diving air-breathing animals is the limitation of oxygen stores. ~hese animals can carry only a finite amount of oxygen in their lungs, blood, and tissues when they dive. They must manage this oxygen store Printed In Canada 1 Imprime au Canada

2 HINDELL ET AL. TABLE 1. Summary of depth and duration of dives and surface time between dives for 14 southern elephant seals Maximum depth (m) Dive duration (min) Surface (min) Seal Season No. and sex f SD Max. f SD Max. f SD n PMM NOTE: n is the total number of dives recorded., postmoult female; PMM, postmoult male;, postbreeding female;, postbreeding male. optimally in order to maximise the time they can spend submerged without resorting to anaerobic glycolysis, with the associated accumulation of toxic lactic acid (Hochachka 1986). The aerobic dive limit is defined as the maximum breathhold possible without any increase in blood lactate during or after the dive. This limit is dependent on the available oxygen stores, the oxygen consumption rate, the degree of peripheral vasoconstriction, and the rate of lactic acid production and consumption (Kooyman 19894). The aerobic performance of seals has been studied in detail only in Weddell seals, Leptonychotes weddellii (Kooyman et al. 1980, 1983), and the aerobic dive limit has been calculated for that species. This paper reports on the diving behaviour of freely swimming adult southern elephant seals during their postmoult and postbreeding periods at sea. The duration and pattern of the dives are described and discussed in light of the calculated aerobic capacity of the seals in an attempt to understand how the seals utilise their limited oxygen stores. Methods The results discussed in this paper are derived from the same data set obtained from the time -depth -temperature recorders described in detail in Hindell et al. (1991a, 199 lb). A total of 39 time-depth recorders (Wildlife Computers, Woodinville, Washington, U. S. A.) were deployed on adult southern elephant seals during Thirteen were put on adult females and 6 on adult males at the end of their annual moult, with a further 10 deployed on adult females and adult males at the end of the breeding season. The subjects were all selected at random, and the females were of comparable mass (Table 2). The postmoult animals were at sea for 6-8 months, so the switch-on time of the recorders needed to be staggered to allow complete coverage of this time. Postbreeding seals were only at sea for 2-3 months, a short enough period to be covered by a single recorder. Only 14 of the recorders were subsequently recovered or contained intact data. The time-depth profile of each dive was examined, and the dive was subsequently classified as one of the six dive types outlined in Hindell et al. (1991b). These dive types were described on the basis of such parameters as the amount of time spent at the maximum depth of the dive, the rate of ascent and descent, and the general form of the dive profile. The dive types were "rest" dives, "travel" dives, "surface" dives, "general nonforaging" dives, "pelagic foraging" dives, and "benthic foraging" dives. Pelagic foraging and benthic foraging dives were those dives with a distinct period between the descent and ascent phases of the dive. The former appear to have occurred in the water column, and the latter on the ocean floor. These types of dives were the most common and together accounted for approximately 75 % of the seals' total time while at sea (Hindell et al. 1991b). Rest dives were characterised by a rapid rate of descent to about 200 m, a long period of a much more gradual rate of descent, and a final rapid return to the surface. It was postulated that the period of gradual descent represented time that the seal was resting or even sleeping in the water. Estimation of aerobic dive limit Theoretical aerobic dive limits were calculated for each seal. The total available oxygen store (To,) for southern elephant seals was taken to be L O,/kg (Kooyman 1989a, p. 61). This figure was derived by assuming a blood volume (relative to lean body weight) of 22 %, a haematocrit of 59.3 % (Bryden and Lim 1969), a blood oxygen capacity of L1100 g (Lane et al. 1972), and a myoglobin concentration of 5.1 g1100 g (Simpson et al. 1970). The oxygen consumption rate during a dive (the diving metabolic rate, DMR) has not been measured in elephant seals. However, in the absence of better information, the resting metabolic rate may be used to approximate the diving metabolic rate (Kooyman 1989~). Consequently, in this study we used an estimate of the resting metabolic rate ( x lean ma~so,'~ (L 0, Imin); Schmidt-Neilsen 1983) as a measure of diving metabolic rate. This equation has been demonstrated to hold as well for marine mammals as for terrestrial mammals (Lavigne et al. 1986; Huntley 1987). The theoretical aerobic dive limit (ADL) was then ADL = (lean mass x To,)/DMR (Kooyman 1989a, p. 122) Fat, and in particular blubber, has major thermoregulatory and energetic roles in southern elephant seals (Bryden 1968) and can contribute as much as 38% of the total mass of these animals, depending on the age and reproductive status of the animal (Bryden 1972). However, as fat plays no part in oxygen stores, the estimated lean mass of the seals was used in the calculation of the aerobic dive limit. Total body water estimates derived from tritium dilution experiments from 6 females at the end of lactation in 1987 indicated that cows that had recently weaned their pups and were about to return to sea consisted of approximately 25% fat (M. A. Hindell, unpublished data). This value was used to estimate the lean weight of all of the females. This may tend to underestimate the fat content of postmoult animals, as they have shorter fasts.and less energetic demands than lactating females (Ling and Bryden 198 1). The lean mass of the males was esti-

3 CAN. J. ZOOL. VOL. 70, 1992 TIME OF DAY FIG. 1. Two examples of extended dives that exceed the estimated aerobic dive limit. (A) The dive profile of female No (estimated ADL = 27.5 min), showing a 120-min dive and the next 9 h of dives. Note that after 5 h of relatively short, inactive dives the seal engaged in another bout of extended dives. (B) A bout of nine dives, all exceeding 40 min, by female No (estimated ADL = 29.5 min). TABLE 2. Calculation of the theoretical aerobic dive limit (ADL) for each seal, derived from the total available oxygen stores (To,) and estimated diving metabolic rate (DMR) (Kooyman 1989a, p. 122) Seal Total wt. Lean wt. To, DMR ADL No. Sex (kg) (kg) (L) (L 0,Imin) (min) NOTE: F, female; M, male. mated from a girthlfat volume relationship established using ultrasound data (D. Slip, unpublished data). The calculated values for the aerobic dive limit are only approximate because the lean mass of the seals would have changed slightly during the time at sea, many of the parameters used to estimate To, were derived from limited samples, and we only have an estimate of the diving metabolic rate. The values do, however, provide a useful framework for consideration of the aerobic capacity of the seals in this study. All of the statistical analyses were performed using the SAS statistical package (SAS Institute Inc. 1988). All percentage data were arcsine transformed before analysis. All means are reported + standard deviation. TABLE 3. Percentage of dives exceeding the calculated ADL limits, the mean duration (ksd, min) of those dives, and the proportion of extended dives that were foraging dives, for 14 individual southern elephant seals classified by sex and deployment Seal duration % No. Sex Deployment % >ADL (min) foraging 857 F 1419 F 1423 F 1432 F 1440 F 905 F 1918 F 1930 F 1938 F 1948 F 1453 M 1475 M 1963 M 1969 M F F M F M NOTE: PM1, postmoult, February -April; PM2, postmoult, April-June; PM3, postmoult, July-September; PB, postbreeding; F, female; M, male. Results Duration of dives The mean depth and duration of dives and time spent on the surface between dives for each seal are listed in Table 1. The mean depth varied from 259 to 589 m, but there was no pattern

4 HINDELL ET AL. TABLE 4. The total number of dives exceeding the theoretical ADL that occurred in bouts of two or more dives for each seal, with the mean (ksd) number of dives per bout, the maximum number of dives, the mean (fsd) bout duration (including surface time), and the maximum total bout duration Number of dives Duration of bout (min) Seal No. of dives No. Type in bouts Max. Max PMM F M NOTE:, postmoult female; PMM, postmoult male;, postbreeding female;, postbreeding male. Values within a column followed by the same letter are significantly different (p > 0.05). TABLE 5. Relationship between bouts of extended dives and extended surface intervals (ESI); data are the number of ESIs not preceded by bouts of extended dives and the length (ksd) of those ESIs, and the number of ESIs that were preceded by bouts of extended dives and the mean length (ksd) of those ESIs, with the mean number of dives in those bouts ESIs preceded by bout ESIs not preceded by bout length Bout length Seals No. length (min) No. (min) (min) k k f Males f Total f f f4.5 NOTE: The data are shown separately for males and postmoulting () and postbreeding females (). with respect to sex or time of year. The deepest recorded dive was 1256 m by female No A total of 44 out of dives (0.09%) exceeded 1000 m, or approximately 3 per seal. Of these 44 dives, 23 were pelagic foraging dives and 21 were general nonforaging dives. The mean duration of the dives made by females differed between the postmoult and postbreeding deployments, with postmoult females staying submerged for an average of 8 rnin longer than the postbreeding females (nested ANOVA, indi- vidual seals nested within deployment, F9,,, = 7.59, p = 0.02). The longest dive time recorded was 120 rnin by postmoult female No A total of 120 dives lasted for longer than 60 rnin (0.24% of all dives). Of these dives, 82 were pelagic foraging dives. Of the 38 nonforaging dives, 30 were rest dives and the remainder general nonforaging dives. The mean surface time ranged from 2.0 to 4.1 min, and again there was no marked pattern between the sexes or the time of year, although there was a tendency for males to spend more time on the surface. Some seals had occasional extended surface intervals of up to 14 h. Extended surface intervals were defined as periods of more than 10 min spent on the surface between dives. The dive profile of the 120-min dive by female No illustrates that this seal spent a very short period of time on the surface, even after protracted dives (Fig. 1A). After a 120-min dive descending to over 900 m, the seal spent 2.5 min on the surface before diving for a further 30 min to a depth of over 600 m. The subsequent 13 dives are shown, and at no time did the seal spend more than 3 rnin on the surface between dives. However, normal pelagic foraging dives did not start again until 6 h later. In the six dives immediately following the long dive, while they were not characteristic rest dives, she showed no evidence of foraging behaviour. All six dives were also longer than 30 min.

5 374 CAN. J. ZOOL. VOL. 70, 1992 Depth (m) FIG. 2. Relationship between duration and depth of foraging dives, showing the 95% confidence limits about the predicted mean value at 100 m depth intervals. Analysis of covariance was used to test for differences in slope between the seals: (A) for the five postmoult females (41,,m251 = , p < ); (B) for the five postbreeding females (F,,,l,,771 = , p = ); (C) for the four males (4,,58671 = , p = ). The insets show the slope of the curve for each individual, with the associated standard error (numerals on the x-axis identify the seals). Theoretical aerobic dive limits of southern elephant seals The mean estimated lean mass of the seals in this study ranged from 240 to 319 kg for the females and from 1283 to 2709 kg for the males (Table 2). The theoretical aerobic dive limits calculated from these masses ranged from 27.5 to 30.2 min for the females and from 42.0 to 51.4 min for the males. The mean calculated aerobic dive limit of the postbreeding females was 29.5 f 0.7, significantly longer than the mean of 28.3 f 0.9 for the postmoult females (t = 2.40, df = 8, p = 0.04). However, the difference between the groups was only 1.2 min and would have little effect on the practical aerobic capacity of the seals. The average aerobic dive limit for the males was min Depth (m) FIG. 3. Relationship between rate of descent and depth of foraging dives, showing the 95% confidence limits about the predicted mean value at 100 m depth intervals. For details of the analysis of covariance see Fig. 2. All of the seals in this study performed some dives that exceeded their calculated aerobic dive limit (Table 3). These dives will be referred to as extended dives for the remainder of this paper. The proportion of extended dives ranged from 0.1 % for male No to 72.0% for postmoult female No The pooled percentages of extended dives were 44.1 % for the postmoult cows, 7.3% for the postbreeding females, and 0.6% for the males. A one-way ANOVA indicated that there were significant differences in the proportion of dives that exceeded the calculated ADL among the three groups (F,2,111 = 12.69, p = 0.001). A Tukey honestly significant difference indicated that there were significant differences between. the postmoult females and both the postbreeding females and the males, but not between the postbreeding females and the males. Extended dives were

6 HINDELL ET AL ,...,..., , Depth (m) FIG. 4. Relationship between rate of ascent and depth of foraging dives, showing the 95% confidence limits about the predicted mean value at 100 m depth intervals. For details of the analysis of covariance see Fig. 2. predominantly foraging dives (either pelagic or benthic) (Table 3). Foraging dives constituted % of all extended dives. Bouts of extended dives Seals were also capable of performing series, or bouts, of extended dives with little surface time between each dive. For the purposes of this study a bout is defined as two or more sequential dives separated by surface intervals of less than 10 min. Figure 1B shows a series of eight dives by 1 seal that occurred over an 8.5-h period. Each of the dives was classified as a pelagic foraging dive and exhibited a considerable number of "wiggles" during the bottom time. This animal spent 7 h continuously diving, and presumably foraging, with a total of only 16 min on the surface (2 min between each dive). A total o{...,...,...,...,...~ Depth (m) FIG. 5. Relationship between the time spent at the bottom of a dive and depth of foraging dives, showing the 95 % confidence limits about the predicted mean value at 100 m depth intervals. For details of the analysis of covariance see Fig. 2. of 5246 (or 51 %) of all dives by postmoult females were part of bouts of extended dives (Table 4), many more than the total of 1181 (or 5 %) for the postbreeding females. Two of 4 males did not display bouts of extended dives at all. The other 2 males spent a total of 10 (<0.1%) of their dives in extended bouts. The maximum number of extended dives in a bout ranged from 0 for two of the males to 63 for postmoulting female No A nested two-way ANOVA, nesting individual seals within time of year, indicated that there was a difference between postmoult and postbreeding females in the number of extended dives in bouts (4,8] = 6.54, p = 0.03). There were also significant interseal differences within the two groups (48,7681, p = 0.001). Males were not included in the analysis because there were insufficient data, but their mean number of extended dives per bout was , somewhat lower than for the females. The maximum total duration (including submerged and sur-

7 CAN. J. ZOOL. VOL Depth (m) FIG. 6. Depth of each foraging dive plotted against the duration of that dive for two seals, No (A) and No (B). There were significant regressions in each case (p < 0.05). The equation calculated for each relationship is also shown. face time) of a bout of extended dives was 2865 min, or just surface intervals was the same for those intervals following under 2 days, for postmoulting female No Nested two- bouts as for those that did not follow bouts (t = 0.869, p = way ANOVA revealed a difference in the duration of bouts 0.386). between the postmoult and postbreeding females (Fl,pr = 5.78, p = 0.04). Again, there were significant interseal differences in the length of bouts within the two groups (48,7681 = 10.82, p = 0.001). The longest bout of continuous foraging dives greater than the calculated aerobic limit was 29 dives lasting 21 h. Extended surjace intervals and rest periods Extended surface intervals of 30 min or more did not appear to be directly associated with the end of a bout of extended dives. Only 6% of all surface intervals greater than 30 min were preceded by bouts of extended dives (Table 5). The mean number of dives per bout, on those occasions when they were followed by extended surface intervals, was only 6.5 f 4.5, which is less than the overall mean number of dives per bout, indicating that it was not the unusually long bouts that were followed by protracted periods on the surface. The mean duration of the extended surface interval was unaffected by the occurrence of bouts of extended dives. The mean length of the Relationships between dive depth and dive duration, rate of descent, rate of ascent, and bottom time The relationships between dive depth and dive duration, time spent at the bottom of the dive, rate of descent, and rate of ascent were investigated using analysis of covariance. The analysis concentrated on pelagic foraging dives. Benthic foraging dives were not used, as they were confined to a very limited range of depths. Other nonforaging dives were also excluded, as by definition they were dives in which the seal spent no time at the bottom of the dive (Hindell et al. 1991b). All seals showed a significant positive relationship between the depth and duration of their foraging dives, but the slopes of the lines differed between the individual seals (Fig. 2). The rate of descent of a dive was generally positively related to dive depth (Fig. 3), with the sole exception of male No Rate of ascent was positively correlated with depth for all 4 males, but negatively correlated for 1 postmoult and 1 postbreeding female (Fig. 4). The relationship between the time

8 HINDELL ET AL. 377 spent at the bottom of a dive and the depth of that dive varied considerably between the males. For 1 male the slope showed a negative relationship, but for the other 3 the slope was either not significantly different from zero (hence the depth of the dive had no effect on the time spent at the bottom), or showed a positive relationship (Fig. 5). Of the 5 postmoult females, only 1 showed a negative relationship whereas 4 of 5 postbreeding females showed a negative relationship. The limited degree of overlap between the error bars for the slopes of the individual seals indicates that there was considerable interseal variation in all of these relationships. Two of the 14 seals, both postmoult females, showed an apparent discontinuity in the scatterplot of dive depth and dive duration (Fig. 6). For a distinct group of deep dives the relationship between depth and duration was weaker than for the main group of shallower dives. This is similar to, but not as marked as, the pattern described by Le Boeuf et al. (1988) for all postbreeding northern elephant seal females in their study. The shift, or breakpoint, occurred at between 400 and 500 m for 1 animal and around 700 m for the other. Discussion The maximum dive depth of 1256 m recorded for a 342-kg female in this study is second only to the 1570 m recorded for by an adult male northern elephant seal, Mirounga angustirostris, weighing over 2000 kg (De Long and Stewart 1989). Whereas such deep dives are relatively uncommon, constituting less than 1 % of all dives, the mean depth of dives achieved by individual southern elephant seals, ranging from 270 to 590 m, is equalled only by northern elephant seals (Le Boeuf et al. 1986, 1988) and is much deeper than the dive depths achieved by any otariid species (Gentry and Kooyman 1986) or Weddell seals (Kooyman 1981). The maximum dive duration of 120 min recorded by the same 342-kg female is the longest dive by a marine mammal so far recorded, and is almost double the previous longest dive of 73 min by a Weddell seal (Kooyman 1981). The longest known dive of a northern elephant seal is 62 rnin (Le Boeuf et al. 1989). A total of 120 dives (or 0.24%) exceeded 60 rnin in this study. Perhaps the most notable features of southern elephant seal diving behaviour are that most females exceeded their calculated aerobic dive limits and,that some of them did so most of the time. It may be significant that the seals that most consistently did this were pregnant, postmoult females. Female southern elephant seals also had the ability to perform bouts of up to 63 consecutive dives, which lasted for up to 47 h and all exceeded the calculated aerobic dive limit. These bouts were made up of several dive types, including rest dives, but were primarily foraging dives. Both Weddell seals and northern elephant seals are known to perform series of extended dives. Weddell seals can have bouts of up to 11 h without a surface rest period (Kooyman et al. 1980), and northern elephant seals can go for 18 days without spending more than 10 rnin on the surface between dives (Le Boeuf et al. 1988), although it was not reported how many of these dives exceeded the theoretical aerobic capacity of the animals. One female southern elephant seal in this study went for 40 days with no surface period longer than 6 min (Hindell et al. 199 lb). Mechanisms for dealing with high lactate levels When an animal, or any of its component organs, depletes its entire oxygen store and relies on anaerobic metabolism, it produces toxic by-products, principally lactic acid, that must be metabolised as soon as possible. Lactic acid continues to build up as long as the animal or specific tissue is anaerobic and can only be reduced once the animal begins to use aerobic metabolism once more (Hochachka 1986). In only 2-5 % of their dives do Weddell seals exceed their aerobic limit (Kooyman et al. 1980, 1983). When this happens they usually require considerable recovery times to break down the toxic anaerobic metabolites (Kooyman 1989~). A 45-min dive can require up to 70 rnin resting on the surface. If elephant seals employed similar mechanisms to those commonly used by Weddell seals (Kooyman et al. 1980), they would require a period of inactivity, presumably on the surface, to reoxygenate the blood and tissues and remove the lactate. However, in this study very few of the extended dives or bouts of extended dives were followed by a period of more than 10 min on the surface, or by a rest dive. Dives of up to 83 rnin were still followed by foraging dives. In fact, the longest dive for most individual seals was immediately followed by an active dive. This suggests that most dives performed by southern elephant seals were not anaerobic. The longest dive recorded in this study was 120 min, and although immediately followed by a brief 2.5 min at the surface, it was then followed by a series of six relatively inactive dives, all of which were longer than the estimated aerobic dive limit. Based on measurements made in a small number of Weddell seals that continued to dive after a long anaerobic dive (Castellini et al. 1988), the 4 h of relatively inactive dives would have been long enough to clear the lactic acid produced during a 2-h dive (G. L. Kooyman, personal communication), provided that these dives were completely aerobic (although they did exceed the calculated aerobic dive limit). The obvious conclusion is that the dives immediately following the 120-min dive did not exceed the animal's true aerobic capacity, even though they did exceed the calculated aerobic dive limit. Kooyman (1989b) further suggested that northern elephant seals performing a series of anaerobic dives may be able to process some of the lactic acid built up during the aerobic phases of each dive (e.g., surface time). This would still involve a nett increase in lactate levels, but it would certainly reduce the total accumulation at the end of the bout and allow for longer bouts. The possible mechanisms for enhancing aerobic dive limits are discussed below. Mechanisms for reducing lactate accumulation during continuous, prolonged diving Periods of prolonged anaerobic metabolism may be rare in southern elephant seals. Le Boeuf et al. (1988) suggested that northern elephant seals rarely exceed their aerobic dive limit, even with dives as long as 50 min. For southern elephant seals to maintain a series of dives of rnin duration as aerobic dives, the animals would need to reduce their metabolic rate to 50% of their estimated resting metabolic rate during dives. Weddell seals may reduce their metabolic requirements by 75 % during the descent phase of a dive and by 55 % during the ascent phase (Qvist et al. 1986; Hochachka and Guppy 1987). An average elephant seal foraging dive is made up of approximately 33% bottom time and 66% travelling time (Hindell et al. 1991b). If the metabolic rate can be reduced to 25 % of the resting metabolic rate during descent and to 45% of the resting metabolic rate for the remainder of the dive, the overall dive requirements would be approximately 40% of the resting metabolic rate. This value is necessarily approximate, but suggests that many of the southern elephant seals' extended dives might not involve anaerobic metabolism. Only nine of the dives in this study would exceed an aerobic dive limit calcu-

9 378 CAN. J. ZOOL. VOL. 70, 1992 lated using 40% of the estimated resting metabolic rate. The mechanisms used by marine mammals to reduce their metabolic rate while diving are collectively known as the dive response (Scholander 1940; Elsner and Gooden 1983). This consists of apnoea, bradycardia, and a redistribution of blood flow to important organs such as the swimming muscles, the brain, and the heart. Although originally described for captive animals in forced-diving experiments (Scholander et al. 1942; Elsner 1965) and so not truly representative of free-diving animals (Kanwisher et al ), studies of free-diving Weddell seals have shown that the metabolic rate during dives is reduced through a combination of these mechanisms (Kooyman et al. 1973; Kooyman 1985; Zap01 et al. 1979). Southern elephant seals also show bradycardia as a response to anaesthetic-induced apnoea, reducing the heart rate by up to 30% (D. Slip, unpublished data). Any metabolic shortfall produced by these processes is made up by anaerobic glycolysis in those organs receiving reduced blood supply (Hochac hka 1986). Hochac hka and Guppy (1987) proposed that the kidney and liver may use metabolic-arrest mechanisms to reduce the buildup of toxic anaerobic metabolites. On the basis of blood-flow patterns measured during dives, Guppy et al. (1986) hypothesised that some seals have the capacity to controllably arrest, or at least suppress, metabolism in these hypoperfused tissues in anticipation of long dives. We do not know if elephant seals can alter metabolism at the tissue level in anticipation of long dives, but there is some evidence that they can at least anticipate the depth and therefore the duration of a dive. This is suggested by the observation that most elephant seals in this study increased their rate of descent on deeper dives (see Fig. 4). As the rate of descent is generally constant once a dive begins (see Fig. l), the seals must know how deep they expect to go and behave accordingly. Le Boeuf et al. (1988) used the two-stage relationship between dive depth and dive duration (see Fig. 6) in northern elephant seals as supporting evidence for the animals' ability to vary their metabolic rate in response to dive duration. They suggested that by decreasing the descent time in the deeper dives (through increasing swimming speed) the seals "shift gears" and increase their oxygen consumption rate. This would maximise bottom time but reduce the overall dive time because of the increased oxygen demands incurred by the seals with increasing swimming speed. However, the two-stage relationship was uncommon in southern elephant seals, occurring in only 2 of 14 seals, suggesting that the animals in this study were employing different strategies to maximise the time at the bottom of the dive. Half of the females and 1 of the males in this study showed a decrease in the time spent at the bottom of a dive with increasing depth. One of these animals (No. 1419) showed the two-stage relationship in depth -duration distribution, but actually exhibited shorter bottom times in the deeper dives. These seals may have been using close to their total oxygen reserves during the deeper dives, as they did not spend more time at depth despite expending considerable energy to get there. The increased rates of descent and ascent during deeper dives do not appear to be sufficient to offset the greater travel time required for deep dives and did not result in a "shift of gears" as in northern elephant seals. This implies that the slight changes in swimming speed did not have a major impact on oxygen stores. The remaining seals were able to either maintain a constant bottom time regardless of the depth of the dive, or actually increase the time spent at the bottom of a dive with increasing dive depth. However, unlike northern elephant seals, most of these animals did not show a shift in the dive duration-depth distribution, with the consequent decrease in dive duration for deeper dives. Either these animals were not as limited by their oxygen stores as the other females, or they were better able to deal with lactic acid accumulation. This is not surprising for the males, which have larger oxygen stores. It does suggest that these females may employ different strategies of oxygen conservation or lactate metabolism from those of the other females, but what these might be is unknown. The postmoult females in this study performed many more extended dives and more bouts of extended dives than the postbreeding females or any of the males. The ability to make long dives may partly depend on which of these strategies is employed. Most postmoult females spent more time at the bottom with increasing depth, which suggests that they were less limited by oxygen stores than most of the postbreeding females, which spent less time at the bottom with increasing depth. However, there were exceptions. Postbreeding female No showed a positive relationship between bottom time and depth, but only 4% of her total dives were extended dives. Conversely, postmoult female No showed a negative relationship between bottom time and depth of dive, but 68% of the dives exceeded the calculated aerobic dive limit. If certain organs such as the kidney and liver are switching off during extended dives, then they will need to switch on again at some stage to carry out their functions. Both southern and northern elephant seals perform series of long feeding dives that last for many hours. These dives would presumably involve the active pursuit, capture, and ingestion of prey. Not only the important organs such as the brain, heart, and swimming muscles, but also those involved in digestion and excretion would need to function during these bouts. These organs may turn on during the brief 3- to 4-min interdive surface interval, but this is unlikely to be long enough to process the entire backlog built up during a 30- to 50-min feeding dive. This may be a major role of both rest dives and extended surface intervals. Southern elephant seals spent an average of at least 70 min per day on either rest dives or extended surface intervals. Most of the seals performed a series of rest dives on most days (Hindell et al b), indicating that one period of switching on the kidneys and liver each day may be enough to compensate for any delay in organ function. This study has shown that southern elephant seals are capable of consistently performing dives far in excess of the theoretical aerobic limits calculated from parameters derived from other species. This may mean that the true aerobic capacity of elephant seals, particularly postmoult females, cannot be calculated in this way. Either the animals have evolved unique mechanisms for dealing with the accumulation of very high levels of lactic acid (such as metabolizing it on subsequent dives), or they reduce the accumulation of lactic acid by dramatically reducing their diving metabolic rate. There is now a pressing need for further physiological studies on this species. There are two possible approaches. One is to look at apnoea of seals during normal terrestrial sleeping behaviour, as in studies on northern elephant seals (Castellini 1988), or at induced apnoea resulting from anaesthesia (Gales 1989). Although elephant seals are not as convenient to use for controlled diving studies as Weddell seals, time -depth recorders modified to record such parameters as heart rate and body

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