Pattern and depth of dives in Northern elephant seals, Miruunga angustirustris
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1 J. Zool., Lond. (A) (1986) 208, 1-7 Pattern and depth of dives in Northern elephant seals, Miruunga angustirustris B. J. LE BOEUF, D. P. COSTA, A. C. HUNTLEY Department of Biology and Coastal Marine Studies, University of California, Santa Cruz, California USA G. L. KOOYMAN AND R. W. DAVIS Physiological Research Laboratory A-004, Scripps Institution of Oceanography, University of Calqornia, Sun Diego, La Jolla, California USA (Accepted 12 February 198.5) (With 1 figure in the text) A time-depth recorder was attached to a female Northern elephant scal at the end of her lactation fast before she entered the sea to feed. The animal dived continuously during its first 11 days at sea, the period recorded for a total of 653 dives. Mean dive time was 21 min, with the longest submersion lasting 32 min. Mean surfke interval between dives was 3 min, resulting in a total surface time of I1 %. Mean dive depth was 333 m and the deepest dive was 630 m, the deepest ever recorded for a pinniped. A depth histogram recorder attached to another female yielded a similar frequency distribution of dive depths. Contents Page Introduction... 1 Mcthods... 2 Results... 2 Discussion... 4 References... 5 Introduction Although the onshore behaviour of the Northern elephant seal, Mirounga angustirostris, has been studied extensively (e.g., Bartholomew, 1952; Le Boeuf, 1974; Reiter, Panken & Le Boeuf, 1981), little is known about the animal s behaviour at sea, where most of each individual s life is spent and where feeding takes place. Adult females and males spend 84% and 67% of the year at sea, respectively. The adult female annual pattern is as follows. Five weeks on land for parturition, nursing and copulation are followed by 2.5 months at sea feeding; 2-4 weeks on land moulting are followed by approximately 7.5 months at sea feeding and then a return to the rookery to give birth and complete the annual cycle (Le Boeuf & Peterson, 1969; Le Boeuf, Whiting & Gantt, 1972; Le Boeuf, 1981). There is little information on dispersal of elephant seals at sea after they leave the breeding colonies, and animals of both sexes and all ages are seldom seen by mariners (Bonnell, Le Boeuf, Pierson, Dettman & Farrens, 1978; Condit & Le Boeuf, 1984). We obtained acomplete dive record of an adult female for her first 11 days at sea after she gave birth and weaned her pup, and a frequency distribution of dive depths made by another post-parturient female during her first seven days at sea /86/ The Zoological Society of London
2 2 B. J. LE BOEUF ET AL. The period between weaning her pup and moulting is an ideal time to record a female s activity at sea. Because females fast throughout lactation and lose a third of their mass (Costa, Le Boeuf, Ortiz & Huntley, 1986), we reasoned that they begin feeding soon after departing the rookery. Methods On 16 February 1983, we immobilized 2 lactating females at Aiio Nuevo Point, California, using ketamine hydrochloride (Briggs, Henrickson & Le Boeuf, 1975). The drug was injected into the hind quarters with a COZ powered pistol (Cap-Chur Darts and Pistol, Palmer Chemical Co.). The females were measured, rolled into a nylon stretcher and weighed with a 1000 kg dynamometer (Chatillon WT kg) suspended from an aluminum tripod. A time-depth recorder (TDR) was attached to the ankle of one female and a depth histogram recorder (DHR) was attached to the ankle of the other (Kooyman, Gentry & Urquhart, 1976; Kooyman, Billups & Farwell, 1983). Both instruments were attached with padded straps, a technique successful with Weddell seals, Leptonychotes weddelli (Kooyman, 1966). The TDR weighs 500 g and is designed to record the absolute time and depth of all dives for about 14 days; the DHR weighs 95 g and records only the depth of dives in 4 pre-set intervals, which ranged from 6.8 to 667 m in this study. The instruments were calibrated prior to attaching them to the animals (Gentry & Kooyman, 1985). Both females gave birth on 28 January, nursed their pups daily, weaned them and returned to sea to feed by 19 February. They were expected to return to the same location to moult during the last week in April, approximately 9-10 weeks after departure, thus allowing retrieval of the recording instruments. This prediction was based on studies of marked females; during this period, mean duration at sea ( f 1 S.D.) for 18 females in 1981 was days, and for 33 females in 1982 it was 664 f8.5 days. The day after each female returned to the rookery, she was immobilized, weighed and the depth recorder retrieved. The TDR film record was developed, enlarged and digitized; a computer program calculated and summarized all dives into frequency distributions for depth, duration and time of day (Gentry & Kooyman, 1985). Results Both females returned to the site later than expected. The female bearing the DHR spent 93 days at sea during which she gained 57 kg. The female bearing the TDR spent 127 days at sea, gained 19 kg and was already moulting when she appeared on land. In comparison, a marked, uninstrumented female that went to sea at the same time gained 43 kg in 92 days. In 1982, the weight gain of three marked, uninstrumented females was 132 kg in 63 days, 25 kg in 66 days and 54 kg in 68 days. The ankles of both experimental females, to which the instruments were attached, were sore from the chafing of the straps. We emphasize the TDR record because it yielded more information. The TDR recorded all diving activity for the female s first 11 days at sea. Several aspects of the record are noteworthy. Most remarkable was the pattern and consistency of the record. From the time the seal went to sea, until the TDR ran out of recording film 11 days later, the seal dived repeatedly for a total of 653 dives. The female s diving pattern is summarized by the data in Table I. On average, the seal dived 61 times per day, each dive lasted about 20 min followed by min (mean & 1 S.D.) on the surface, resulting in a daily surface time of 1 1 %. Only 13 surface intervals exceeded four minutes. The maximum dive time of 32 minutes was more than a 50 % increase in duration over the mean daily dive time.
3 PATTERN AND DEPTH OF DIVES IN NORTHERN ELEPHANT SEALS 3 TABLE I Dive characteristics of the TDR female during her,first I I days at sea (see text). Means & one standarddeviation from the mean Ddy No. of dives Surface time (%I Maximum depth (4 Mean depth (m) Maximum dive time (min) Mean dive time (min) *I **I f I i % I f i I i i i f i k3.2 20% 1.6 Average Total ~ ~ * 15.5h ** 26h Neither day 1 nor 11 included in overall average 251 Dive depth (m) FIG. 1. Frequency distribution of dive depths of the female to which a time-depth recorder was attached. Total dives = 653. The mean depth of dives was 333 f42.7 m. The maximum dive depth recorded was 630 m. With the exception of the first 1 1 dives, when the animal swam near the bottom as she was departing the rookery, there were few shallow dives. A frequency analysis of dive depths (Fig. 1) shows that only 6 % of all dives were less than 200 m. From the first dive of 55 m, the dives got progressively deeper in increments of about 10 m, until dives 12, 13 and 14 when the depths reached 108 m, 234 m and 338 m, respectively. It was at this time that the seal probably reached the edge of the continental
4 4 B. J. LE BOEUF ET AL. shelf. The time lapse from the first dive until this sharp increase in depth at the 14th dive was 5 h. If the seal swam at about 2 m/sec directly offshore, it would have travelled 36 km. A bottom contour map of the Aiio Nuevo area shows that the continental slope is 10 km to 48 km offshore, depending on the direction taken. The DHR record provides similar data on the depth of dives. The record ran for the female s first seven days at sea during which the seal dived 510 times; 9.2 % of the dives were between 6.8 and 82 m, 31.2 % between 82 and 199 m, 45.3 % between 199 and 442 m, and 14.3 % between 442 and 667 m. Discussion Several conclusions and questions can be drawn about Northern elephant seal dive capacities and behaviour from these records. As predicted from various aspects of their physiology (Bartholomew, 1954; Harrison & Tomlinson, 1956; Bryden & Lim, 1969; Lythgoe & Dartnall, 1970; Lane, Morris & Sheedy, 1972), elephant seals dive deeply and spend much of their time at depth. The maximum dive depth of 630 m is the deepest dive recorded for any pinniped, surpassing the record of 600 m observed in Weddell seals recorded during more than 100 days of sea time (Kooyman, 1972, 1975, 1981). Maximum dive depths obtained with similar instruments from other pinnipeds are much lower: between 121 and 175 m for Hawaiian monk seals, Monachus schaunslandii, with most dives being between 10 and 40 m (Kooyman et al. 1983), 274 m for California sea lions, Zalophus californiunus (Feldkamp, De Long & Antonelis, 1983), 186 m for Galapagos sea lions, Z.C. wollebaeki (Kooyman & Trillmich, 1985) and 207 m or less for five species of fur seals, Callorhinus ursinus, Arctocephalus gazella, A. pusillus, A. australis and A. galapagoensis (Gentry & Kooyman, 1985). The only marine mammals for which observations suggest dives to greater depths than 630 m are Sperm whales, Physeter macrocephalus, and White whales, Delphinapterus leucas (Laurie, 1933; Heezen, 1957; Backus & Schevill, 1966; Ridgway, Bowers, Miller, Schultz, Jacobs & Dooley, 1984). The fact that elephant seals spend so little time near the surface has important implications for population estimation and assessment of distribution patterns. Surveys of animals at sea would have to incorporate considerable correction factors to be useful. To what extent the dive patterns of the two females in this study were affected by the instruments carried and the unusual sea and weather conditions in 1983 is uncertain. Was the relatively long stay at sea and the relatively low mass gain of females due in part to the added weight and chafing of the instruments which impeded prey catching? Did the females have to travel further to obtain prey because of the effects of an intense and widespread El Niiio event in progress throughout much of the eastern Pacific that caused a reduction in plankton, fish and squid (Cane, 1983; Rasmusson & Wallace, 1983; Barber & Chavez, 1983)? Fur seals and sea lions in the Galapagos Islands and off the coast of Peru were in poor condition and incurred heavy mortality rates, especially among new-born pups (Limberger, Trillmich, Kooyman & Majluf, 1983). In addition, fierce winter storms in 1983 caused high pup mortality at several elephant seal rookeries along the California coast, including Aiio Nuevo (Le Boeuf & Condit, 1983). It is significant that, despite potential handicaps, the subjects were capable of diving in the pattern described. Does the continuous diving for 11 days or more mean a non-stop feeding effort? Why are they diving as deeply during the day as at night when their deep diving prey (Condit & Le Boeuf, 1984) migrate closer to the surface? What are the sleep requirements of these animals? Do some of the dives represent sleep periods? While sleeping on land, elephant seals exhibit apnoeas of several
5 PATTERN AND DEPTH OF DIVES IN NORTHERN ELEPHANT SEALS 5 minutes duration during which bradycardia occurs and metabolism decreases (Bartholomew, 1954; Kenny, 1979; Huntley & Costa, 1983; Huntley, 1984). We recorded sleep apnoeas in lactating females at Aiio Nuevo Point lasting 21 min. Perhaps some of the dives represent the animal quietly drifting down at about 10 to 20 m/min while asleep, a behaviour observed in aquaria (Bartholomew, 1954). If so, why does the seal sleep at such great depths? Might it be that the safest place for a pelagic seal, whether diving or sleeping, is below predators like the White shark, Carcharodon carcharias? The eyes of both the mammal and the fish are on top of their heads. Potential prey on or near the surface stands out to a shark below because the prey is silhouetted against the light. Most shark attacks on elephant seals occur near the surface of the water (Ainley, Strong, Huber, Lewis & Morrell, 1981; Le Boeuf, Riedman & Keyes, 1982). If elephant seals try to maximize their time below the surface, then the percentage of surface time and the average dive duration correlate well with a hypothesis proposed for diving patterns of Wcddell seals (Kooyman et al., 1980; Kooyman, Castellini et al., 1983). In both animals, most dives do not exceed durations that require blood or tissue lactic acid to increase above normal levels. Consequently, the dive recovery is only for loading of oxygen stores and is brief. It is not necessary to process lactic acid, the end product of anaerobic glycolysis, which would require significantly more time. An adult Weddell seal and a young Northern elephant seal female are approximately the same size. A fat Weddell female is 450 kg and has a lean body mass of 315 kg since 30 of its mass is blubber (Lenfant, Elsner, Kooyman & Drabek, 1969). This is slightly higher than the lean body mass of 265 kg calculated for Northern elephant seal females at the end of lactation (Costa et al., 1986). We estimate that the 0, stores would be approximately the same in 1 he two species, resulting in an aerobic dive limit of about min. The narrow range around this limit exhibited by the elephant seal in this study (Table I) suggests that it is necessary for the animal to keep maximum dive durations between min to allow continued diving with such short surface intervals. 1 n summary, these diving records of Northern elephant seal females have broad and important implications for: (i) understanding underwater behaviour of this mammal, (ii) analyses of feeding strategies and their energetic costs, (iii) population assessment, and (iv) estimates of aerobic needs in diving marine mammals. Implications for analyses of prey distribution and energy requirements of predators, studies of predator avoidance by other large sea mammals, and assessment of sleep requirements of pinnipeds at sea are more indirect, but offer promising leads for future research. Supported by NSF Grants DEB , BNS , USPHS Grant HL17731 and NOAA Grant no. NA80AA-D We thank J. Reiter, L. Higgins, S. Davenport, J. Pernia, R. Condit and W. Clinton for field assistance, Lady Clairol Tnc. for animal marking solutions, and the Aiio Nuevo State Reserve rangers for their cooperation. REFERENCES Ainley, D. G., Strong, C. S., Huber, H. P., Lewis, T. J. & Morrell, S. (1981). Predation by sharks on pinnipeds at the Farallon Islands. Fish. Bull. U.S. natn. ocean. atmos. Admn 78: Backus, R. H. & Schevill, W. E. (1966). Physeter clicks. In Whales, dolphins andporpoises: Norris, K. S. (Ed.). Berkeley: University of California Press. Barber, R. T. & Chavez, F. P. (1983). Biologcdl consequences of El Niiio. Science, Wash Bartholomew, G. A. (1952). Reproductive and social behavior in the Northern Elephant Seal. Univ. Calif. Publs Zool. 47: Bartholomew, G. A. (1954). Body temperature and respiratory and heart rates in the northern elephant seal. J. Mammal
6 6 B. J. LE BOEUF ET AL. Bonnell, M. L., Le Boeuf, B. J., Pierson, M. O., Dettman, D. H. & Farrens, G. D. (1978). Pinnipeds of the Southern California Bight. 3-Investigator s Reports, Part I. In Marine mammal andseabirdsurveys of the Southern California Bight area, : Norris, K. S., Le Boeuf, B. J. & Hunt, G. L. (Eds). Springfield, Illinois: National Technical Information Service PB I. Briggs, G. D., Henrickson, R. V. & Le Boeuf, B. J. (1975). Ketamine immobilization of northern elephant seals. J. Am. vet. med. Ass. 167: Bryden, M. M. & Lim, G. H. K. (1969). Blood parameters of the Southern elephant seal (Mirounga leonina, Linn.) in relation to diving. Comp. Biochem. Physiol. 28: Cane, M. A. (1983). Oceanographic events during El Nifio. Science, Wash Condit, R. & Le Boeuf, B. J. (1984). Feeding habits and feeding areas of the northern elephant seal. J. Mammal Costa, D. P., Le Boeuf, B. J., Ortiz, C. L. & Huntley, A. C. (1986). The energetics of lactation in the northern elephant seal. J. Zool., Lond. (A)(In press). Feldkamp, S. D., DeLong, R. L. & Antonelis, G. A,, Jr. (1983). Diving behavior of California sea lions (Zalophus californianus). Biennial conference on the biology of marine mammals No. 5. Nov. 27-Dec. 1, 1983, Boston, Massachusetts. Gentry, R. L. & Kooyman, G. L. (1985).(Eds). Fur seals: maternalstrategies on landandat sea. Princeton: University Press. Harrison, R. J. & Tomlinson, J. D. W. (1956). Observations of the venous system in certain Pinnipedkd and Cetacea. Proc Soc. Lond. 126: Heezen, B. C. (1957). Whales entangled in deep-sea cables. Deep-sea Res Huntley, A. C. (1984). Relationships between metabolism, respiration, heart rate and arousal states in the northern elephant seal. Ph.D. Thesis, University of California, Santa Cruz. Huntley, A. C. & Costa, D. P. (1983). Cessation of ventilation during sleep: a unique mode of energy conservation in the northern elephant seal. Proc. int. Union Physiol. Sci. 15: 203. Kenny, R. (1979). Breathing and heart rates of the southern elephant seal, Mirounga leonina (L.). Pap. Proc. R. Soc. Tmm. 113: Kooyman, G. L. (1966). Maximum diving capacities of the Weddell seal, Leptonychotes weddelli. Science, Wash. 151: Kooyman, G. L. (1972). Deep diving behaviour and effects of pressure in reptiles, birds, and mammals. Symp. SOC. exp. Biol. No. 26: Cambridge: Cambridge University Press. Kooyman, G. L. (1975). A comparison between day and night diving in the Weddell seal. J. Mammal. 56: Kooyman, G. L. (1981). Weddell seal: consummate diver. Cambridge, London &New York: Cambridge University Press. Kooyman, G. L., Billups, J. 0. & Farwell, W. D. (1983). Two recently developed recorders for monitoringdiving activity of marine birds and mammals. In Experimental biology at sea: Macdonald, A. G. & Priede, I. G. (Eds). London: Academic Press. Kooyman, G. L., Castellini, M. A., Davis, R. W. & Maue, R. A. (1983). Aerobic diving limits ofimmature Weddell seals. J. comp. Physiol. 151: Kooyman, G. L., Gentry, R. L. & Urquhart, D. L. (1976). Northern fur seal diving behavior: a new approach to its study. Science, Wash. 193: Kooyman, G. L. & Trillmich, F. (1985). Diving behavior of Galapagos sea lions. In Fur seals: maternal behavior on landand at sea. Gentry, R. L. & Kooyman, G. L. (Eds). Princeton: University Press (In press). Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. W. & Sinnett, E. E. (1980). Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J. comp. Physiol. 138: Lane, P. A. B., Morris, R. J. H. & Sheedy, J. W. (1972). A haematological study of the southern elephant seal (Mirounga leonina, Linn.). Comp. Biochem. Physiol Laurie, A. H. (1933). Some aspects of respiration in Blue and Fin Whales. Discovery Rep. 7: Le Boeuf, B. J. (1974). Male-male competition and reproductive success in elephant seals. Am. Zool. 14: Le Boeuf, B. J. (1981). Elephant seals. In The natural history of,420 Nuevo: Le Boeuf, B. J. & Kaza, S. (Eds). Pacific Grove, Calif.: Boxwood Press. Le Boeuf, B. J. & Condit, R. (1983). The hgh cost of living on the beach. Pacif. Discovery 36: Le Boeuf, B. J. & Peterson, R. S. (1969). Social status and mating activity in Elephant seals. Science, Wash. 163: Le Boeuf, B. J., Riedman, M. & Keyes, R. S. (1982). White shark predation on pinnipeds in California coastal waters. Fish. Bull. Calif
7 PATTERN AND DEPTH OF DIVES IN NORTHERN ELEPHANT SEALS 7 Le Boeuf, B. J., Whiting, R. J. &Gantt, R. F. (1972). Perinatal behaviour of northern elephant seal females and their young. Behaviour 43: Lenfant, C., Elmer, R., Kooyman, G. L. & Drabek, C. M. (1969). Respiratory function of the blood of the adult and fetus Weddell seal, Leptonychotes weddelli. Am. J. Physiol Limberger, D., Trillmich, F., Kooyman, G. L. & Majluf, P. (1983). Reproductive failure of fur seals in Galapagos and Peru in Trop. Oceun-Atmos. Newsl. 21: Lythgoe, J. V. & Dartnall, H. J. A. (1970). A deep sea rhodopsin in a mammal. Nature, Lond. 227: Rasmusson, E. M. &Wallace, J. M. (1983). Meteorological aspects ofthe El Nifiolsouthern oscillation. Science, Wush ~ Reiter, J., Pdnken, K. J. & Le Boeuf, B. J. (1981). Female competition and reproductive success in northern elephant seals. Anirn. Behuv Ridgway, S. H., Bowers, C. A,, Miller, D., Schultz, M. L., Jacobs, C. A. & Dooley, C. A. (1984). Diving and blood oxygen in the White whale. Can. J
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