Eleven—
Diet of the Northern Elephant Seal

George A. Antonelis, Mark S. Lowry, Clifford H. Fiscus, Brent S. Stewart, and Robert L. DeLong

ABSTRACT. The diet of northern elephant seals, Mirounga angustirostris , at San Miguel Island, California, was examined by stomach lavage during the spring and summer from 1984 through 1990. Identifiable hard parts of prey species were recovered from the stomachs of 193 of 195 seals sampled. Cephalopods occurred in all stomachs containing identifiable remains of prey. Most prey species (70%) identified inhabit epi-, meso-, or bathypelagic oceanic zones, and relatively few (30%) occur in neritic or benthic regions. The five most frequently occurring prey species were the cephalopods Octopoteuthis deletron (58.0%), Histioteuthis heteropsis (43.0%), Gonatopsis borealis (40.9%), Histioteuthis dofleini (39.4%) and the teleost Merluccius productus (38.9%). The diets of males and females were similar, with the exception of a significantly higher occurrence of cyclostomes in the stomachs of subadult males. Variability in the diet of elephant seals was probably influenced by annual changes in the availability and abundance of prey.

The population of northern elephant seals, Mirounga angustirostris , has increased greatly during the past eight decades and may now number about 127,000 rangewide (Bartholomew and Hubbs 1960; Cooper and Stewart 1983; Stewart et al., this volume). Elephant seal behavior during brief periods ashore has been well documented (e.g., Bartholomew 1952; Le Boeuf 1974; Reiter, Panken, and Le Boeuf 1981), but their foraging ecology has only recently come under study (Hacker 1986; Antonelis et al. 1987; Le Boeuf et al. 1988, 1989; DeLong and Stewart 1991; Sakamoto et al. 1989; DeLong, Stewart, and Hill 1992; Le Boeuf, this volume; Stewart and DeLong, this volume). Here we describe the diet of northern elephant seals based on the examination of prey remains recovered from stomach contents and discuss the ecological relationships between elephant seals and their prey.

Methods

We lavaged the stomachs of 11 adult male, 69 subadult male, and 115 female northern elephant seals when they hauled out on land to molt at San Miguel Island, California, in spring (late April/early May) and summer (July) from 1984 through 1990. Stomach lavage was accomplished by chemically immobilizing each seal with ketamine hydrochloride, intubating its stomach, and flushing out the remaining parts of prey with 3 to 5 liters of seawater (Antonelis et al. 1987; DeLong and Stewart 1991). Prolonged apnea associated with the use of ketamine hydrochloride and poor health condition resulted in the death of 6 of 195 elephant seals chemically immobilized. Portions of the dietary information from the 1984 field season were previously reported by G. A. Antonelis et al. (1987).

The percent occurrence of prey species found in the stomachs of elephant seals was used as an index of prey consumption. Those species occurring in over 30% of the stomachs were considered major prey items. Dietary information was determined by identifying remains of sagittal otoliths and bones (fish), mouthparts (cephalopods and cyclostomes), elasmobranch and cyclostome egg cases (Cox 1963), crustacean exoskeletons (Schmitt 1921), and tunicates (Thompson 1948).

We estimated age groups (< 1 yr., 1 yr., 2 yrs., 3 yrs., 4–7 yrs.) of Pacific whiting, Merluccius productus , eaten by seals in 1984–1986 on the basis of size relationships between otoliths from stomach contents and known-age whiting reference specimens (Antonelis et al. 1987) and then estimated fish size using relationships among age, weight, and length (Dark 1975). Digestive erosion did not compromise our ability to categorize otoliths into age groups because Pacific Whiting size differences are conspicuous during the first three years of rapid growth (Dark 1975; Antonelis et al. 1987).

We estimated body sizes (mantle length) of individuals of one cephalopod prey, Gonatopsis borealis , from measurements of lower rostral beak length (Clarke 1986). These beak measurements were obtained from samples collected from 1984 to 1986. Sufficient data on relationships between body size and beak measurements were not available for the other cephalopods identified in this study. The annual occurrence of single and multiple prey taxa found in the stomachs of elephant seals (1984–1986) was calculated as percentages of the total number of stomachs containing identifiable food remains.

The null hypotheses (1) male and female elephant seals consumed the same prey and (2) diet did not differ among years were tested with a logistic regression analysis model (Aitkin et al. 1989). We compared the deviance explained by the variables (sex and year) to the deviance of the model without entering the variables. Changes in deviance were approximated by a chi-square distribution with degrees of freedom equal to the change in the

degrees of freedom between the two models. Data from stomach lavages conducted from 1988 to 1990 were not tested statistically because of insufficient sample sizes.

Results

We identified 53 prey taxa from stomach contents of 193 elephant seals (tables 11.1 and 11.2). No identifiable remains of prey were recovered from the stomachs of two subadult males. Thirty-seven (70%) of those taxa inhabit one or more of the pelagic habitats (epi-, meso-, or bathypelagic), whereas 16 taxa (30%) are restricted to neritic or benthic zones.

Cephalopods were the most commonly identified prey of elephant seals (table 11.1), consisting of 28 species, 6 of which have not been previously reported as prey of northern elephant seals (Gonatus onyx, Japetella heathi, Architeuthis japonica, Megalocranchia sp., Octopus bimaculatus , and Ommastrephes bartrami ). We recovered cephalopod remains from all of the stomachs containing identifiable parts of prey species (11 adult males, 67 subadult males, and 115 adult females). Octopoteuthis deletron, Histioteuthis heteropsis, Gonatopsis borealis , and Histioteuthis dofleini were the most frequently occurring cephalopods found in the stomachs. We estimated mantle length of G. borealis eaten as 13.6–28.0 cm

Other prey groups were recovered from stomachs less often than cephalopods. Pacific whiting and pelagic red crabs, Pleuroncodes planipes , were the predominant fish and crustacean species (table 11.2). Two of the identified fish species, Sebastolobus alascanus and Icichythys lockingtoni , had not been previously reported as elephant seal prey.

Diets of male and female seals were not significantly different (c² > 3.84, df = 1, p > .05) with one exception; cyclostomes occurred more frequently in the stomachs of subadult males (c² = 3.84, df = 1, p < .05) than in adult females (fig. 11.1). Seals ate teleost fish more frequently (c² = 5.99, df = 2, p < .05) in 1985 (males = 42%, females = 54%) than they did in 1986 (males = 30%, females = 27%). Crustaceans were consumed more often (c² = 5.99, df = 2, p < .05) in 1984 (males = 80%, females = 76%) than in 1986 (males = 17%, females = 14%); cephalopods were eaten more frequently (c ² = 5.99, df = 2, p < .05) in 1985 (males = 95%, females = 97%) than in 1984 (males = 76%, females = 79%). The diversity of prey eaten varied among years, with the greatest number of taxa consumed in 1984 and the fewest in 1986 (fig. 11.2).

The age composition of Pacific whiting that were eaten by elephant seals varied among years (fig. 11.3), but most fish (79% of 252) were less than 4 years old. Overall, 2-year-old Pacific whiting were the most often eaten age group (33%), followed by 1-year-old (21%), 4- to 7-year-old (21%), 3-year-

Fig. 11.1
Percent occurrence of the six major prey categories lavaged from the stomachs of adult male,
subadult male, and adult female northern elephant seals (1984, 1985, 1986, and 1988–1990).

Fig. 11.2
Occurrence of single and multiple prey taxa lavaged from
the stomachs of northern elephant seals, 1984–1986.

Fig. 11.3
Estimated age of Pacific whiting otoliths lavaged from the
stomachs of northern elephant seals, 1984–1986.

old (15%), and first-year fish (10%). Pacific whiting that were less than 1 year old were rarely eaten in 1985 (1%) and in 1986 (7%) but were common prey (20%) in 1984 (fig. 11.3). The 1984 Pacific whiting cohort was also well represented in the diets of seals as 1-year-old fish in 1985 (27%) and as 2-year-old fish in 1986 (41%). The frequency of occurrence of 3-and 4-year-old Pacific whiting was greatest in 1986 and 1985, respectively (fig. 11.3).

The average length and weight estimates of individual 1-year-old, 2-year-old, and 3-year-old Pacific whiting were 15.4 cm and 0.038 kg, 28.0 cm and 0.163 kg, and 42.3 cm and 0.496 kg, respectively. The average size of individual 4- to 7-year-old Pacific whiting ranged from 44.6 cm (~ 0.570 kg) to 51.8 cm (~ 0.854 kg).

Discussion

Our lavage studies indicate that elephant seals feed primarily on epi- and mesopelagic cephalopods, although other prey types that inhabit pelagic habitats are occasionally eaten. Recent data on the spatial and temporal distribution of foraging adult northern elephant seals (Stewart and DeLong 1990; Le Boeuf, this volume; Stewart and DeLong, this volume) reinforce these interpretations of the importance of resources in meso- and epipelagic habitats to northern elephant seals. Benthic organisms in the neritic zone may be more important prey for adult elephant seals when they forage over the continental shelf during migrations to and from breeding or haul-out locations. The foraging locations of juvenile elephant seals are unknown, but studies are currently under way (Le Boeuf, this volume). Limited dietary information (Hacker 1986) indicates that juveniles may feed frequently in the neritic zone.

All five major prey species make some type of diel vertical migration. O. deletron has been described as a vertical spreader that is found at 200 to 400 m depths during the day but disperses both upward (usually in the upper 100 m at night) and downward at night; the maximum reported depth is 1,600 m (Jefferts 1983; Roper and Young 1975). H. heteropsis, H. dofleini , and G. borealis are all second-order vertical migrators that move toward the surface at night (usually no shallower than 200 m) from daytime depths of 300 to 400 m (H. heteropsis and H. dofleini ) to 400 to 700 m (G. borealis ; Jefferts 1983, Roper and Young 1975). Pacific whiting migrate between daytime depths of 150 to 200 m and surface waters at night (Ermakov 1974); maximum daytime depths may reach 1,000 m (Best 1963). These depth ranges and diel variations of prey distribution are consistent with data on diving patterns recorded for adult elephant seals (e.g., Le Boeuf et al. 1986, 1988, 1989; DeLong and Stewart 1991; Stewart and DeLong, this volume; Le Boeuf, this volume). These results are also consistent

with the hypothesis that adult female and adult male seals dive to and forage on vertically migrating prey in the offshore mesopelagic zone (Le Boeuf et al. 1988; DeLong and Stewart 1991). Additional studies of the diel movement patterns of these prey and their association with the deep scattering layer may provide valuable insight into the foraging behavior of the northern elephant seal.

The luminescent characteristics of cephalopods may be an important factor that facilitates their being visually detected and preyed on by elephant seals, especially under low-light conditions. Three of the four major cephalopod prey (O. deletron, H. heteropsis , and H. dofleini ) are highly luminescent relative to the other less frequently occurring cephalopod prey (Nesis 1982). Unlike most of the other prey, these three cephalopods occur in the darkness of the bathypelagic zone, where a high degree of luminescence might make them more vulnerable to predation by elephant seals.

Only two other prey occurred in over 30% of the stomachs of elephant seals: pelagic red crabs (P. planipes ) and Pacific whiting. Pelagic red crabs were transient prey, occurring in the diet of the seals only in 1984 (44%) and in 1985 (38%). Pelagic red crabs have rarely been recovered during lavage studies since this time. Their consumption was evidently linked to the movement of large numbers of these crabs into the offshore waters of California during the 1982–83 El Niño Southern Oscillation (Stewart, Yochem, and Schreiber 1984; Hacker 1986). The influx of this prey into the region and, perhaps, the change in availability of other prey (e.g., Bailey and Incze 1985; Fiedler, Methot, and Hewitt 1986; Trillmich and Ono 1991) likely contributed to the high frequency of occurrence of P. planipes in those years.

The variable patterns of occurrence of Pacific whiting in the diet of northern elephant seals illustrate the relationship between the abundance and availability of a prey resource and the frequency of its consumption (fig. 11.3). Juvenile Pacific whiting (<1–3 years of age) are most commonly found in the epi- and mesopelagic waters, near the central and southern California coasts (Bailey, Francis, and Stevens 1982). Biomass estimates of this resource vary annually and are greatly influenced by the strength of each year class (Dorn et al. 1990). The great strength of the 1984 whiting cohort (ibid.) was clearly reflected in the seals' diets. Relative to other cohorts, the 1984 cohort occurred most often in elephant seals' diets each year as first-year (1984), 1-year-old (1985), and 2-year-old fish (1986). Similar relationships have been demonstrated between the abundance and availability of prey resources and their consumption by California sea lions, Zalophus californianus (Bailey and Ainley 1982; Antonelis, Fiscus, and DeLong 1984; Lowry et al. 1990).

Most other noncephalopod prey were only occasionally eaten during the spring and summer months. The inclusion of these prey in the diet of the

northern elephant seal does indicate, however, that these seals are capable of foraging on other prey species. For example, when resource availability was altered by the 1982–1983 El Niño Southern Oscillation (Trillmich and Ono 1991), the effects continued through 1984 when elephant seals foraged on a greater variety of prey taxa. G. A. Antonelis and C. H. Fiscus (1980) suggested that such dietary diversification might be expected during times of resource depletion.

The only detectable difference between the diets of subadult males and adult females was the more frequent occurrence of cyclostomes in the diet of the former. E. S. Hacker (1986) reported that juvenile males and females ate cyclostomes as well as other neritic and nearshore benthic animals. Further studies are needed to determine whether or not consistent differences exist between adult and immature elephant seals.

Northern elephant seals and other pinnipeds in the California Current eat some of the same prey (Antonelis and Fiscus 1980). The degree to which their foraging habitats overlap is minimized by the relatively short time elephant seals remain in nearshore waters. Most adult males and females move far offshore of their rookeries to feed in the Gulf of Alaska and the central/eastern North Pacific, respectively (Stewart and DeLong 1990; Le Boeuf, this volume; Stewart and DeLong, this volume). The degree to which juveniles forage in nearshore waters is poorly understood.

The size of prey consumed by northern elephant seals is not well documented. Our limited results on the size of Pacific whiting and G. borealis indicate that elephant seals tend to forage on prey that range from about 13 to 52 cm. O. deletron, H. heteropsis , and H. dofleini also occur in this size range (Nesis 1982), but additional information is needed to accurately describe the size of these and other prey consumed by northern elephant seals.

Assessing the importance of prey species on the basis of trace remains obtained by lavaging the stomachs of elephant seals must always be made with caution. Some of these prey, such as euphausiids, may be eaten incidental to other prey or may be secondary prey items (prey of the primary prey species) as suggested by W. F. Perrin et al. (1973). Biases may result also from individual differences in the time between feeding and lavage. In studies such as ours, most of the prey species of northern elephant seals are probably consumed relatively close to San Miguel Island and do not adequately represent those prey eaten while on the foraging grounds in the Gulf of Alaska or the central/eastern North Pacific (Stewart and DeLong 1990; Le Boeuf, this volume; Stewart and DeLong, this volume). Differential passage rates of cephalopod beaks versus otoliths in the stomachs of marine predators is another possible source of bias (Fiscus 1990; Miller 1978; Pitcher 1980). Such biases make it extremely difficult to accurately evaluate the energetic contribution of various prey species to the diet of northern elephant seals. Despite these limitations, we have demonstrated

the ability to detect changes in the diet of elephant seals that are associated with documented changes in the availability of prey (e.g., Pacific whiting and pelagic red crabs). Similar predator-prey relationships cannot be made for cephalopods and elephant seals because so little information is available on the ecology and status of cephalopod stocks in the North Pacific. This lack of information emphasizes the need for future studies on the ecological relationships between northern elephant seals and their prey.

Acknowledgments

We thank the following for their aid in this study: E. Berry, J. Barlough, D. DeMaster, S. Diamond, D. Hanan, S. Hawes, T. Loughlin, L. Hansen, J. Scholl, and D. Skilling for field assistance; J. Allen, S. Crockford, J. Dunn, D. Dwyer, B. Goetz, S. Hawes, F. G. Hochberg, D. Siefert, R. Wigen, and M-S. Yang for identifying prey remains; S. Melin for data base organization; B. Sinclair for assisting during the analysis of prey remains and for reviewing literature; A. York and L. Fore for statistical advice; and the staffs of the National Marine Mammal Laboratory, Alaska Fisheries Science Center, and Coastal Zone and Estuarine Studies Division Development Shop, Northwest Fisheries Science Center, Seattle, for help in constructing the lavage apparatus. J. Baker, B. Le Boeuf, R. Gentry, G. Kooyman, T. Loughlin, M. Perez, and B. Sinclair provided helpful critical reviews of the manuscript.

References

Aitkin, M., D. Anderson, B. Francis, and J. Hinde. 1989. Statistical Modeling in GLIM . Oxford: Clarendon Press.

Antonelis, G. A., and C. H. Fiscus. 1980. The pinnipeds of the California current. California Cooperative Oceanic Fisheries Investigations Report 21: 68–78.

Antonelis, G. A., C. H. Fiscus, and R. L. DeLong. 1984. Spring and summer prey of California sea lions, Zalophus californianus , at San Miguel Island, California, 1978–1979. Fishery Bulletin 82: 67–76.

Antonelis, G. A., M. S. Lowry, D. P. DeMaster, and C. H. Fiscus. 1987. Assessing northern elephant seal feeding habits by stomach lavage. Marine Mammal Science 3: 308–322.

Bailey, K. M., and D. G. Ainley. 1982. The dynamics of California sea lion predation of Pacific whiting. Fishery Research 1: 163–176.

Bailey, K. M., R. C. Francis, and P. R. Stevens. 1982. The life history and fishery of Pacific whiting, Merluccius productus. California Cooperative Oceanic Fisheries Investigations Report 23: 81–98.

Bailey, K. M., and L. S. Incze. 1985. El Niño and the early life history of recruitment of fishes in temperate marine waters. In El Niño North , ed. W. S. Wooster

and D. L. Fluharty, 143–165. Washington Sea Grant, University of Washington, Seattle.

Bartholomew, G. A. 1952. Reproductive and social behavior of the northern elephant seal. University of California Publications in Zoology 47: 369–472.

Bartholomew, G. A., and C. L. Hubbs. 1960. Population growth and seasonal movements of the northern elephant seal, Mirounga angustirostris. Mammalia 24: 313–324.

Best, E. A. 1963. Contribution to the biology of Pacific hake, Merluccius productus. California Cooperative Oceanic Fisheries Investigations Report 9: 51–56.

Butler, T. H. 1980. Shrimps of the Pacific coast of Canada. Canadian Bulletin of Fisheries and Aquatic Sciences 202.

Clarke, M. R., ed. 1986. A Handbook for the Identification of Cephalopod Beaks . Oxford: Clarendon Press.

Cooper, C. F., and B. S. Stewart. 1983. Demography of northern elephant seals, 1911–1982. Science 219: 969–971.

Cox, K. W. 1963. Egg-cases of some elasmobranchs and a cyclostome from California waters. California Fish and Game 49: 271–289.

Dark, T. A. 1975. Age and growth of Pacific hake, Merluccius productus. Fishery Bulletin 73: 336–355.

DeLong, R. L., and B. S. Stewart. 1991. Diving patterns of northern elephant seal bulls. Marine Mammal Science 7: 369–384.

DeLong, R. L., B. S. Stewart, and R. D. Hill. 1992. Documenting migrations of northern elephant seals using day length. Marine Mammal Science 8: 155–159.

Dorn, M. W., R. D. Methot, E. P. Nunnallee, and M. E. Wilkins. 1990. Status of the coastal Pacific whiting resource in 1990. Status of the Pacific coast groundfish fishery through 1990 and recommended acceptable biological catches for 1991. Stock assessment and fishery evaluation. Appendix Vol. I. Pacific Fishery Management Council, Portland, Ore.

Ermakov, Y. K. 1974. The biology and fishery of Pacific hake, Merluccius productus . Ph.D. dissertation, Pacific Scientific Institute of Marine Fisheries and Oceanography (TINRO), Vladivostok, USSR.

Fiedler, P. C., R. D. Methot, and R. P. Hewitt. 1986. Effects of California El Niño 1982–1984 on the northern anchovy. Journal of Marine Research 44: 317–338.

Fiscus, C. H. 1990. Notes on North Pacific gonatids: Identification of body fragments and beaks from marine mammals. Abstracts and Proceedings of the Annual Meeting held in Seattle, Wash., June 18–22, 1990, Western Society of Malacologists, Annual Report 23.

Hacker, E. S. 1986. Stomach content analysis of short-finned pilot whales (Globicephala macrorhynchus ) and northern elephant seals (Mirounga angustirostris ) from the southern California Bight. National Marine Fisheries Service, Southwest Fisheries Center Administrative Report LJ-86-08C.

Jefferts, K. 1983. Zoogeography and systematics of cephalopods of the northeastern Pacific Ocean. Ph.D. dissertation, Oregon State University, Corvallis.

Le Boeuf, B. J. 1974. Male-male competition and reproductive success in elephant seals. American Zoologist 14: 163–176.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous,

deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 66: 446–458.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, G. L. Kooyman, and R. W. Davis. 1986. Pattern and depth of dives in northern elephant seals, Mirounga angustirostris. Journal of Zoology, London 208: 1–7.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals. Canadian Journal of Zoology 67: 2514–2519.

Lowry, M. S., C. W. Oliver, C. Macky, and J. B. Wexler. 1990. Food habits of California sea lions, Zalophus californianus , at San Clemente Island, California. Fishery Bulletin 88: 509–521.

Miller, D. S., and R. N. Lea. 1972. Guide to the coastal marine fishes of California. California Department of Fish and Game, Fish Bulletin 157: 1–235.

Miller, L. K. 1978. Energetics of the Northern Fur Seal in Relation to Climatic and Food Resources of the Bering Sea . Marine Mammal Commission, Washington, D.C. (Available U.S. Department of Commerce, National Technical Information Service, as PB-275296.)

Nesis, K. N. 1982. Cephalopods of the World . Translated from Russian by B. S. Levitov and edited by L. A. Burgess. Department of Nekton, P. P. Shirshov Institute of Oceanography, USSR Academy of Sciences, Moscow.

Perrin, W. F., R. R. Warner, C. H. Fiscus, and D. B. Holts. 1973. Stomach contents of porpoise, Stenella spp. and yellowfin tuna, Thunnus albacares , in mixed-species aggregations. Fishery Bulletin 71: 1077–1092.

Pitcher, K. W. 1980. Stomach contents and feces as indicators of harbor seal, Phoca vitulina , foods in the Gulf of Alaska. Fishery Bulletin 78: 797–798.

Reiter, J., K. J. Panken, and B. J. Le Boeuf. 1981. Female competition and reproductive success in northern elephant seals. Animal Behaviour 29: 670–687.

Roper, C. F. E., and R. E. Young. 1975. Vertical distribution of pelagic cephalopods. Smithsonian Contributions to Zoology 209: 1–51.

Sakamoto, W., Y. Naito, A. C. Huntley, and B. J. Le Boeuf. 1989. Daily gross energy requirements of a female northern elephant seal, Mirounga angustirostris. Nippon Suisan Gakkaishi 55: 2057–2063.

Schmitt, W. L. 1921. The marine decapod crustacea of California. University of California Publications in Zoology 23: 1–470.

Stewart, B. S., and R. L. DeLong, 1990. Sexual differences in migrations and foraging behavior of northern elephant seals. American Zoologist 30: 44A.

Stewart, B. S., P. K. Yochem, and R. W. Schreiber. 1984. Pelagic red crabs as a food source for gulls: A possible benefit of El Niño. Condor 86: 341–342.

Thompson, H. 1948. Pelagic tunicates of Australia . Commonwealth Council for Scientific and Industrial Research, Melbourne, Australia.

Trillmich, F., and K. Ono, eds. 1991. Pinnipeds and El Niño . Heidelberg and Berlin: Springer Verlag.