An Overview of the Ecology of Antarctic Seals 1
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1 AMER. ZOOL., 31: (1991) An Overview of the Ecology of Antarctic Seals 1 DONALD B. SINIFF Department of Ecology, Evolution and Behavior, University of Minnesota, Minneapolis, Minnesota SYNOPSIS. Four species of seals occupy the pack-ice region of the oceans surrounding the Antarctic Continent. These seals include the crabeater (Lobodon cardnophagus), leopard (Hydrurga leptonyx), weddell (Leplonychotes weddellii), and ross (Ommatophoca rossii), and are true seals with special adaptations for living in the pack-ice region. Two other seal species, the southern elephant seal (Mirounga leonina) and the fur seal (Arctocephalus gazella) (the only eared seal of this region) generally occur further to the north and use land rather than ice during the period of birth of young. This paper reviews the status of these species, and examines the general ecology of the four species that inhabit the pack-ice zone. In general, the four species that occupy the pack-ice zone have specialized in habitats and habits so that little overlap in diets or habitat use exist among these species. The exception is the interaction between the leopard and the crabeater which occupy the same regions and eat krill (Euphausia superba), particularly during the winter. The impact of the potential harvest of krill by man on these species is discussed. Further, the impact that recovery of the large baleen whales that feed in this region during the summer is discussed with regard to the changes that might occur as competition for krill by the large vertebrate species increases. INTRODUCTION The Southern Ocean is occupied by six pinniped species and it is generally considered that each species represents a separate genus, thus 6 out of 19 pinniped genera worldwide are represented in this area (Laws, 1984). One in particular, the crabeater seal {Lobodon cardnophagus), is so abundant it is thought to comprise about half of the total world stock of pinnipeds (Laws, 1977). Within these six species of pinnipeds are five species of true seals (Family Phocidae). These include the crabeater previously mentioned, the leopard seal (Hydrurga leptonyx), the weddell seal (Leptonychotes weddelli), the ross seal (Ommatophoca rossii) and the southern elephant seal (Mirounga leonina). The single species of eared seal, the Antarctic (Kerguelen) fur seal (Arctocephalusgazella), is generally considered to be the only member of the Family Otariidae that occupies this region (Laws, 1984), although the closely related species Arctocephalus tropicalis occurs to the north and the two species overlap in range at Marion Island (Condy, 1978). The four species of Antarctic seals that 1 From the Symposium on Antarctic Marine Biology presented at the Annual Meeting of the American Society of Zoologists, December 1988, at San Francisco, California. generally occupy the pack-ice region are the crabeater, the leopard, the weddell, and the ross seal. The elephant seal is generally found more to the north in the sub-antarctic islands. The four species of seals that occupy the pack-ice region have never been exploited by man and thus are often considered pristine with respect to man's influence on their populations. The elephant seal and fur seal were driven to near extinction by exploitation in the late 19th century (Bonner, 1982). Since then they have recovered and have expanded into some of the areas that they previously occupied. However, the current growth of the elephant seal population seems to have stopped in some areas and it is even declining in others (McCann and Rothery, 1988). This paper is concerned with the current status of the four species, because they have not been exploited previously, have been proposed to be used as monitors or indicators of changes in the ecosystem as interest in exploiting the fishes, krill and other resources of Antarctica continue to develop. Various nations that belong to the recently ratified Convention for the Conservation of Antarctic Marine Living Resources (CCAMLR) are developing research programs to establish long-term data bases for certain environmental and population parameters of seals and pen- 143
2 144 DONALD B. SINIFF guins. These data are intended to be used to reflect changes in the system brought about by man's exploitation of biological and mineral resources of this region. This paper examines our current knowledge of the four pack-ice species of Antarctic seals and points out concerns and problems associated with using population parameters to monitor ecosystem changes. ANTARCTIC SEALS OF THE PACK-ICE AND FAST-ICE Crabeater seal The crabeater seal occupies the pack-ice region that surrounds the Antarctic continent. Its population size has been estimated to be between 15 and 30 million (Laws, 1977, 1984) and it is considered the most abundant seal in the world. Although considered to be increasing in abundance, based on changes in age at maturity (Bengston and Laws, 1985), more recent work (Erickson and Hanson, 1990) suggests populations may have recently declined in abundance. This species forms family groups in packice regions in the spring (Oritsland, 1970; Siniff et al., 1979; Shaughnessy and Kerry, 1989) which are composed of a male, female and pup. The length of time the family group remains together is uncertain, but is considered to be 14 to 21 days by Shaughnessy and Kerry (1989) rather than the four weeks speculated by Siniff et al. (1979). The crabeater feeds almost exclusively on the Antarctic krill (Euphausia superba) (Oritsland, 1977; Laws, 1984), the major food item of many of the large baleen whales that, before being decimated by commercial whaling, occupied the Antarctic waters during the summers. This seal species has special lobed teeth which assist it in sifting the small shrimp-like organisms from the water. Two predators have played a significant role in the evolution of the crabeater's life history: the killer whale (Orcinus orca) and the leopard seal. It is well known that the killer whale actively seeks crabeaters of all ages while the leopard seal preys primarily upon newly-weaned pups or animals in their first year of life (Siniff and Bengston, 1977; Laws, 1984). This predator pressure has been hypothesized as being a major evolutionary force in the crabeater's life history, particularly during the mating and pupping season. The crabeater seal has received recent attention because it is hypothesized to be one of the first species impacted by a significant harvest of Antarctic krill. Under the CCAMLR, there has been agreement to limit any commercial harvest of Antarctic krill to a level that will not significantly impact other species of the ecosystem. The crabeater seal would seem to be an organism which would respond to declines in krill abundance. Thus, measures of feeding activity, body condition, and other biological parameters have been suggested for use in determining the effect of commercial harvest of krill upon the ecosystem. As of this time, no significant harvest of krill has taken place in Antarctic waters and studies establishing baseline information for measures of parameters are currently being discussed. Weddell seal The life history of the weddell seal is well documented since it occupies fast-ice environments close to the Antarctic continent and often adjacent to Antarctic bases. Pregnant females come onto the surface of the ice, along predictable annual tide cracks, to give birth in late October and November. In the more northern regions, pupping sometimes occurs in September. Two different studies have shown considerable differences in pupping rates between weddells at the northern extremes (Signey Island) of their range, and those at the southern extreme (McMurdo Sound) (Croxall and Hiby, 1983). In McMurdo Sound annual pupping rates varied from 0.46 to 0.79, which Croxall and Hiby (1983) considered to be related to an age bias in tagged samples. However, it now appears that there have been large differences in annual pupping rates in McMurdo Sound (Testa, 1987) although the exact cause is unknown. The length of the weddell pup's dependency period is between five and six weeks.
3 ECOLOGY OF ANTARCTIC SEALS 145 Towards the end of this period, females come into estros and breeding occurs. Adult males occupy underwater territories beneath the cracks in the ice which also provide access to the surface for the females. Breeding occurs under the ice in these regions. Weddell seals feed primarily on fish species, particularly the Antarctic cod (Dissostichus mawsoni) and the Antarctic silverfish (Pleuragramma antarcticum). Long-term studies of physiology (Kooyman, 1981) and population characteristics (Testa and Siniff, 1987), of weddell seals have been carried out in McMurdo Sound. Also, as indicated above, long-term population studies have occurred at Signey Island (Croxall and Hiby, 1983). These studies have generally indicated that the weddell, once it is an adult, returns to annually the same pupping colony with a high degree of predictability. However, young animals disperse away from the colonies where they are born, and probably spend the first four to five years of their lives in pack-ice regions. As they approach maturity, they move ashore and onto fast-ice areas where colonies occur. Once they have moved into a colony as adults, they remain in these areas for annual pupping and breeding (Testa and Siniff, 1987). Since the weddell's distribution is restricted primarily to near-shore fast-ice, it is unlikely that commercial ventures exploiting krill or other resources will have a significant impact upon this species. The population has been estimated to number approximately 800,000 and is basically stable, except for some colonies which occur close to Antarctic bases where seals have been "harvested" in order to feed dog teams. It may prove that future exploitation of krill may influence young weddell seals because of their off-shore dispersal and dependence on pelagic prey. The seals are not impacted by predators during most of their adult life as they remain close to shore in heavy pack-ice regions, where access by killer whales and leopard seals is limited. As the ice breaks up in the austral spring and summer, a few are preyed upon by killer whales and even smaller numbers by leopard seals, but the overall impact of predation is considered small (Testa and Siniff, 1987). Leopard seal The leopard seal is the largest of the four Antarctic seal species and has become known for its rather spectacular predatory activities. It regularly kills warm-blooded animals but feeds as well on fish, cephalopods, and Antarctic krill (Siniff and Stone, 1985). It is well known for its foraging activity around penguin colonies where it preys on young penguins as they go to sea for the first time. At this time, in late summer, leopard seals often stalk the shoreline waiting for young, naive birds to enter the water on their way out to sea. More recently, leopard seals have been documented taking young, recently weaned, crabeater seals (Siniff and Stone, 1985). The leopard seal is a solitary animal, and little is known about its movement patterns in the Antarctic pack-ice regions. Immature leopard seals are known to congregate regularly on sub-antarctic islands as they migrate north during the late autumn and winter (Rounsevell and Eberhard, 1980; Rounsevell, 1988). Recently, the degree to which leopard seals move northward seems to be cyclic, and has been hypothesized to be correlated with regional oceanograhic features of the Antarctic pack-ice (Testa et al., 1991). The reproductive cycle and behavior of the leopard seal during the pupping and breeding seasons are not well known. Siniff and Stone (1985) summarized data from collected animals, field observations, and the literature. Leopard seal pupping occurs in November, with breeding occurring within the next month. The female is not accompanied by the male during the period of lactation. Behavior during breeding has not been observed. Diet is generally varied but seasonal differences do occur (Siniff and Stone, 1985). During the midsummer period of December and January, newly-weaned crabeater seals become important prey. Then in late January and February, young penguins become available and are extensively taken. Antarctic krill compose up to 60 percent of the leopard seal's diet throughout the
4 146 DONALD B. SINIFF year, with krill being the most important prey item during the winter (Lowry et al., 1988). Fish and cephalopods are also taken periodically, composing about 5 to 20 percent of the diet over the year. The leopard seal is a very important predator in the Antarctic marine ecosystem and has presumably had a significant impact upon the evolution of life history patterns of many vertebrate species, particularly crabeater seals and various penguin species. During the winter, it would appear that the leopard seal competes directly with various krill-feeding specialists, particularly the crabeater seal. Because the leopard seal is a feeding generalist it may be less efficient in its foraging abilities, and thus be at a disadvantage should krill become scarce at this time. Ross seal The ross seal is the least known of the four Antarctic species. For unknown reasons, it is relatively rare in Antarctic packice waters. The population size has been estimated to be around 220,000 (Laws, 1984). It has been sighted in all pack-ice regions which surround the Antarctic continent, so it has wide distribution, but it is never very abundant in any one location. It seems to be most abundant in the King- Haakon-VII Sea, where the South African Antarctic Research Program has found it to make up about 15 percent of the seals in the pack-ice (Condy, 1977). The reproductive period of this species appears to be in November and December, with breeding occurring from mid-february to early March (Laws, 1984). Most collections of this species have shown that it feeds primarily on cephalopods and probably has deep diving capabilities (Laws, 1984). It would appear that any changes in krill abundance, that may be anticipated because of commercial harvest, will probably not have any direct effect upon the distribution and abundance of this species. Further, because the ross seal is so rare, it would be difficult to obtain sufficient data to document changes in its population status that would be tied to changes caused by any commercial ventures. It has never been harvested by man, and it would appear that changes in the ecosystem brought about by the past exploitation of whales would only have enhanced its food resources. OVERVIEW OF THE FOUR SPECIES OF PACK-ICE SEALS Laws (1984) provides an excellent review of our current understanding of the life history, population status and general understanding of the biology of the weddell, leopard, ross, and crabeater seals. Table 1 summarizes the main life history characteristics of these four species and indicates their major differences and similarities. These species differ greatly in their feeding habits and the life history patterns that characterize their reproductive biology. However, they share such characteristics as occupancy of the pack-ice region and a circumpolar distribution. Their relative abundances differ greatly. As mentioned earlier, the crabeater is by far the most abundant species. The reasons for these differences in abundance are not well known, although it appears that the crabeater has taken advantage of a superabundant prey species, the Antarctic krill, and has become a specialist at feeding upon this particular prey item. The leopard seal occupies a high trophic level, feeding upon many vertebrate and several invertebrate species. The weddell seal exploits the fastice, living very close to the Antarctic continent, and has adaptations which the other seals lack and which allow it to persist in these regions. It is a specialist in a habitat sense. The reason for the scarcity of the ross seal is simply unknown. It appears to be a cephalopod-feeding specialist and because of its unique adaptations and habitat requirements it might be too specialized to ever become very abundant, perhaps because of the lack of cephalopods within the pack-ice region throughout much of the year. CONCLUSIONS As mentioned earlier, the four species of Antarctic seals occupying the pack-ice zone have not been impacted directly by activities of man in the Southern Ocean. This
5 Species eddell (Leptonychotes weddelli) rabeater (Lobodon carcinophagus) eopard (Hydrurga le/jtonyx) oss (Ommatophoca rossii) TABLE 1. A summary of the various life history aspects of the four species of Antarctic seals that live in the pack-ice zone. Habitat Usually heavy, persistent ice, close to Antarctic continent Pack ice, floes Pack ice, floes Pack ice, floes Pattern of distribution Clumped, particularly during breeding, pupping, and moulting seasons Dispersed (group sizes average 2-3) Dispersed, single animals most common Dispersed Food Fish; a few species Krill; mostly one species Birds (penguins), seals (crabeater weanlings), fish, krill, cephalopods Mostly cephalopods and a few fish species Pupping and mating characteristics Polygamous, males defend underwater territories, breeding at end of lactation Serial monogomy, males defend female/pup pairs, breeding in male/female pairs after weaning. Mostly unknown, female alone with pup, breeding proposed within one month after weaning Mostly unknown, female alone with pup, breeding may occur about one month after weaning Predator pressure Little, killer whale; rarely leopard seal Intense, leopard seals and killer whales Some, killer whales Some, killer whales and perhaps leopard seals Annual pupping/ pregnancy rates Pupping: ; pregnancy: Pregnancy: Pregnancy: 0.47, 0.61, 0.85 and 0.93 (four data sets) Pregnancy: 0.88 and 0.90; from two small data sets O o 0 o 1) ;> z o n o m r
6 148 DONALD B. SINIFF seems to be because they have occupied the pack-ice region, and they have simply not been available for commercial harvest because of their inaccessibility and the high cost of operating in such vigorous habitats. It seems unlikely that the economics of this situation will change in the near future, and it is very probable that these four species will remain relatively untouched, at least directly, by human activities. These four species of seals belong to a general group of species which we call large mammals. This group has certain characteristics in common which make them unique but difficult to study (Fowler and Smith, 1981). The most common characteristic that makes this true is their lengthy lifespan, an attribute which makes it difficult to understand their population dynamics, as scientists need to follow population parameters for many years. Since individuals often live 25 or 30 years, making predictions about changes in population parameters requires observations on the same population for at least this long. This has been difficult and, with the exception of two studies in weddell seals (Croxall and Hiby, 1983; Testa, 1987), data on Antarctic seal species are often limited to brief population censuses, or other short-term observations. Although the four species of pack-ice seals have not been exploited, many of their competitor species have been harvested extensively. For example, most of the species of large whales that summered in the Southern Ocean, were driven to very low population levels because of extensive pressure from commercial whaling (Allen, 1980). Also, populations of southern elephant seals and southern fur seals were dramatically reduced (Bonner, 1982). Therefore, the ecosystem in which the pack-ice seals live is far from pristine and is, in fact, recovering from the previous exploitation of the other species of large mammals. These recovering species often forage on the same prey items as the packice seals, and thus, it seems certain that competition for food, particularly krill, is probably increasing. This should increase competitive interactions among these large species of mammals, and should have measurable effects upon the population dynamics of the species involved. For example, it has been hypothesized (Siniff and Stone, 1985; Lowry et al., 1988) that crabeater and leopard seals compete for krill particularly during the winter. It seems likely that as other large krill-feeding mammals increase in abundance this competition will increase with resultant changes in behavior, movement patterns, and/or population parameters of these two species. Moreover, the causes for the cycles postulated by Testa et al. (1989) are unknown at the present time. It is unknown what effect the recovery of large mammals will have upon the Antarctic seals, but certainly it will be a complicating factor in interpreting population data. At the present time, the CCAMLR is considering certain parameters associated with the pack-ice seals to be used as indices with respect to krill abundance in certain regions of the Antarctic. For example, they are proposing to measure such parameters as foraging times of penguins going to sea to obtain food for their chicks, growth rates of southern fur seal pups whose mothers feed primarily on krill, foraging times and foraging cycles of crabeater seals in the pack-ice region particularly during the winter, and other parameters associated with krill-feeding predators. The theme common to these measurements is that harvesting of krill by man will reduce its abundance in the Southern Ocean and this reduction will be reflected in longer foraging times and slower growth rates. While the logic of such measurements seems clear, it is obvious that these measurements are being made on a dynamic system which is recovering from an extreme disturbance created by recent overharvesting of large mammals. Moreover, Doidge and Croxall (1989) have shown how the behavior of individual females influences weight gain in fur seal pups, and therefore, may be a major influence on weight gain over a wide range of resource states. It could be expected that changes in foraging parameters will occur, but the relationship of these to changes in krill abundance is obscure. Harvest of krill by man may complicate the relationships involved, but it seems that any
7 ECOLOGY OF ANTARCTIC SEALS 149 impacts caused by man may be likely to become lost in this changing system. It is important that future studies of the Antarctic pack-ice seals be focused on furthering our understanding of the basic life history characteristics of these species. For example, it is critical that we document mating systems and attempt to understand the evolutionary pressures that brought about these systems. Further, it would seem important that we document current distributions and abundance since these may be the first to change as competition for krill increases. Changes in population and foraging parameters may have little to do with man's current influence, but more to do with changes in the overall system as it recovers from man's previous activities. REFERENCES Allen, K. R Conservation and management of whales. University of Washington Press, Seattle. Bengston, J. L. and R. M. Laws Trends in crabeater seal age at maturity: An insight into Antarctic marine interactions. InW.R. Siegfried, P. R. Condy, and R. M. Laws (eds.), Antarctic nutrient cycles and food webs, pp Springer- Verlag, Berlin. Bonner, W. N Seals and man, a study of interactions. University of Washington Press, Seattle. Condy, P. R Results of the 4th seal survey in the King-Haakon-VII Sea Antarctica. South Afr. J. Res. 7: Condy, P. R Distribution, abundance and annual cycle of fur seals {Arctocephalus spp.) on the Prince-Edward Islands South Africa. South Afr. J. Wildlife Res. 8: Croxall.J. P. and L. Hiby Fecundity, survival and site fidelity in weddell seals, Leptonychotes weddelli.]. Appl. Ecol. 20: Doidge, D. W.andJ. P.Croxall Factors affecting weaning weight in Antarctic fur seals (Arctocephalus gazella) at South Georgia. Polar Biol. 9(3): Erickson, A. W. and M. B. Hanson Continental estimates and population trends of Antarctic ice seals. In K. Kerry and G. Hempel (eds.), Proceedings 5th Symposium on Antarctic Biology, pp Springer-Verlag, Berlin, Heidelberg. Fowler, C. W. and T. D. Smith Dynamics of large mammal populations, pp John Wiley and Sons, New York. Kooyman, G. L Weddell seal consummate diver. Cambridge University Press, Cambridge. Laws, R. M The significance of vertebrates in the Antarctic marine ecosystem. In G. A. Llano (ed.), Adaptations within Antarctic ecosystems, pp Proceedings of the 3rd SCAR Symposium on Antarctic Biology. Smithsonian Institution, Washington, D.C. Laws, R. M Seals. In R. M. Laws (ed.), Antarctic ecology, Vol. 2, pp Academic Press, London. Lowry, L.,J. W. Testa, and W. Calvert Winter feeding of crabeater and leopard seals near the Antarctic Peninsula. Polar Biol. 8(6): McCann, T. S. and P. Rothery Population size and status of the southern elephant seal (Mirounga leonina) at South Georgia, Polar Biol. 8(4): Oritsland, T Sealing and seal research in the southwest Atlantic pack ice, Sept.-Oct In M. W. Holdgate (ed.), Antarctic ecology, Vol. 1, pp Academic, New York. Oritsland, T Food consumption of seals in the Antarctic pack ice. In G. A. Llano (ed.), Adaptations within Antarctic ecosystems, pp Proceedings of the 3rd SCAR Symposium on Antarctic Biology. Smithsonian Institution, Washington, D.C. Rounsevell, D Periodic eruptions of itinerant leopard seals with the Australasian sector of the Southern Ocean, Pap. Proc. R. Soc. Tasm., 122: Rounsevell, D. and I. Eberhard Leopard seals, Hydrurga leptonyx (Pinnipedia), at Macquarie Island from 1949 to Austral. Wildlife Res. 7: Shaughnessy, P. D. and K.R.Kerry Crabeater seals (Lobodon carcinophagus) during the breeding season: Observations on five groups near Enderby Land, Antarctica. Marine Mammal Sci. 5(1): Siniff, D. B. and J. L. Bengston Observations and hypotheses concerning the interactions among crabeater seals, leopard seals and killer whales. J. Mammal. 58: Siniff, D. B. and S. Stone The role of the. leopard seal in the tropho-dynamics of the Antarctic marine ecosystem. In W. R. Siegfried, P. R. Condy, and R. M. Laws (eds.), Antarctic nutrient cycles and food webs, pp Proceedings of the 4th SCAR Symposium on Antarctic Biology. Springer-Verlag, Berlin, Heidelberg, New York. Siniff, D. B., I. Stirling, J. L. Bengston, and R. A. Reichle Social and reproductive behaviour of crabeater seals, Lobodon carcinophagus, during the austral spring. Can. J. Zool. 57: Testa, J. W Long-term reproductive patterns and sighting bias in weddell seals (Leptonychotes weddelli). Canad.J. Zool. 65(5): Testa, J. W., R. Oehlert, J. Bengston, R. Laws, D. Ainley, and D. Siniff Temporal variability in Antarctic marine ecosystems: A possibility. J. Fish, and Aquatic Sci. (In press) Testa, J. W. and D. B. Siniff Population dynamics of weddell seals (Leptonychotes weddelli) in McMurdo Sound, Antarctica. Ecological Monogr. 57:
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