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Eared Seals
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E EARED SEALS Otariidae B. Louise Chilvers The pinniped family Otariidae or the eared seals (sea lions and fur seals) is composed of seven extant genera with 16 species (Table 1). The word “otariid” comes from the Greek word otarion meaning “little ear,” referring to the small but visible external ear flaps (pinnae), which distinguish Otariidae from other pinnipeds. Otariids are distributed predominately in the southern hemisphere, with only three species in the North Pacific. The family is traditionally divided into two subfamilies, Otariinae (sea lions; 5 genera with 6 extant species, 1 extinct) and Arctocephalinae (fur seals; 2 genera with 10 species).
I. Classification Otariids are thought to have evolved in the Miocene (15–17 million years ago) in the North Pacific. Fossil records and genetics indicate that the family diversifying rapidly while spreading into the southern hemisphere, where all but three of the extant species now live. Molecular phylogenetic studies support the hypothesis that the basal position, or oldest species, in this family is Callorhinus ursinus (the Northern fur seal; Fig. 1). Otariids are divided into two subfamilies, fur seals (Arctocephalinae) and sea lions (Otariinae), with the major distinctions between them being the larger size of sea lions and the presence of a thick underfur layer in fur seals. The sea lions are genetically well defined in five genera and six extant species and one extinct species (Table 1). However, there is still debate regarding the taxonomic structure of the fur seals (Wynen et al., 2001; Berta and Churchill, 2012). Herein, the IUCN taxonomic classification of fur seals is followed, in which fur seals are classified into two genera: Callorhinus in the North Pacific with a single species representative, the Northern fur seal, and nine species in the southern hemisphere within the genus Arctocephalus (Table 1). The close relationship between sea lions and fur seals is indicated by intergenetic hybrids. At Macquarie Island, Australia’s subantarctic, New Zealand fur seal males mate with Antarctic fur seal females, Arctocephalus gazella and subantarctic, A. tropicalis female fur seals and produce hybrid pups (Lancaster et al., 2006). In the North Pacific, Californian sea lions are known to interbreed with both Steller sea lions and northern fur seals.
II. Morphology and Physiology The most distinctive feature that distinguishes otariids from phocids is their external ears. Along with the external ear pinnae, they have an air-filled external auditory canal and middle ear structure more similar to terrestrial mammals’ ears than other marine mammals. Otariids have semiaquatic lifestyles, feeding and migrating in the sea, but breeding and resting on land. They have much Encyclopedia of Marine Mammals. © 2018 Elsevier Inc. All rights reserved.
larger fore flippers and pectoral muscles than phocids, relatively speaking, and they have the ability to turn their hind limbs forward and walk on all fours, making them far more maneuverable on land. These larger fore flippers and pectoral muscles are also the mechanism by which otariids propel themselves in the water, rather than the hind-flipper-driven swimming typical of phocids. This swimming style means they can attain higher bursts of speed and have greater maneuverability in the water than phocids. Otariids also have more dog-like shaped heads with sharp, well-developed canines relative to phocids. There are distinct morphological and behavioral differences between fur seals and sea lions. Compared to sea lions, fur seals have a thick underfur used for insulation as well as the coarse guard hairs found on sea lions, are generally smaller, eat smaller prey, and go on longer foraging trips. Male otariids range in size from the 70 kg (150 lb) Galapagos fur seal to over 1000 kg (2200 lb) for the Steller sea lion. Similarly, female otariids range from 25 kg (60 lb) for the Galapagos fur seal to 270 kg (600 lb) for the Steller sea lion. Mature male otariids weigh two to six times as much as females, with proportionately larger heads, necks, and chests, and males in most species have predominant manes, which are not found among phocids.
III. Distribution and Habitat All otariids breed between 60°S and 55°N latitude. Most of the species (four sea lion and six fur seal species) breed in temperate latitudes, two species, the Galapagos sea lion and fur seal, breed on the equatorial Galapagos Islands, and the remaining four species breed in high temperate or subpolar regions (Table 1; Schipper et al., 2008). Northern fur seals, Californian and Steller sea lions are the only species that still breed in their ancestral range within the North Pacific. The two northern sea lion species are also the only two sea lion species that have overlapping ranges, while all other sea lions are allopatric to the countries and areas they are named after. The South American sea lion and fur seal, and Antarctic fur seal are the only species that breed in the Southern Atlantic Ocean. There are no otariids in the North Atlantic. The extent to which the modern distribution of otariids is a reflection of their decimation during 19th-century sealing, which led to the near extinction of most species, is unknown. Breeding occurs on both mainland and island sites within their ranges but due to past and present human pressures, island sites predominant worldwide, with four species restricted to island group distributions (i.e., Galapagos sea lion and fur seal, Juan Fernandez fur seal, and the New Zealand sea lion). Otariids’ preferred breeding substrate is rock or sand, although species like the New Zealand sea lions are known to travel up to 1.5 km inland and up to 400 m above sea level when breeding; some occupy forest areas. Knowledge of the at-sea distributions of otariids is predominately based on data from foraging lactating females, which are known to be restricted in their foraging range due to the need to
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TABLE 1 Distribution, Abundance, and Conservation Status (IUCN Red List Classification and Trend) of Otariids
E
Common Name
Scientific Name
Location
Population Estimatesa
IUCN Threat Status and Trenda
Steller sea lion California sea lion Galapagos sea lion Australian sea lion New Zealand sea lion South American sea lion Northern fur seal Galapagos fur seal South American fur seal New Zealand fur seal Antarctic fur seal Juan Fernandez fur seal Cape fur seal Australian fur seal Guadalupe fur seal Subantarctic fur seal
Eumetopias jubatus Zalophus californianus Z. wollebaeki Neophoca cinerea Phocarctos hookeri Otaria byronia Callorhinus ursinus Arctocephalus galapagoensis A. australis A. forsteri A. gazella A. phillippii A. pusillus pusillus A. p. doriferus A. townsendi A. tropicalis
High north temperate North temperate Equatorial South temperate South temperate South temperate Subpolar (Arctic) Equatorial South temperate South temperate Subpolar (Antarctic) North temperate South temperate South temperate North temperate High south temperate
140,000 380,000 15,000 12,700 11,700 250,000+ 1,290,000 15,000 300,000+ 200,000+ 6,000,000+ 32,000 2,000,000 12,000 20,000 400,000
Near threatened—increasing Least concern—increasing Endangered—decreasing Endangered—decreasing Endangered—decreasing Least concern—stable Vulnerable—decreasing Endangered—decreasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—stable
a
IUCN Red List (www.iucnredlist.org).
at sea). All male otariids are known to move away or “migrate” from breeding areas outside the breeding seasons; however, these migrations may still be within island groups for Galapagos species, while others can cover 100 s or even 1000 s of kilometers.
IV. Behavior and Ecology
Figure 1 The northern fur seal, Callorhinus ursinus, is thought to be the oldest species in the Otariidea family (Photo by Brian Fadely-NOAA Fisheries, Permit No. 14327). return to dependent pups on land. In general, otariids at sea ranges occur predominately over and on the edges of the continental shelves or in trenches and upwellings close to their breeding colonies. Overall, fur seal species usually have significantly longer foraging trips (250 km from colony) and spend more days at sea (average 5–9 days depending on age of pup) than sea lion species (average 30–100 km from colony depending on species and 1–3 days
Otariids are colonial, highly synchronized annual breeders, aggregating on traditional breeding beaches or rocky areas, with the exception of the Australian sea lion, which breeds year-round. Most otariid females are highly philopatric to the breeding area where they were born, with some species known to be philopatric to areas within 100 m of their birth place. All species are polygynous with territorial males breeding with more than one female. There is high variability to the extent to which males control females within the breeding areas between species. For the majority of otariids, males arrive first at breeding areas and establish and hold territories. Females typically arrive ashore 1 or 2 days before giving birth and are usually in estrous within 5–10 days after giving birth. After birth, females cycle time at sea foraging and time on shore with their pups. Most otariid colonies have highly synchronized birth pulses, with the majority of births occurring in a 2–3 week period. All otariids have a period of embryonic diapause (delayed implantation) of 3–4 months following fertilization with gestation believed to be 8–9 months, allowing for pup births and mating to occur in a 12-month cycle (Gentry and Kooyman, 1986). The exception to this rule is the Australian sea lion (Fig. 2) which has a 17.5 month breeding cycle with the gestation period extended to up to 14 months, although the pups when born are no more developed than other otariid pups. Female Australian sea lions are highly philopatric, with colonies <100 km apart breeding 5–6 months apart due to the high philopatry of the resident females. For most otariid species, females reach sexual maturity at 3 years of age and breed for the first time between 3 and 5 years of age. Males typically mature at 5–7 years of age, and breed even later
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E Figure 2 The Australian sea lion, Neophoca cinerea, has an atypical 17.5 month, nonsuccinct breeding cycle, thought to have arisen due to the highly variable environment in which this species evolved (Photo by Mark Hindell). due to the need to be socially mature, that is, large and dominant enough to hold breeding territories. Males typically only live to be teenagers, while females are known to live and breed well into their late 20s. Females only have one pup per breeding episode, and often have gaps between pups. Pup survival in the first year is highly variable (from 0 to 90+% survival) for otariids depending on species, climate affects (El Niño events), disease events, and maternal investment levels, meaning the life time pup production for a female otariid can range from 0 to 10 pups. Otariids are visual, generalist foragers that feed on fish, squid, and crustaceans (including krill). Some male otariids are also known to feed on sea birds and fur seal pups. Sea lions tend to feed close to shore over continental shelves, targeting larger fish, octopus, and squid, while the smaller fur seals tend to take longer, offshore foraging trips during which they feed on larger numbers of smaller prey items including krill. These foraging patterns strongly reflect the central-place foraging patterns of female otariids that combine land-breeding and rearing of pups with marine foraging.
V. Interactions With Humans Contact with humans leads to the extinction of the Japanese sea lion (Zalophus japonicas) and the near extinction of many other otariids, due to excessive harvesting. Their colonial, terrestrial breeding, at predicable locations, made them highly vulnerable to overexploitation. The fur seal and sea lion species that survived historical sealing did so only in dramatically reduced numbers in highly restricted locations. For example, the Antarctic fur seal (now the most abundant otariid; Table 1) was thought to be extinct from overharvesting; however, a few small populations were found on isolated islands (Wynen et al., 2001). Harvesting of otariids is now limited to subsistence harvest from first nations in the North Pacific (predominately of Northern fur seals) and commercial harvests of Cape fur seals in Namibia (Cumming, 2015). Most species are still recovering, dispersing into their former ranges, and increasing in numbers. Some species still have highly restricted ranges such as the Australian and New Zealand sea lions (Table 1). Currently, the greatest threat to otariids arises from direct and indirect fisheries interactions. Across all pinnipeds, one in three species is classified as threatened compared to one of five mammals generally and this is mainly due to fisheries interactions (Kovacs
Figure 3 Marine debris entanglement and digestion is an increasing problem for otariids (Photo by B. Louise Chilvers).
et al., 2012). Incidental mortality in fishing operations, commonly referred to as bycatch, is an acute threat for Australian and New Zealand sea lions and a possible factor in the complex assemblage of reasons for the decline of the Steller sea lion (Read, 2008). Indirect fisheries interactions including intentional shooting of pinnipeds by fishermen, competition for fish resources, and fisheries-induced changes to ecosystems that change prey abundance and distribution can additionally impact otariid populations. Marine debris entanglement and digestion is an increasing problem for individual animals; however, it is not known if or how these interactions affect populations (Fig. 3; Page et al., 2004). In the near future, global climate change is likely to be a factor influencing otariids abundance and distribution, however, to a lesser extent than for ice breeding phocid species (Kovacs et al., 2012). Expected changes in ocean currents due to global warming are likely to alter prey abundance and distribution, with the highest impacts expected to be experienced by South Pacific otariids, given the significant role of El Niño events in the Southern Oscillation (Nicholls, 2008).
References Berta, A., and Churchill, M. (2012). Pinniped taxonomy: Review of currently recognized species and subspecies, and evidence used for their description. Mamm. Rev. 42, 207–234. Cumming, D.H.M. (2015). Seal Range State Policy and Management Review. IUCN SSC/CEESP Sustainable Use and Livelihoods Specialist Group, Gland, Switzerland. Gentry, R.L., and Kooyman, G.L. (1986). “Fur Seals: Maternal Strategies on Land and at Sea.” Princeton University Press. Kovacs, K.M., Aguilar, A., Aurioles, D., Burkanov, V., Campagna, C., Gales, N., Gelatt, T., Goldsworthy, S.D., Goodman, S.J., Hofmeyr, G.J.G., Härkönen, T., Lowry, L., Lydersen, C., Schipper, J., Sipilä, T., Southwell, C., Stuart, S., Thompson, D., and Trillmich, F. (2012). Global threats to pinnipeds. Mar. Mamm. Sci. 28, 414–436. Lancaster, M.L., Gemmell, N.J., Negro, S., Goldsworthy, S., and Sunnucks, P. (2006). Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Mol. Ecol. 15, 3681–3692. Nicholls, N. (2008). Recent trends in the seasonal and temporal behaviour of the El Nino-Southern Oscillation. Geophys. Res. Lett. 35, L29703.
Earless Seals
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Page, B., McKenzie, J., McIntosh, R., Baylis, A., Morrissey, A., Calvert, N., Haase, T., Berris, M., Dowie, D., Shaughnessy, P.D., and Goldsworthy, S.D. (2004). Entanglement of Australian sea lions and New Zealand fur seals in lost fishing gear and other marine debris before and after Government and industry attempts to reduce the problem. Mar. Pollut. Bull. 49, 33–42. Read, A.J. (2008). The looming crisis: interactions between marine mammals and fisheries. J. Mamm. 89, 541–548. Schipper, J., Chanson, J., Chiozza, F., Cox, N., Hoffmann, M., Katariya, V., Lamoreux, J., Rodrigues, A., Stuart, S.N., Temple, H.J., Baillie, J., Boitani, L., Lacher, T.E., Mittermeier, R.A., Smith, A.T., Absolon, D., Aguiar, J.M., Amori, G., Bakkour, N., Baldi, R., Berridge, R.J., Bielby, J., Black, P.A., Blanc, J.J., Brooks, T.M., Burton, J.A., Butynski, T.M., Catullo, G., Chapman, R., Cokeliss, Z., Collen, B., Conroy, J., Cooke, J.G., da Fonseca, G.A.B., Derocher, A.E., Dublin, H., Duckworth, J.W., Emmons, L., Emslie, R.H., Festa-Bianchet, M., Foster, M., Foster, S., Garshelis, D.L., Gates, C., Gimenez-Dixon, M., Gonzalez, S., Gonzalez-Maya, J.F., Good, T.C., Hammerson, G., Hammond, P.S., Happold, D., Happold, M., Hare, J., Harris, R.B., Hawkins, C.E., Haywood, M., Heaney, L., Hedges, S., Helgen, K.M., Hilton-Taylor, C., Hussain, S.A., Ishii, N., Jefferson, T.A., Jenkins, R.K.B., Johnston, C.H., Keith, M., Kingdon, J., Knox, D., Kovacs, K.M., Langhammer, P., Leus, K., Lewison, R., Lichtenstein, G., Lowry, L.F., Macavoy, Z., Mace, G., Mallon, D.P., Masi, M., McKnight, M.W., Medellín, R., Medici, P., Mills, G., Moehlman, P.D., Molur, S., Mora, A., Nowell, K., Oates, J.F., Olech, W., Oliver, W.R.L., Oprea, M., Patterson, B., Perrin, W.F., Polidoro, B.A., Pollock, C., Powel, A., Protas, Y., Racey, P., Ragle, J., Ramani, P., Rathbun, G., Reeves, R.R., Reilly, S.B., Reynolds III, J.E., Rondinini, C., Rulli, M., Rylands, A.B., Savini, S., Schank, C.J., Sechrest, W., Self-Sullivan, C., Shoemaker, A., SilleroZubiri, C., De Silva, N., Smith, D.E., Srinivasulu, C., Stephenson, P.J., van Strien, N., Talukdar, B.K., Taylor, B.L., Timmins, R., Tirira, D.G., Tognelli, M.F., Tsytsulina, K., Veiga, L.M., Viel, J.-C., Williamson, L., Wyatt, S.A., Xie, Y., and Young, B.E. (2008). The biogeography of diversity, threat, and knowledge in the world’s terrestrial and aquatic mammals. Science 322, 225–230. Wynen, L., Goldsworthy, S.D., Insley, S.J., Adams, M., Bickham, J.W., Francis, J., Gallo, J.P., Hoelzel, A.R., Majluf, P., White, R.W.G., and Slade, R. (2001). Phylogenetic relationships within the eared seals (Otariidae: Carnivora): implications for the historical biogeography of the family. Mol. Phylogenet. Evol. 21, 270–284.
EARLESS SEALS Phocidae Mike O. Hammill
The Phocidae can be divided into two subfamilies—the Monachinae, consisting of the southern phocids, the southern (Mirounga leonine) and northern elephant seals (M. angustirostris) and the monk seals and the Phocinae, or northern seals (Table 1). The separation between these two groups has been confirmed, but some discussions about the relationships among members within the subfamilies continue. Taxonomically, the gray seal (Halichoerus grypus) remains problematic. There are indications that gray seals are a sister species of the Caspian seal (Pusa caspica), and it clusters within the genus Phoca, but for some reason Halichoerus has retained its distinct generic status (Nyakatura and Bininda-Emonds, 2012). The resolution to this problem depends to some degree on whether Phoca should remain as a single genus, as four separate genera or some intermediate solution (see Nyakatura and BinindaEmonds, 2012).
II. Distribution Phocids are found throughout all of the world’s major oceans except for the Indian Ocean. Twelve species breed on ice, five species breed on land. Uniquely, the gray seal breeds on both land and on land-fast ice as well as pack ice (Fig. 1). Among the ice-breeding seals, eight species breed primarily on the pack ice; four breed primarily on land-fast ice. Phocids in the Northern Hemisphere have also colonized freshwater areas; these include the harbor seal (Phoca vitulina mellonae) in freshwater lakes of northern Quebec; the ringed seal (P. hispida ladogensis and P. h. saimensis) in Lakes Lagoda and Saimaa in Russia and Finland, respectively; and the Baikal seal (P. sibirica) in Lake Baikal in Siberia. Climate change will reduce ice cover in polar and temperate regions, which in turn will affect the current distribution of some species and perhaps even the survival of some (e.g., Hammill et al., 2015). Many species that are currently ice-breeders may not be able to transition to becoming land-breeders; therefore, they will follow the ice-retreat toward polar regions, but this will expose them to increased risk of predation from polar bears (especially the pups). Species breeding in restricted areas such as harp seals in the Gulf of St Lawrence (Canada) or ringed and gray seals in the Baltic Sea are likely to lose their breeding habitats entirely. The retreat of ice may also reduce foraging opportunities (e.g., see chapter Ringed Seal). However, not all species will be negatively impacted by the loss of ice. Gray seals breed both on land and on ice in the Baltic Sea and in the Gulf of St Lawrence Canada. As the ice retreats, access to new terrestrial locations, which can be colonized might be enhanced, but their suitability will depend on other factors such as levels of disturbance and exposure to predators.
I. Systematics
III. Ecology
The family Phocidae, consists of the earless or “true” seals. They are distinguished from sea lions and fur seals (family Otariidae), by the absence of external visible ear pinnae, internal testes, generally larger size, and the inability to draw their hind limbs forward under their body when on land (King, 1983). This latter characteristic, the absence of tusks, and a notched tongue also distinguish them from the family Odobenidae (walruses). Pinnipeds are considered to be monophyletic in origin descending from an arctoid carnivore. There remains some discussion on whether the monophyletic origin has affinity with bears (Ursidae) or to the weasel, otter, raccoon group (Musteloidea) (Sato et al., 2006), but recent evidence argues for greater affinity between the Pinnipedia and Mustelidae, which in turn share affinity with bears in the suborder Arctoidea (Sato et al., 2006; Nyakatura and Bininda-Emonds, 2012).
Pinnipeds are adapted to marine foraging but must haul out on land or ice for parturition and successful rearing of offspring. Marine adaptations in phocid seals include a thick blubber layer for insulation, modifications in limbs and body shape to improve hydrodynamics and agility, and anatomical and physiological changes to improve diving performance. Pinnipeds, unlike cetaceans, have not developed a biosonar system. Instead, they rely on visual and tactile means to locate prey. In the wild, blind well-nourished phocids have been observed meaning that these animals probably rely on their vibrissae to detect and capture prey. Using their heavily innervated vibrissae, phocid seals are capable of detecting very small changes in water velocity, which enables them to detect the wake of a swimming fish (Denhardt et al., 1998). However, phocids are thought to use vision as the
E EARED SEALS Otariidae B. Louise Chilvers The pinniped family Otariidae or the eared seals (sea lions and fur seals) is composed of seven extant genera with 16 species (Table 1). The word “otariid” comes from the Greek word otarion meaning “little ear,” referring to the small but visible external ear flaps (pinnae), which distinguish Otariidae from other pinnipeds. Otariids are distributed predominately in the southern hemisphere, with only three species in the North Pacific. The family is traditionally divided into two subfamilies, Otariinae (sea lions; 5 genera with 6 extant species, 1 extinct) and Arctocephalinae (fur seals; 2 genera with 10 species).
I. Classification Otariids are thought to have evolved in the Miocene (15–17 million years ago) in the North Pacific. Fossil records and genetics indicate that the family diversifying rapidly while spreading into the southern hemisphere, where all but three of the extant species now live. Molecular phylogenetic studies support the hypothesis that the basal position, or oldest species, in this family is Callorhinus ursinus (the Northern fur seal; Fig. 1). Otariids are divided into two subfamilies, fur seals (Arctocephalinae) and sea lions (Otariinae), with the major distinctions between them being the larger size of sea lions and the presence of a thick underfur layer in fur seals. The sea lions are genetically well defined in five genera and six extant species and one extinct species (Table 1). However, there is still debate regarding the taxonomic structure of the fur seals (Wynen et al., 2001; Berta and Churchill, 2012). Herein, the IUCN taxonomic classification of fur seals is followed, in which fur seals are classified into two genera: Callorhinus in the North Pacific with a single species representative, the Northern fur seal, and nine species in the southern hemisphere within the genus Arctocephalus (Table 1). The close relationship between sea lions and fur seals is indicated by intergenetic hybrids. At Macquarie Island, Australia’s subantarctic, New Zealand fur seal males mate with Antarctic fur seal females, Arctocephalus gazella and subantarctic, A. tropicalis female fur seals and produce hybrid pups (Lancaster et al., 2006). In the North Pacific, Californian sea lions are known to interbreed with both Steller sea lions and northern fur seals.
II. Morphology and Physiology The most distinctive feature that distinguishes otariids from phocids is their external ears. Along with the external ear pinnae, they have an air-filled external auditory canal and middle ear structure more similar to terrestrial mammals’ ears than other marine mammals. Otariids have semiaquatic lifestyles, feeding and migrating in the sea, but breeding and resting on land. They have much Encyclopedia of Marine Mammals. © 2018 Elsevier Inc. All rights reserved.
larger fore flippers and pectoral muscles than phocids, relatively speaking, and they have the ability to turn their hind limbs forward and walk on all fours, making them far more maneuverable on land. These larger fore flippers and pectoral muscles are also the mechanism by which otariids propel themselves in the water, rather than the hind-flipper-driven swimming typical of phocids. This swimming style means they can attain higher bursts of speed and have greater maneuverability in the water than phocids. Otariids also have more dog-like shaped heads with sharp, well-developed canines relative to phocids. There are distinct morphological and behavioral differences between fur seals and sea lions. Compared to sea lions, fur seals have a thick underfur used for insulation as well as the coarse guard hairs found on sea lions, are generally smaller, eat smaller prey, and go on longer foraging trips. Male otariids range in size from the 70 kg (150 lb) Galapagos fur seal to over 1000 kg (2200 lb) for the Steller sea lion. Similarly, female otariids range from 25 kg (60 lb) for the Galapagos fur seal to 270 kg (600 lb) for the Steller sea lion. Mature male otariids weigh two to six times as much as females, with proportionately larger heads, necks, and chests, and males in most species have predominant manes, which are not found among phocids.
III. Distribution and Habitat All otariids breed between 60°S and 55°N latitude. Most of the species (four sea lion and six fur seal species) breed in temperate latitudes, two species, the Galapagos sea lion and fur seal, breed on the equatorial Galapagos Islands, and the remaining four species breed in high temperate or subpolar regions (Table 1; Schipper et al., 2008). Northern fur seals, Californian and Steller sea lions are the only species that still breed in their ancestral range within the North Pacific. The two northern sea lion species are also the only two sea lion species that have overlapping ranges, while all other sea lions are allopatric to the countries and areas they are named after. The South American sea lion and fur seal, and Antarctic fur seal are the only species that breed in the Southern Atlantic Ocean. There are no otariids in the North Atlantic. The extent to which the modern distribution of otariids is a reflection of their decimation during 19th-century sealing, which led to the near extinction of most species, is unknown. Breeding occurs on both mainland and island sites within their ranges but due to past and present human pressures, island sites predominant worldwide, with four species restricted to island group distributions (i.e., Galapagos sea lion and fur seal, Juan Fernandez fur seal, and the New Zealand sea lion). Otariids’ preferred breeding substrate is rock or sand, although species like the New Zealand sea lions are known to travel up to 1.5 km inland and up to 400 m above sea level when breeding; some occupy forest areas. Knowledge of the at-sea distributions of otariids is predominately based on data from foraging lactating females, which are known to be restricted in their foraging range due to the need to
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TABLE 1 Distribution, Abundance, and Conservation Status (IUCN Red List Classification and Trend) of Otariids
E
Common Name
Scientific Name
Location
Population Estimatesa
IUCN Threat Status and Trenda
Steller sea lion California sea lion Galapagos sea lion Australian sea lion New Zealand sea lion South American sea lion Northern fur seal Galapagos fur seal South American fur seal New Zealand fur seal Antarctic fur seal Juan Fernandez fur seal Cape fur seal Australian fur seal Guadalupe fur seal Subantarctic fur seal
Eumetopias jubatus Zalophus californianus Z. wollebaeki Neophoca cinerea Phocarctos hookeri Otaria byronia Callorhinus ursinus Arctocephalus galapagoensis A. australis A. forsteri A. gazella A. phillippii A. pusillus pusillus A. p. doriferus A. townsendi A. tropicalis
High north temperate North temperate Equatorial South temperate South temperate South temperate Subpolar (Arctic) Equatorial South temperate South temperate Subpolar (Antarctic) North temperate South temperate South temperate North temperate High south temperate
140,000 380,000 15,000 12,700 11,700 250,000+ 1,290,000 15,000 300,000+ 200,000+ 6,000,000+ 32,000 2,000,000 12,000 20,000 400,000
Near threatened—increasing Least concern—increasing Endangered—decreasing Endangered—decreasing Endangered—decreasing Least concern—stable Vulnerable—decreasing Endangered—decreasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—increasing Least concern—stable
a
IUCN Red List (www.iucnredlist.org).
at sea). All male otariids are known to move away or “migrate” from breeding areas outside the breeding seasons; however, these migrations may still be within island groups for Galapagos species, while others can cover 100 s or even 1000 s of kilometers.
IV. Behavior and Ecology
Figure 1 The northern fur seal, Callorhinus ursinus, is thought to be the oldest species in the Otariidea family (Photo by Brian Fadely-NOAA Fisheries, Permit No. 14327). return to dependent pups on land. In general, otariids at sea ranges occur predominately over and on the edges of the continental shelves or in trenches and upwellings close to their breeding colonies. Overall, fur seal species usually have significantly longer foraging trips (250 km from colony) and spend more days at sea (average 5–9 days depending on age of pup) than sea lion species (average 30–100 km from colony depending on species and 1–3 days
Otariids are colonial, highly synchronized annual breeders, aggregating on traditional breeding beaches or rocky areas, with the exception of the Australian sea lion, which breeds year-round. Most otariid females are highly philopatric to the breeding area where they were born, with some species known to be philopatric to areas within 100 m of their birth place. All species are polygynous with territorial males breeding with more than one female. There is high variability to the extent to which males control females within the breeding areas between species. For the majority of otariids, males arrive first at breeding areas and establish and hold territories. Females typically arrive ashore 1 or 2 days before giving birth and are usually in estrous within 5–10 days after giving birth. After birth, females cycle time at sea foraging and time on shore with their pups. Most otariid colonies have highly synchronized birth pulses, with the majority of births occurring in a 2–3 week period. All otariids have a period of embryonic diapause (delayed implantation) of 3–4 months following fertilization with gestation believed to be 8–9 months, allowing for pup births and mating to occur in a 12-month cycle (Gentry and Kooyman, 1986). The exception to this rule is the Australian sea lion (Fig. 2) which has a 17.5 month breeding cycle with the gestation period extended to up to 14 months, although the pups when born are no more developed than other otariid pups. Female Australian sea lions are highly philopatric, with colonies <100 km apart breeding 5–6 months apart due to the high philopatry of the resident females. For most otariid species, females reach sexual maturity at 3 years of age and breed for the first time between 3 and 5 years of age. Males typically mature at 5–7 years of age, and breed even later
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E Figure 2 The Australian sea lion, Neophoca cinerea, has an atypical 17.5 month, nonsuccinct breeding cycle, thought to have arisen due to the highly variable environment in which this species evolved (Photo by Mark Hindell). due to the need to be socially mature, that is, large and dominant enough to hold breeding territories. Males typically only live to be teenagers, while females are known to live and breed well into their late 20s. Females only have one pup per breeding episode, and often have gaps between pups. Pup survival in the first year is highly variable (from 0 to 90+% survival) for otariids depending on species, climate affects (El Niño events), disease events, and maternal investment levels, meaning the life time pup production for a female otariid can range from 0 to 10 pups. Otariids are visual, generalist foragers that feed on fish, squid, and crustaceans (including krill). Some male otariids are also known to feed on sea birds and fur seal pups. Sea lions tend to feed close to shore over continental shelves, targeting larger fish, octopus, and squid, while the smaller fur seals tend to take longer, offshore foraging trips during which they feed on larger numbers of smaller prey items including krill. These foraging patterns strongly reflect the central-place foraging patterns of female otariids that combine land-breeding and rearing of pups with marine foraging.
V. Interactions With Humans Contact with humans leads to the extinction of the Japanese sea lion (Zalophus japonicas) and the near extinction of many other otariids, due to excessive harvesting. Their colonial, terrestrial breeding, at predicable locations, made them highly vulnerable to overexploitation. The fur seal and sea lion species that survived historical sealing did so only in dramatically reduced numbers in highly restricted locations. For example, the Antarctic fur seal (now the most abundant otariid; Table 1) was thought to be extinct from overharvesting; however, a few small populations were found on isolated islands (Wynen et al., 2001). Harvesting of otariids is now limited to subsistence harvest from first nations in the North Pacific (predominately of Northern fur seals) and commercial harvests of Cape fur seals in Namibia (Cumming, 2015). Most species are still recovering, dispersing into their former ranges, and increasing in numbers. Some species still have highly restricted ranges such as the Australian and New Zealand sea lions (Table 1). Currently, the greatest threat to otariids arises from direct and indirect fisheries interactions. Across all pinnipeds, one in three species is classified as threatened compared to one of five mammals generally and this is mainly due to fisheries interactions (Kovacs
Figure 3 Marine debris entanglement and digestion is an increasing problem for otariids (Photo by B. Louise Chilvers).
et al., 2012). Incidental mortality in fishing operations, commonly referred to as bycatch, is an acute threat for Australian and New Zealand sea lions and a possible factor in the complex assemblage of reasons for the decline of the Steller sea lion (Read, 2008). Indirect fisheries interactions including intentional shooting of pinnipeds by fishermen, competition for fish resources, and fisheries-induced changes to ecosystems that change prey abundance and distribution can additionally impact otariid populations. Marine debris entanglement and digestion is an increasing problem for individual animals; however, it is not known if or how these interactions affect populations (Fig. 3; Page et al., 2004). In the near future, global climate change is likely to be a factor influencing otariids abundance and distribution, however, to a lesser extent than for ice breeding phocid species (Kovacs et al., 2012). Expected changes in ocean currents due to global warming are likely to alter prey abundance and distribution, with the highest impacts expected to be experienced by South Pacific otariids, given the significant role of El Niño events in the Southern Oscillation (Nicholls, 2008).
References Berta, A., and Churchill, M. (2012). Pinniped taxonomy: Review of currently recognized species and subspecies, and evidence used for their description. Mamm. Rev. 42, 207–234. Cumming, D.H.M. (2015). Seal Range State Policy and Management Review. IUCN SSC/CEESP Sustainable Use and Livelihoods Specialist Group, Gland, Switzerland. Gentry, R.L., and Kooyman, G.L. (1986). “Fur Seals: Maternal Strategies on Land and at Sea.” Princeton University Press. Kovacs, K.M., Aguilar, A., Aurioles, D., Burkanov, V., Campagna, C., Gales, N., Gelatt, T., Goldsworthy, S.D., Goodman, S.J., Hofmeyr, G.J.G., Härkönen, T., Lowry, L., Lydersen, C., Schipper, J., Sipilä, T., Southwell, C., Stuart, S., Thompson, D., and Trillmich, F. (2012). Global threats to pinnipeds. Mar. Mamm. Sci. 28, 414–436. Lancaster, M.L., Gemmell, N.J., Negro, S., Goldsworthy, S., and Sunnucks, P. (2006). Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Mol. Ecol. 15, 3681–3692. Nicholls, N. (2008). Recent trends in the seasonal and temporal behaviour of the El Nino-Southern Oscillation. Geophys. Res. Lett. 35, L29703.
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Page, B., McKenzie, J., McIntosh, R., Baylis, A., Morrissey, A., Calvert, N., Haase, T., Berris, M., Dowie, D., Shaughnessy, P.D., and Goldsworthy, S.D. (2004). Entanglement of Australian sea lions and New Zealand fur seals in lost fishing gear and other marine debris before and after Government and industry attempts to reduce the problem. Mar. Pollut. Bull. 49, 33–42. Read, A.J. (2008). The looming crisis: interactions between marine mammals and fisheries. J. Mamm. 89, 541–548. Schipper, J., Chanson, J., Chiozza, F., Cox, N., Hoffmann, M., Katariya, V., Lamoreux, J., Rodrigues, A., Stuart, S.N., Temple, H.J., Baillie, J., Boitani, L., Lacher, T.E., Mittermeier, R.A., Smith, A.T., Absolon, D., Aguiar, J.M., Amori, G., Bakkour, N., Baldi, R., Berridge, R.J., Bielby, J., Black, P.A., Blanc, J.J., Brooks, T.M., Burton, J.A., Butynski, T.M., Catullo, G., Chapman, R., Cokeliss, Z., Collen, B., Conroy, J., Cooke, J.G., da Fonseca, G.A.B., Derocher, A.E., Dublin, H., Duckworth, J.W., Emmons, L., Emslie, R.H., Festa-Bianchet, M., Foster, M., Foster, S., Garshelis, D.L., Gates, C., Gimenez-Dixon, M., Gonzalez, S., Gonzalez-Maya, J.F., Good, T.C., Hammerson, G., Hammond, P.S., Happold, D., Happold, M., Hare, J., Harris, R.B., Hawkins, C.E., Haywood, M., Heaney, L., Hedges, S., Helgen, K.M., Hilton-Taylor, C., Hussain, S.A., Ishii, N., Jefferson, T.A., Jenkins, R.K.B., Johnston, C.H., Keith, M., Kingdon, J., Knox, D., Kovacs, K.M., Langhammer, P., Leus, K., Lewison, R., Lichtenstein, G., Lowry, L.F., Macavoy, Z., Mace, G., Mallon, D.P., Masi, M., McKnight, M.W., Medellín, R., Medici, P., Mills, G., Moehlman, P.D., Molur, S., Mora, A., Nowell, K., Oates, J.F., Olech, W., Oliver, W.R.L., Oprea, M., Patterson, B., Perrin, W.F., Polidoro, B.A., Pollock, C., Powel, A., Protas, Y., Racey, P., Ragle, J., Ramani, P., Rathbun, G., Reeves, R.R., Reilly, S.B., Reynolds III, J.E., Rondinini, C., Rulli, M., Rylands, A.B., Savini, S., Schank, C.J., Sechrest, W., Self-Sullivan, C., Shoemaker, A., SilleroZubiri, C., De Silva, N., Smith, D.E., Srinivasulu, C., Stephenson, P.J., van Strien, N., Talukdar, B.K., Taylor, B.L., Timmins, R., Tirira, D.G., Tognelli, M.F., Tsytsulina, K., Veiga, L.M., Viel, J.-C., Williamson, L., Wyatt, S.A., Xie, Y., and Young, B.E. (2008). The biogeography of diversity, threat, and knowledge in the world’s terrestrial and aquatic mammals. Science 322, 225–230. Wynen, L., Goldsworthy, S.D., Insley, S.J., Adams, M., Bickham, J.W., Francis, J., Gallo, J.P., Hoelzel, A.R., Majluf, P., White, R.W.G., and Slade, R. (2001). Phylogenetic relationships within the eared seals (Otariidae: Carnivora): implications for the historical biogeography of the family. Mol. Phylogenet. Evol. 21, 270–284.
EARLESS SEALS Phocidae Mike O. Hammill
The Phocidae can be divided into two subfamilies—the Monachinae, consisting of the southern phocids, the southern (Mirounga leonine) and northern elephant seals (M. angustirostris) and the monk seals and the Phocinae, or northern seals (Table 1). The separation between these two groups has been confirmed, but some discussions about the relationships among members within the subfamilies continue. Taxonomically, the gray seal (Halichoerus grypus) remains problematic. There are indications that gray seals are a sister species of the Caspian seal (Pusa caspica), and it clusters within the genus Phoca, but for some reason Halichoerus has retained its distinct generic status (Nyakatura and Bininda-Emonds, 2012). The resolution to this problem depends to some degree on whether Phoca should remain as a single genus, as four separate genera or some intermediate solution (see Nyakatura and BinindaEmonds, 2012).
II. Distribution Phocids are found throughout all of the world’s major oceans except for the Indian Ocean. Twelve species breed on ice, five species breed on land. Uniquely, the gray seal breeds on both land and on land-fast ice as well as pack ice (Fig. 1). Among the ice-breeding seals, eight species breed primarily on the pack ice; four breed primarily on land-fast ice. Phocids in the Northern Hemisphere have also colonized freshwater areas; these include the harbor seal (Phoca vitulina mellonae) in freshwater lakes of northern Quebec; the ringed seal (P. hispida ladogensis and P. h. saimensis) in Lakes Lagoda and Saimaa in Russia and Finland, respectively; and the Baikal seal (P. sibirica) in Lake Baikal in Siberia. Climate change will reduce ice cover in polar and temperate regions, which in turn will affect the current distribution of some species and perhaps even the survival of some (e.g., Hammill et al., 2015). Many species that are currently ice-breeders may not be able to transition to becoming land-breeders; therefore, they will follow the ice-retreat toward polar regions, but this will expose them to increased risk of predation from polar bears (especially the pups). Species breeding in restricted areas such as harp seals in the Gulf of St Lawrence (Canada) or ringed and gray seals in the Baltic Sea are likely to lose their breeding habitats entirely. The retreat of ice may also reduce foraging opportunities (e.g., see chapter Ringed Seal). However, not all species will be negatively impacted by the loss of ice. Gray seals breed both on land and on ice in the Baltic Sea and in the Gulf of St Lawrence Canada. As the ice retreats, access to new terrestrial locations, which can be colonized might be enhanced, but their suitability will depend on other factors such as levels of disturbance and exposure to predators.
I. Systematics
III. Ecology
The family Phocidae, consists of the earless or “true” seals. They are distinguished from sea lions and fur seals (family Otariidae), by the absence of external visible ear pinnae, internal testes, generally larger size, and the inability to draw their hind limbs forward under their body when on land (King, 1983). This latter characteristic, the absence of tusks, and a notched tongue also distinguish them from the family Odobenidae (walruses). Pinnipeds are considered to be monophyletic in origin descending from an arctoid carnivore. There remains some discussion on whether the monophyletic origin has affinity with bears (Ursidae) or to the weasel, otter, raccoon group (Musteloidea) (Sato et al., 2006), but recent evidence argues for greater affinity between the Pinnipedia and Mustelidae, which in turn share affinity with bears in the suborder Arctoidea (Sato et al., 2006; Nyakatura and Bininda-Emonds, 2012).
Pinnipeds are adapted to marine foraging but must haul out on land or ice for parturition and successful rearing of offspring. Marine adaptations in phocid seals include a thick blubber layer for insulation, modifications in limbs and body shape to improve hydrodynamics and agility, and anatomical and physiological changes to improve diving performance. Pinnipeds, unlike cetaceans, have not developed a biosonar system. Instead, they rely on visual and tactile means to locate prey. In the wild, blind well-nourished phocids have been observed meaning that these animals probably rely on their vibrissae to detect and capture prey. Using their heavily innervated vibrissae, phocid seals are capable of detecting very small changes in water velocity, which enables them to detect the wake of a swimming fish (Denhardt et al., 1998). However, phocids are thought to use vision as the