Ecology is the study of the interactions between individuals

Transcription

1 852 inniped Ecology Iceland, Orkney Islands (Scotland), Hebrides Islands (Scotland), Greenland, and the Faeroe Islands. The intensive drive fishery in Newfoundland ( ) is estimated to have taken 54,000 animals and to have reduced the local population substantially. The population may be recovering, but more information is needed. Fisheries for short-finned pilot whales have operated in the Caribbean, Indonesia, and in Japan. The drive fisheries in the Faeroe Islands and in Japan continue today. These fisheries have been in existence for several hundred years. In 2006, the catch of long-finned pilot whales in the Faeroes was 856 animals; in 2004, Japan reported a catch of 63 shortfinned pilot whales. The Faeroe fishery is considered sustainable. The incidental bycatch of cetaceans in fisheries is a worldwide phenomenon. Most bycatch goes unreported because this information is not recorded in many countries. ilot whales are particularly susceptible to entanglement in driftnets. The effect of such mortality on pilot whale populations is unknown. Bycatch records are kept in the United States. In northeast US waters, pilot whales have been taken incidentally in a variety of fisheries including pelagic drift gill nets, pelagic long lines, pelagic pair trawls, and trawls for mackerel, herring, and squid. Most takes occurred along the shelf break. Some of these fisheries are now closed. None of the current fisheries exceed the allowable annual take for pilot whales under US law. ilot whales off California are taken incidental to driftnet fisheries targeting swordfish and sharks. A take reduction plan was implemented in 1997 and currently the incidental take is lower than the allowable annual limit. rior to the El Ni ño of , pilot whales were taken incidentally in the Californian squid purse-seine fishery. ilot whale redistribution in response to El Ni ñ o is the likely reason no mortality was reported for this fishery during the following years. Currently the squid fishery is not monitored, but there have been anecdotal reports of pilot whales seen near squid fishing operations in recent years. Driftnet fisheries similar to those in California operate out of Mexico; any pilot whale takes there are likely from the same population of short-finned pilot whales that occurs off California. A minimal number of pilot whales have been reported taken incidental to the long-line fisheries based in Hawaii. The mortality and injury sustained by pilot whales interacting with the fishery occurred outside the 200 nmi Exclusive Economic Zone (EEZ) of Hawaii. Less is known about pilot whale populations away from the nearshore areas of Hawaii, so the impact of the takes on these whales is also not known. Long-finned pilot whales from both sides of the north Atlantic carry high levels of organochlorine contaminants (pesticides such as DDT and CB) in their tissues. Concentrated organochlorines may impair reproduction or increase susceptibility to disease. Studies are continuing on the effects these compounds have on marine mammals. Accumulations of cadmium and mercury are also present in the tissues of long-finned pilot whales from the Faeroe Islands. As top predators, pilot whales are a repository of these heavy metals accumulating through the marine food chain. ilot whales seem unusually tolerant to elevated levels of these metals, as studies have not yet revealed a major toxicity problem in these species. See Also the Following Articles See Delphinids, Overview Hunting of Marine Mammals References Amos, B., Schlotterer, C., and Tauz, D. (1993 ). Social structure of pilot whales revealed by analytical DNA profiling. Science 260, Bernard, H. J., and Reilly, S. B. ( 1999 ). ilot whales. In Handbook of Marine Mammals ( S. H. Ridgway, and R. Harrison, eds ), Vol. 6, pp Academic ress, London. Donovan, G.., Lockyer, C. H., and Martin, A. R. (eds.). (1993). Biology of Northern Hemisphere pilot whales. Rep. Int. Whal. Comm. 14 (Special Issue). Duignan,., et al. (1995 ). Morbillivirus infection in two species of pilot whales ( Globicephala sp.) from the western Atlantic. Mar. Mamm. Sci. 11, Fullard, K. J., Early, G., Heide-Jørgensen, M.., Bloch, D., Rosing- Asvid, A., and Amos, W. ( 2000 ). opulation structure of long-finned pilot whales in the North Atlantic: a correlation with sea surface temperature? Mol. Ecol. 9, Nawojchik, R., St. Aubin, D. J., and Johnson, A. (2003 ). Movements and dive behavior of two stranded, rehabilitated long-finned pilot whales (Globicephala melas ) in the northwest Atlantic. Mar. Mamm. Sci. 19, Ottensmeyer, C. A., and Whitehead, H. ( 2003 ). Behavioural evidence for social units in long-finned pilot whales. Can. J. Zool. 81, Rendell, L. E., Matthews, J. N., Gill, A., Gordon, J. C. D., and Macdonald, D. W. (1999 ). Quantitative analysis of tonal calls from five ondontocete species, examining interspecific and specific variation. J. Zool. Lond. 249, Reynolds, J. E., and Rommel, S. A. (eds) (1999 ). Biology of Marine Mammals. Smithsonian Institution ress, Washington, DC. inniped Ecology W.D. BOWEN, C.A. BECK, AND D.A. AUSTIN Ecology is the study of the interactions between individuals and their environment. In this context, environment is taken broadly to include other organisms and the physical characteristics of habitat. These interactions take place at various spatial and temporal scales, and influence both the abundance and distribution of individuals. However, ecology is also a historical science in that the patterns we see today reflect past events and phylogenetic relationships. Thus, processes acting on both evolutionary and ecological time-scales have undoubtedly influenced many of the characteristics of pinniped ecology we see today. innipeds are large, long-lived, aquatic mammals exhibiting delayed sexual maturity and reduced litter size; a single precocial offspring is the norm. As such, they share many of the demographic features of other large mammals. opulation numbers do not change dramatically from year to year, and numbers are most sensitive to changes in adult survival, followed by juvenile survival and fecundity ( Eberhardt and Siniff, 1977 ). We assume that these characteristics are under selection and that variability in foraging success affects survival probability and reproductive performance of individuals. Inevitably, discussions of pinniped ecology and other aspects of pinniped biology will overlap. Here we focus on five aspects of pinniped ecology: abundance, distribution, reproduction, foraging, and the ecological roles of pinnipeds in aquatic ecosystems. I. Abundance Despite the interest in the ecology of pinnipeds, the abundance of many species is poorly known. The abundance of commercially harvested species (e.g., past-northern fur seals [ Callorhinus ursinus ]

2 inniped Ecology 853 or present-harp seals [ agophilus groenlandicus ]) is generally better known than for those species that have not been exploited. The accuracy and precision attached to the estimates of abundance varies greatly, owing to the difficulty in carrying out surveys or to the lack of effort to obtain good estimates. Good estimates of abundance are important because abundance and trends in abundance are perhaps the most useful indicators of population status. Commercial exploitation decimated many pinniped species, in some cases to levels nearing extinction (e.g., northern elephant seals [Mirounga angustirostris ]). Over the past several decades or more, some species have recovered or are continuing to recover. Thus, the present abundance of heavily exploited species may not be a good measure of their preexploitation numbers. inniped species range over four orders of magnitude in abundance, from the crabeater seals (Lobodon carcinophaga ) at about 12 million (probably the most abundant marine mammal in the world) to the Mediterranean monk seal (Monachus monachus ) at probably fewer than several hundred individuals ( Reijnders et al., 1993 ). hocid species are generally more abundant than otariids, with 15 of 18 phocid species numbering greater than 100,000 individuals compared with only 8 of 14 otariid species ( Bowen and Siniff, 1999 ). The reasons for this difference are not entirely clear. Over the past 100 years, both families have been commercially exploited and subjected to other human factors that might have influenced abundance. More likely, the greater abundance of phocids is the result of their greater use of high-productivity areas in temperate and polar waters than is the case in most otariid species. The three most abundant otariids, the northern fur seal, Antarctic fur seal ( Arctocephalus gazella ), and South African fur seal ( A. pusillus pusillus ), all forage in seasonally productive, high-latitude ecosystems, a characteristic shared with the most abundant phocid species (i.e., the ringed seal [ usa hispida ], the harp seal, and the crabeater seal). Abundance is determined by the movement of individuals in and out of the population, and by births and deaths. These processes are influenced by ecological factors such as predation, food supply, breeding habitat, disease, competition with other species, and environmental variability, and by both direct and indirect human activities. In the absence of human effects, combinations of these ecological factors determine abundance and some of which, operating in a density-dependent way, will regulate population size about a level known as carrying capacity. With the recovery of populations from earlier periods of exploitation, there is increasing evidence that a number of species have reached or are approaching the current carrying capacity of their environments (e.g., Weddell seal [ Leptonychotes weddellii ], gray seals [ Halichoerus grypus ], harbor seals [ hoca vitulina ], harp seals). During periods of recovery, species such as Antarctic fur seal, Northern fur seal, gray seal, and harbor seal increased at rates in excess of 12% per year over several decades or more. At Sable Island, Canada, the number of gray seal pups born each year has increased exponentially, with a doubling time of about 6 years, for more than 40 years. Although they can increase rapidly, pinniped populations may decline even more rapidly as a result of epizootics, such as the phocine distemper virus that killed large numbers of harbor seals in the North Sea, and during short-term extreme changes in ocean climate, such as El Ni ñ o (see below). II. Distribution Fundamentally, pinniped distributions reflect the need to give birth on solid substrate of land or ice, and to feed at sea. Within these broad constraints, the distribution of pinnipeds is affected by physical (e.g., ice cover, location of remote islands) and biological (e.g., productivity, abundance of predators) characteristics of habitat, demographic factors (e.g., population size, age, sex, and reproductive status), morphological and physiological constraints and human actions (e.g., disturbance). Although each of these factors may influence distribution, combinations of factors are generally responsible for the distribution patterns we observe. inniped distribution is also three-dimensional, where the third dimension is water depth and the underlying bathymetry. Although a complete understanding of pinniped distribution must consider this three-dimensional world, this aspect of pinniped behavior is discussed in sections on Energetics, Telemetry, and Diving Behavior. inniped species have a restricted and generally patchy distribution in most aquatic environments: estuaries and continental shelves (e.g., gray seals), tropical seas (e.g., monk seals [ Monachus spp.], Galapagos fur seals [ Arctocephalus galapagoensis ]), the deep ocean (e.g., elephant seals [ Mirounga spp.]), Arctic (e.g., ringed seals) and Antarctic polar seas (e.g., crabeater seals, Antarctic fur seals), and freshwater lakes (e.g., Baikal seals [ usa sibirica ]) (King, 1983 ). However, our understanding of the distribution of most species is based primarily on the location of breeding colonies. We know considerably less about where most species forage at sea, and our view of overall distribution is therefore incomplete. For example, based on the location of breeding colonies, northern elephant seals range from Baja California to central California. However, satellite telemetry studies show that this species forages over broad areas of the North acific Ocean for much of the year. This new information has dramatically changed our understanding of the ecology of this and a growing number of species (e.g., gray seal, harbor seals, and southern elephant seals [ Mirounga leonina ]). The distributions of pinniped breeding colonies seem to reflect the evolutionary history of pinnipeds and the distribution of resources. At large scales, both sea lion and fur seal distributions reflect their origins in the acific Ocean. Northern fur seals and Steller sea lions (Eumetopias jubatus ) are widely distributed along both sides of the North acific Ocean. The four other species of sea lions occupy colonies along the west coast of South America, southern Australia, and New Zealand. With the exception of the northern fur seal and Guadalupe fur seal, the other six species of fur seals occur in tropical or subtropical southern waters, but also extend into the cool, nutrient-rich waters of the South Atlantic and Indian Oceans. Sea lion and fur seal breeding colonies are usually located on remote islands near areas of high biological productivity (e.g., northern fur seals, Antarctic fur seals), which provide both protection from mainland predators and nearby food sources. These conditions are particularly important for lactating females. Species of the Family hocidae are widely distributed in biologically productive temperate and polar seas. Although most abundant in the North Atlantic and Antarctic Oceans, a reflection of their evolutionary origins in the Atlantic basin during the middle Miocene, phocid species have circumpolar distributions in both the Arctic Ocean (e.g., ringed seal, bearded seal [ Erignathus barbatus ]) and Antarctic Ocean (e.g., Weddell seal, crabeater seal), as well as a broad distribution in the North acific Ocean (e.g., harbor seal, largha seal [ hoca largha ], ribbon seal [ Histriophoca fasciata ]). Several endangered species also occur in tropical waters (Hawaiian [Monachus schauinslandi ] and Mediterranean monk seals). innipeds must return to a solid substrate (land or ice) to give birth, rear their offspring, and in many species to molt. For most species, these requirements result in seasonal changes in distribution. In the case of species that breed on pack ice, such as harp and hooded (Cystophora cristata ) seals and the walrus ( Odobenus rosmarus ),

3 854 inniped Ecology seasonal changes in ice cover virtually guarantee changes in distribution. This may partly explain why 7 of 13 (54%) species of pinnipeds that give birth on ice (i.e., most phocid seals and the walrus) are migratory, compared to only 4 of 20 (20%) species that give birth on land (2 of 6 phocids, 2 of 14 otariids; Bowen and Siniff, 1999 ). However, this difference also may be partly explained by the variable quality of data on the at-sea distribution of pinnipeds. Migration appears to be a common feature of the ice-breeding phocid species, but this behavior is perhaps best documented in the northern elephant seal. This land-breeding species shows extreme sexual size-dimorphism, with males being about five times heavier than females. Northern elephant seals undertake the longest known migration and some of the deepest dives reported for a mammal (Stewart and DeLong, 1993). Individual elephant seals make two long-distance migrations of 18,000 21,000 km between breeding and molting sites in California and pelagic foraging areas in the North acific. Using the California Current as a corridor to areas further north, northern elephant seals leave the breeding beaches in southern California for northern offshore foraging areas. The first migration occurs following the breeding season, in which adult male and female elephant seals travel an average of 11,967 and 6289 km respectively, and remain at sea for an average of 124 and 73 days. After the molt, the seals depart on a second migration; females are at sea for approximately twice as long as males and cover an average distance of 12,264 km compared to an average of 9608 km by males. Males migrate farther north than females, with most males traveling as far as the northern Gulf of Alaska and the eastern Aleutian Islands. These sex differences in foraging distribution, and presumably diet, may have evolved to reduce competition between females and males. III. Reproductive Ecology The reproductive ecology of pinniped species share features that reflect their common ancestry as terrestrial carnivores, and their subsequent adaptation to a predominately aquatic lifestyle. As noted previously, a conserved trait of their terrestrial ancestry is the requirement for all pinniped species to give birth to their offspring on a solid substrate (land or ice). However, pinnipeds must feed at sea, often some distance from the breeding grounds. This spatial and temporal separation of parturition from aquatic foraging is thought to have played a large role in shaping the mating and lactation strategies of pinnipeds. Three general strategies have evolved to deal with the conflict between at-sea foraging and terrestrial parturition (see below); however, the requirement for terrestrial parturition has likely contributed to some common features of pinniped reproduction, such as birth synchrony. In most pinniped species, reproduction is seasonal and highly synchronous (e.g., harp seals). The evolution of reproductive synchrony is often associated with seasonal resource availability. In ice-breeding species (e.g., harp and hooded seals), the timing of reproduction is linked to the seasonal availability of sea ice. Seasonal changes in prey abundance and environmental conditions can also influence the timing of parturition and mating. The Hawaiian monk seal displays only weak synchrony in reproduction. In this species, births extend over a 6-month period. Given the less variable tropical habitat of this species, reproductive synchrony may not have been under strong selection relative to species in more variable temperate and polar environments. Subtropical populations of California sea lions ( Zalophus californianus californianus ) and Galapagos fur seals also show slightly less temporal synchrony of reproduction relative to more temperate populations ( Boness, 1991 ). Departures from the annual cycle of reproduction are found in several species. The Australian sea lion ( Neophoca cinerea ) has a cycle lasting 18 months, resulting in a seasonal pattern of births. Similarly, the walrus has a reproductive cycle of 2 years, including a 15-month gestation period, in which the period of births remains seasonal. Other common features of pinniped reproduction include postpartum mating and delayed implantation. These two characteristics of pinniped reproduction also appear to reflect the terrestrial ancestry of the taxa, with both features occurring in many modern terrestrial carnivores (see Female Reproductive Systems). However, selection for postpartum mating may have continued as pinnipeds adapted to their aquatic environment. Given the wide-ranging and dispersed distribution of pinniped species during the at-sea foraging season, the aggregation of individuals at pupping colonies may have offered one of the few predictable opportunities for males and females to mate. Another common feature of pinniped reproduction is the production of a single, precocious offspring; litters of two are rare. Offsprings are born with their eyes open and begin to vocalize within minutes of birth. Neonates are also able to move short distances to their mother and begin suckling shortly after birth. Harbor seal females produce extremely precocial offspring that are capable of swimming and diving with their mothers within an hour after birth (Bowen, 1991 ). A. Mating Systems Within the order innipedia, mating systems range from extreme polygyny (e.g., northern fur seals) to sequential defense by males of individual females. Mating systems are closely associated with the dimensionality and stability of the habitat used, and distribution of females at parturition. Broadly speaking, species can be grouped as land-breeding and aquatic-breeding species. 1. Land-Breeding Species Land-breeding pinniped species include all fur seals and sea lions, northern and southern elephant seals, and the gray seal. These species colonize oceanic islands and coastal areas to give birth and mate. The aggregation of individuals during the breeding season has been attributed to the fact that oceanic islands are relatively rare and unevenly dispersed, such that the availability of suitable pupping sites may limit the distribution of females ( Boness, 1991 ). redation may also select for female clustering, with females being less vulnerable to terrestrial predators and/or harassment by conspecific males when in large groups (dilution effect). Aggregation of females within a stable, two-dimensional habitat has led to the evolution of polygyny in these species, with males defending either resources needed by females (e.g., birth and thermoregulatory sites in otariid species) or the females themselves (e.g., elephant seals and gray seals). By competing with and limiting the access of other males to females, successful males mate with multiple females, thus increasing their reproductive success. The degree of polygyny in land-breeding pinniped species ranges from extreme in the northern fur seal and elephant seals where one male may mate with females, to moderate (6 15 females) in gray seals, Hooker sea lions (hocarctos hookeri ) and the Galapagos fur seal ( Le Boeuf, 1991 ). As in other polygynous species, land-breeding pinniped species are sexually size-dimorphic. Males in these species can be much larger than females and often show other secondary sex characteristics. These dimorphic characteristics are the result of sexual selection for traits that increase an individual s ability to monopolize and defend resources needed by females or females themselves. Large body size, and concomitant body energy stores in the form of subcutaneous blubber, permits dominant males to fast and thus remain ashore

4 inniped Ecology 855 during the period when females become receptive. The most extreme example of sexual size dimorphism in pinnipeds occurs in elephant seals, where males are 5 6 times heavier than females in the northern species and up to 10 times heavier than females in the southern species. 2. Aquatic-Breeding Species Walruses and all other phocid seals (Weddell, Ross [ Ommatophoca rossii ], crabeater, leopard ( Hydrurga leptonyx ), bearded, hooded, ringed, Baikal, Caspian ( usa caspica ), spotted, harp and ribbon) give birth on pack ice or fast ice and mate in the water. Although Hawaiian monk seals and harbor seals give birth to their offspring on land, they too mate in the water. In species where pups are born on ice, females tend to be more widely distributed, although access to breathing holes in the ice may promote clumping in some species (e.g., walrus and Weddell seals). This broader distribution of females, on an unstable habitat, limits the number of females a male can monopolize at any given time, and as a result these species typically show reduced levels of polygyny (e.g., harbor seals; Coltman et al., 1999 ). The fact that mating occurs in the water, a fluid three-dimensional environment, also may limit the ability of males to monopolize females resulting in reduced levels of polygyny. Wells et al. (1999) classified the mating strategies used by icebreeding species as: scrambling-males search for receptive females and move on to the next, sequential defense-males sequentially defend single females through mating, and lekking-males aggregate and attract females using displays. At present, there is insufficient information on the breeding behavior of most aquatic breeding species to draw firm conclusions about the type of mating system used. Until recently, data on the mating behavior of these species is limited to that which can be observed on ice prior to copulation. For example, observational data suggest that hooded seals use a sequential defense mating system whereby males compete with one another to defend a single female and her pup on the ice. The dominant male remains with the pair until the pup is weaned and then enters the water with the female, presumably to mate. However, the application of newer methods, including genetic paternity assessment, animalborne video, and positional analysis of vocalizations have clarified the mating systems of harbor seals ( Boness et al., 2006 ) and bearded seals ( Van arijs and Clark, 2006 ). In species that mate aquatically, there may be less selective advantage for males to be larger than females because of the limited ability of males to monopolize females in this environment. As a consequence, in most of these species, males and females are of similar size and in some cases females are larger than males. For example, male Weddell seals are slightly smaller than females and it has been suggested that smaller size makes the male more agile during underwater mating activities ( Le Boeuf, 1991 ). Underwater vocalizations also appear to be an important component of the mating behavior in aquatically mating pinniped species. For example, in acific walruses, which exhibit a lekking mating system, males perform complex underwater visual and vocal displays in small groups next to female haulout sites to attract females. Male Weddell, harbor, harp, hooded, and bearded seals also produce a range of underwater vocalizations during the breeding season that may be used to attract females or to establish underwater territories or display areas. B. Lactation Strategies Male pinnipeds do not participate in the care of the offspring. Thus, parental care is the exclusive responsibility of the female. Female care involves the transfer of energy-rich milk to the pup, and protection from conspecifics and terrestrial predators ( Bowen, 1991 ). In some species (e.g., the walrus), females may also teach their young to forage, as young accompany mothers on foraging trips during the lactation period. Female pinnipeds have dealt with the temporal and spatial separation of energy acquisition (aquatic foraging) from high levels of energy expenditure (terrestrial lactation) in different ways, resulting in the three basic lactation strategies: long lactation length and foraging cycle, short lactation length and fasting, and long lactation length and aquatic nursing. Although maternal body size has long been thought to have been an important trait in the evolution of these strategies, on the basis of a comparative analysis of 12 life-history and ecological traits,schulz and Bowen (2005) concluded that there is little evidence for the influence of body size on lactation length. The patterns we see today appear to reflect an early divergence in body size between otariids and phocids, which influenced their foraging strategies and metabolic rates and subsequently influenced lactation strategies. Abbreviated lactation seems to represent an adaptation for minimizing the relative milk energy expended over lactation, but may also have been selected to reduce terrestrial predation and the uncertainly of breeding on unpredictable pack ice. 1. Foraging Cycle All otariids and some of the smaller phocid species (e.g., harbor seals) exhibit this lactation strategy. Females come ashore for parturition with a moderate level of stored body energy. After giving birth, females remain onshore and fast while attending and nursing their young for a perinatal period ranging from a few days to a week. After this initial provisioning period, females leave their pups and return to sea to feed. These trips range from less than 1 day in some species to as long as 23 days in others, depending on the distance to the foraging location and prey abundance. Females then return to land to nurse their pup, after which they repeat the cycle until the pup is weaned. The lactation period in otariid species is quite long, ranging from 4 months to 3 years ( Bowen, 1991 ). Females of these species are considered income breeders, relying on current food intake to support both their own metabolic needs and the energetic cost of milk production. The milk produced by female otariids is relatively energy-dense (24 40% fat) compared to terrestrial mammalian species. up growth rates are rather low, ranging from 0.06 kg/day in Galapagos fur seals to 0.38 kg/day in Steller sea lions (Boness and Bowen, 1996 ). Harbor seals, a phocid species, also exhibit a form of this lactation strategy alternating short foraging trips to sea (7 10 h) with terrestrial nursing. The harbor seal is a relatively small phocid species, with females weighing approximately 84 kg at parturition. Given the small quantity of body energy that these females are able to store, female harbor seals are forced to make regular foraging trips to acquire sufficient energy to successfully wean their pups. Compared to otariid species, the length of the lactation period in harbor seals is much shorter (24 days) and the milk produced by females has a relatively higher fat content (50%). Consequently, pup growth rate is higher in harbor seals relative to otariid species (0.6 kg/day). Foraging cycles during lactation also may occur in ringed seals, and other relatively small phocid species. There is evidence that the females of two medium size phocids, the Weddell seal and the harp seal, may also forage during the lactation period. However, as noted above, the intensity of foraging and the degree to which successful weaning of offspring relies on these foraging trips is not clearly understood. Although small body size of some phocid species may limit females to a lactation strategy similar to otariids, difference in mammary gland structure between otariids and phocids may constrain the ability of phocid females from evolving a full-fledged foraging cycle (Schulz and Bowen, 2005 ).

5 856 inniped Ecology 2. Fasting Strategy In the larger-bodied phocid species, females fast during lactation. Females arrive at the breeding site with large energy stores in the form of adipose tissue (i.e., blubber). In the western Atlantic, for example, gray seal females arrive at Sable Island weighing an average of 210 kg. Of this body mass, 32% or 67 kg is fat. After parturition, females fast for the entire lactation period (e.g., 16 days in the case of gray seals), using their stored energy to support the energetic cost of milk production and their own maintenance metabolism. For this reason, female phocids are considered capital breeders having stored energy often months before it is needed. The lactation period in phocids is much shorter than in otariid species ranging from 4 days in hooded seals to 60 days in Weddell seals. Another characteristic feature of the phocid fasting strategy is the production of extremely high fat milk, ranging from 47% fat in southern elephant seals to 61% fat in hooded seals. This energy-dense milk results in a high rate of offspring growth, ranging from 1.4 kg/day in the Hawaiian monk seal to 7.1 kg/day in the hooded seal (Bowen, 1991 ). Weaning occurs abruptly when mothers return to sea to feed. ups often fast for weeks following weaning, living off their accumulated fat stores before entering the water and beginning to forage independently. Unstable breeding habitat, reduction in the fraction of energy expenditure devoted to maternal vs offspring requirements, and increased efficiency of milk energy transfer to offspring leading to higher growth rates all appear to have favored the evolution of the fasting strategy ( Schulz and Bowen, 2005 ). 3. Aquatic Nursing The walrus is the only pinniped species that exhibits aquatic nursing. Just prior to parturition, pregnant females separate from the herd and give birth to their offspring alone on pack ice. New mothers remain on the ice, fasting for the first few days postpartum, and relying on stored body energy accumulated prior to parturition. Subsequently, females and their young return to the herd to forage. Walrus pups suckle in the water for between 2 and 3 years on relatively low-fat milk (24.1%). As with otariids, weaning is gradual. Young walruses begin to feed on benthic organisms as early as 5 months of age and likely gain valuable foraging experience from their mothers over the remainder of lactation. At weaning, female offspring are assimilated into the mother s herd, whereas male offspring join other male groups. Lactation strategies are often viewed from the female s perspective. This seems reasonable, but in long-lived species such as pinnipeds, females may trade-off investment in current offspring against investment in future offspring. This may lead to conflicts between females and their offspring over the level of investment received. The transition from nursing pup to nutritionally independent juvenile usually occurs without parental supervision in pinnipeds. This transition is arguably the most important period of a pinniped s young life. As offspring size affects subsequent survival, we should expect that offspring would attempt to obtain as much milk as they can during lactation. Thus, the nutritional requirements and physiological abilities of individual offspring also must play a role in shaping lactation strategies. For example, the fasting ability of offspring constrains the duration of foraging trips by female fur seals and sea lions. IV. Foraging Successful foraging is essential for survival and reproduction, and is therefore a critical determinant of fitness. innipeds are among the largest vertebrate carnivores in marine ecosystems, and yet the foraging behavior of these upper-trophic level predators is generally poorly understood. As noted earlier, pinnipeds inhabit diverse habitats; consequently they forage over highly variable spatial and temporal scales, and in doing so they exploit a wide range of prey. A. Methods As pinnipeds generally feed under water at remote locations, ecologists rely upon indirect methods to gain insight into their foraging behavior and diets. Very high frequency (VHF) radio tags have been used to study the at-sea locations of coastal species such as harbor seals. Acoustic tags have been used to track the underwater movements of gray seals. More recently, microprocessor-based, time-depth recorders (TDRs) have been used to collect information on dive duration, depth, frequency, and temporal distribution and to calculate the at-sea locations of pinnipeds using solar navigation equations. However, the use of TDRs is often limited by the need to recover the instrument to retrieve the stored information and therefore only those species which can be reliably recaptured are used in TDR studies. In contrast, satellite-linked, time-depth recorders (SLTDRs) transmit collected data on diving parameters and surface positions to polar-orbiting satellites operated by Service Argos. This technology has broadened the range of species that have been studied, but the expense of using satellite-linked tags often places limits on the number of individuals studied. A new generation of tags, using fastloc GS, is providing more accurate locations to permit finer scale studies of foraging behavior and habitat use. Although we have learned a great deal from the use of location telemetry and dive recorders, these studies have provided little insight into the feeding success rate of pinnipeds. Recent work has demonstrated that estimates of feeding success can be determined using stomach-temperature telemetry and animal-borne video. The body temperature of marine prey is often considerably lower than that of its pinniped predator, thus the stomach temperature of the predator should drop following prey ingestion. This approach has been used successfully on free-living gray seals ( Austin et al., 2006a ) and several other species. When combined with information on the diving behavior and movement patterns in the same individual, stomach telemetry can provide new insights into the spatial and temporal patterns of foraging success relative to foraging effort ( Austin et al., 2006b ). Animal-borne video technology has taken our understanding of foraging behavior and diet one step further by providing direct observations of the way in which pinnipeds search for and capture prey, and how foraging behavior changes as a function of prey type (Bowen et al., 2002 ). Determining the diet of marine mammals also requires the use of indirect methods. The most common methods rely on the recovery and identification of hard prey structures that are resistant to digestion from the stomach, intestine, or feces of individual animals. Sagittal otoliths, cephalopod beaks, bones, scales, invertebrate exoskeletons, and shells can be used to determine the species consumed, and in some cases, to estimate the size and age of the prey. Fecal samples are increasingly being used for this purpose because they are less expensive to collect; a high proportion of samples contain identifiable prey, and estimates of diet are less affected by differential rates of digestion than are estimates from stomach samples ( Bowen and Siniff, 1999 ). Although the use of hard parts to estimate the diet of pinnipeds is common, this method is subject to a number of biases, which may limit the value of results. Firstly, stomach and fecal contents only provide an estimate of the diet near the point of collection, and as a result, offshore diets cannot easily be sampled. This may seriously bias the diet of wide-ranging species such as elephant seals, harp seals, northern fur seals, and Juan Fernandez fur

6 inniped Ecology 857 seals ( Arctocephalus philippii ). Secondly, hard parts are often eroded during digestion or are completely digested, such that prey size may be seriously underestimated and prey identification may not be possible. Finally, dietary analysis based on hard parts is strongly biased against soft-bodied or small prey with fragile structures. Inevitably, our understanding of the diets of pinnipeds is tied to the development of new methods. One such method is fatty acid signature analysis and its quantitative formulation, called quantitative fatty acid signature analysis (QFASA) ( Iverson et al., 2004 ). Lipids in marine ecosystems are diverse and characterized by long-chain polyunsaturated fatty acids that originate in unicellular phytoplankton. In carnivores such as pinnipeds, ingested fatty acids with a carbon chain length greater than 14 are deposited in body tissues in a predictable way. As a result, the fatty acid composition or signature of the predator reflects (but will never be the same as) the fatty acid composition of the prey species consumed ( Iverson et al., 2004, also see Blubber, this volume). By comparing the reference signature of various prey species to the fatty acid signature of the predator, obtained from blubber tissue or milk, diet composition can be estimated. The use of fatty acid signature analysis eliminates the dependence on recovery of hard parts and integrates the diet over a period of weeks to months, such that the location of sampling becomes less important. Nevertheless, QFASA depends on having determined the fatty acid composition of potential prey species; there is always the possibility that some prey species may not be reliably distinguish on the basis of fatty acids, leading to false positive identification of prey consumed. Stable isotope ratios of carbon and nitrogen found in the muscle, skin, vibrissae, or blood of pinnipeds and other predators are also being used to investigate diet. These ratios reflect a composite of prey species eaten over a broad time scale. By examining the levels of 15 N/ 14 N found in body tissues, researchers can determine the trophic level at which the pinnipeds fed. The carbon isotope ratio ( 13 C/ 12 C) has been found to vary geographically, and thus the level of carbon isotope in the predator s tissues provides insight into foraging location. While this technique is useful in determining trophic level and foraging location, it does not permit the diet composition of individuals to be estimated, except when only a few prey species are consumed. Finally, recent studies have indicated that the identification of prey species DNA recovered from pinniped feces can provide qualitative information on prey consumed, and may eventually also yield quantitative diet estimates ( Deagle and Tollit, 2007 ). B. Diet A large number of prey species have been identified in the diet of pinniped species, leading to the view that pinnipeds are generalist predators. This is consistent with the expectation that large wideranging predators consume more types of prey as their environment becomes patchier. However, in most cases, a relatively small number of species account for the majority of food eaten ( Bowen and Siniff, 1999 ). For example, gray seals on the Scotian Shelf, Canada, consumed 24 different taxa, but only 2 4 species accounted for over 80% of the energy consumed, depending on the time of the year. Fish and cephalopod species are the main prey types eaten by pinnipeds ( Table I ). However, crustaceans also appear to account for a substantial portion of prey consumed by some species. Crustaceans are a major prey of harp seals in the North Atlantic, and of ringed seals and bearded seals in the Bering Sea. In three Antarctic species, Antarctic fur seals, crabeater seals, and leopard seals, krill accounts for up to 50% of the diet. Unlike most pinnipeds, which generally feed on mobile prey (e.g., fishes, cephalopod molluscs, and crustaceans) in pelagic and benthic habitats, the walrus feed almost exclusively on sessile benthic invertebrates in soft-bottom sediments. Several pinniped species are also known to feed on other pinnipeds ( Bowen and Siniff, 1999 ). There is evidence that adult male South American fur seals ( Arctocephalus australis ) commonly feed on conspecific young. Steller sea lions are known to prey on a variety of pinniped species including harbor seals, ringed seals, bearded seals, young northern fur seals, and spotted seals. Walruses prey on spotted seals, ringed seals, and young bearded seals. The diet and foraging behavior of pinnipeds are influenced by a number of factors. The ecology and behavior of prey species clearly play a role in shaping the foraging tactics of pinnipeds. Research on the foraging behavior of adult male harbor seals at Sable Island, Canada, using animal-borne video, showed that prey behavior affected both capture technique and profitability of different prey types. Other studies have shown that between-year differences in diet composition of harbor seals were correlated with differences in the distribution and abundance of herring ( Clupea spp.) and sprat, two important prey species in Scotland. Intrinsic factors such as age and sex may also play a role in the diet composition of individuals within pinniped species. Given that pinnipeds are long-lived predators, their individual foraging tactics and behavior may change over time to reflect increased physiological capabilities and learning. For example, harbor seal pups feed on pelagic prey such as herring and squid, whereas the diet of adults is dominated by benthic species. Similarly, the contribution of benthic prey (e.g., crabs, clams, and sculpins) to the diet of bearded seals increases with age. Age-specific differences in diet composition have also been found in southern elephant seals and harp seals. In pinniped species that exhibit sexual body-size dimorphism, the diets of adult males and females may differ due to the relationship between energy requirements and body mass, whereby larger individuals require more total energy per unit time than do smaller individuals. Oxygen storage capacity also increases with body mass due to the larger blood pool in which to store oxygen and the larger muscle (myoglobin) mass. In addition, larger animals have a slower mass-specific metabolic rate, such that they utilize their larger oxygen stores at a slower rate relative to smaller individuals. Thus, larger individuals are capable of longer and deeper foraging dives. These physiological attributes may allow, or require, males (the larger sex) to pursue different prey types (potentially higher quality prey) than females. Males and females may also consume different prey to reduce the effects of intraspecific competition for food, and as a reflection of differences in the timing of reproductive costs. Gray seals are a good example of these effects acting on males and females to produce seasonal differences in both the energy density and diversity of the diet ( Beck et al., 2007 ). C. Foraging and Diving Behavior The foraging ecology of pinnipeds and other air-breathing vertebrates is constrained by the need to surface for oxygen. Dive duration is constrained by the interplay between the amount of oxygen that can be stored and the rate at which the diver expends oxygen. Thus, it is inevitable that the distribution of foraging in time and space will be influenced by the physiological constraints. Other factors, such as prey characteristics, presence of competitors, and predators also play an important role in how pinnipeds forage within these physiological constraints. Foraging pinnipeds dive repeatedly with relatively short surface intervals between dives; this cluster of dives is called a dive bout. In

7 858 inniped Ecology TABLE I Major rey of Selected innipeds Species Location Main prey Gray seal (Halichoerus grypus ) Eastern Canada Sandlance, redfish United Kingdom Sandlance Harbor seal (hoca vitulina ) Eastern Canada Herring, Atlantic cod ( Gadus morhua ), pollock (ollachius spp.), squid Western Canada acific hake ( Merluccius productus ), acific herring (Clupea pallasii ) Sweden Atlantic cod, sole, herring, sandlance Harp seal (agophilus groenlandicus ) Northwest Atlantic Arctic cod ( Arctogadus glacialis ), herring, capelin (Mallotus villosus ) White Sea/East ice Capelin, sandlance, herring Hooded seal (Cystophora cristata ) Greenland Greenland halibut (Reinhardtius hippoglossoides ), redfish, Gadidae Ringed seal (usa hispida ) Bering Sea Saffron cod ( Eleginus gracilis ), Arctic cod, shrimps Ribbon seal (Histriophoca fasciata ) Bering Sea ollock, eelpout, Saffron cod Bearded seal (Erignathus barbatus ) Bering Sea Shrimp, crab, clam S. elephant seal (Mirounga leonina ) Heard/Macquarie Island Squids, pelagic and benthic fishes Heard Island Squids, pelagic fishes N. elephant seal (M. angustirostris ) California Cephalopods, acific whiting (hake) Leopard seal (Hydrurga leptonyx ) Southern Ocean Krill, cephalopods, penguins, seals Northern fur seal (Callorhinus ursinus ) North acific Anchovy, herring, capelin, sandlance Bering Sea ollock, capelin, herring, squids South African fur seal ( Arctocephalus pusillus pusillus ) Benquela Current Anchovy, hakes, squid Antarctic fur seal (Arctocephalus gazella ) South Georgia Krill, cephalopods, fish Sub-Antarctic fur seal (A. tropicalis ) Gough Island Squids Australian fur seal (A. pusillus doriferus ) Tasmania Squids South American fur seal ( A. australis ) eru Sardine, southern anchovy, jack mackerel ( Trachurus spp.) Juan Ferná ndez fur seal ( A. philippii ) Alejando Selkirk Island Myctophid fishes, squid New Zealand fur seal ( A. forsteri ) New Zealand Octopus, squid, barracuda Steller sea lion (Eumetopias jubatus ) Gulf of Alaska ollock, herring, squids California sea lion (Zalophus californianus ) California Northern anchovy, acific whiting, squid general, dive bouts are thought to indicate foraging within a prey patch, particularly in otariid species. Theoretically, divers should organize their behavior for optimal use of prey. To organize their behavior in this way, divers should optimize both the time budget of the dive cycle (dive duration and surface interval) and the number of dive cycles to repeat. Both of these factors will influence the amount of prey caught and the energy and time consumed during the dive bout. However, there may be a trade-off between prey depth and profitability, such that prey items that might be exploited when closer to the surface are less likely to be exploited as the depth of that prey increases. Empirical tests of optimal foraging theory and optimal patch use in diving pinnipeds are uncommon, largely due to the difficulty and expense of studying these wide-ranging predators and their prey. However, it appears that some otariids feed near the surface on vertically migrating prey, such as krill, to maximize energetic efficiency. hocids are generally better suited for deep diving and for longer periods of time than are their otariid and odobenid counterparts. This is largely because phocids have a larger blood volume and larger myoglobin content in the muscles and thus store more oxygen per unit of body mass. hocids also dive in continuous bouts and are known to spend up to 90% of their time in the water submerged. Thus, unlike otariids and odobenids, phocid seals live at depth, periodically returning to the surface to breathe. Although diving behavior is often considered to be synonymous with foraging in otariids, dive shape analysis in phocids demonstrates that diving may also be used for travel, predator avoidance, and sleep (Wells et al., 1999 ). D. Factors Affecting Foraging Ecology innipeds are no doubt important consumers of marine species; however, for most species relatively little is still known about the ecological factors affecting diet or foraging success. Knowledge of the at-sea movements of pinnipeds is important because spatial patterns can fundamentally affect the nature and dynamics of species interactions. These interactions largely determine the distribution of foraging. Within the ocean, food is distributed in patches and this distribution can be strongly influenced by the physical properties, such as water temperature and the availability of nutrients. For example, the distribution and migratory patterns of northern