Earless Seals (marine mammals)

I. Systematics

The family Phocidae contains 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, a generally larger size, and the inability to draw their hindlimbs forward under their body when on land. This latter character, the absence of tusks, and a notched tongue also distinguish them from the family Odobenidae or walruses.

There had been considerable debate as to whether pinnipeds were diphyletic or monophyletic in origin. The diphyletic view proposed that odobenids and otariids were related to the bears (Ursidae) and that phocids were more closely linked to otters, weasels, and skunks (Mustelidae). However, a reevaluation of morphological evidence and the application of molecular techniques support the monophyletic hypothesis, with pinnipeds descending from arctoid carnivores, a group that includes the bears.

The Phocidae can be divided into two subfamilies: the Monachinae (Monachus spp.), with 2n=34 chromosomes, consisting of the southern phocids, the southern and northern elephant seals (Mirounga spp.), and the monk seals; and the Phoci-nae, or northern seals, with 2n=34 chromosomes in bearded (Erignathus barbatus) and hooded (Cystophora cristata) seals and 2n=32 chromosomes in the remaining seven species (Table I). The separation between these two groups has been confirmed in molecular studies, but the relationships among members within the subfamilies are uncertain. More recent work indicates that the gray seal (Halichoerus grtjpus) may not be sufficiently separated from the ringed seal to warrant its own genus, and a closer relationship between ribbon and harp seals than of either to the Phoca group. This suggests that the harp seal should retain its old name: Pagophilus groenlandicus. Support has also been found for grouping the ribbon, harp, and hooded together, but the use of karyotypic data as a diagnostic landmark in the phylogenetic analysis may be sufficient to maintain the separation (Table I).

II. Life History

Phocids are found throughout all of the world major oceans except for the Indian Ocean. Twelve species breed on ice and six species breed on land, including the Caribbean monk seal, which is probably extinct. The gray seal breeds on both land and on ice (Fig. 1). Among the ice-breeding seals, eight species breed primarily on pack ice. Four species breed 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 (Pusa hispida lagodensis and Pusa hispida saimensis) in Lakes Lagoda and Saimaa in Russia and Finland, respectively, and the Baikal seal (Pusa sibirica) in Lake Baikal in Siberia. Ringed seals also frequent Nettelling Lake on Baffin Island in northern Canada.

Pinnipeds are adapted to marine foraging but must haul out on land or ice for parturition and successful rearing of offspring. Marine adaptations 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. Compared to otariids, phocids generally spend more time at sea, swim more slowly, and dive to deeper depths and for longer periods. Southern elephant seals (Mirounga leonina) may dive to 1200 m and remain below the surface for up to 120 min. Other deep-diving phocids include northern elephant seals (M. angustirostris) (1500 m), Weddell seals (Leptonychotes weddellii) (700 m), and hooded seals (1000 m). Phocids have adopted what is sometimes referred to as a “slow-lane” strategy to reduce energy use during diving. This is achieved through a combination of (1) apnea with exhalation upon initiation of diving to minimize buoyancy and pressure-related problems; (2) an enhanced oxygen-carrying capacity, which is accomplished by a greater blood volume, an increase in red cell mass (haematocrit) within the blood cell volume, a greater hemoglobin concentration in the red blood cells, and possibly a higher content of oxygen-carrying myoglobin in the muscles; and (3) a generally larger body size to maximize oxygen-carrying abilities while minimizing mass-specific energy demands while diving.

The improvements in swimming ability have occurred at the expense of mobility on land or ice, which in turn increases vulnerability to terrestrial predators. Phocids whelp on the ice, isolated islands, or inaccessible beaches, which makes it more difficult for terrestrial predators to approach seals undetected. Some ice-breeding species, e.g., the Baikal seal and the ringed seals, limit further their accessibility to predators such as humans, bears (Ursus maritimus), arctic foxes (Alopex lagopus), and birds (e.g., Corvus sp., Larus sp.) by using small caves or lairs under the snow. These lairs also provide shelter from cold ambient temperatures. Current global-warming trends will likely result in the reduction of suitable ice habitat for many phocids, particularly in the more temperate regions of their distribution. This will impact not only seal populations, but also predators that rely on seals as food.

III. Reproduction

Sexual maturity is delayed in phocids. Some females are sexually mature at the age of 3+ years, but the mean age of sexual maturity is normally around 4-6 years, although it may vary with the population size and availability of resources. In northwest Atlantic harp seals the mean age of sexual maturity among females may vary from 5.8 and 4.6 years. These changes have mirrored changes in population size due to exploitation. As the population has increased, the mean age of sexual maturity has also increased. It is currently around 5.4 years. Normally about 80% of the adult females are pregnant, but some interannual variability in adult reproductive rates can occur. Extremely low (—-60%) adult reproductive rates have been documented in some years among ringed seals in the Beaufort Sea and Hudson Bay areas of northern Canada. These changes may be related to changes in ice conditions and the availability of food resources.

TABLE 1

Members of (he Family Phocidae, General Distribution, and Breeding Habitat

Males become sexually mature around the same time or slightly later than females, but recently mature males appear to be incapable of defending access to females until 2 or more years after they are sexually mature. Sexually monomorphic species have the longest life expectancies; e.g.. ringed seals aged 45 years old have been reported. The life expectancy of sexually dimorphic species is much shorter, particularly among males. In elephant seals, which show perhaps the most extreme level of sexual dimorphism, males are sexually mature at about 5 years of age, but they seldom achieve any rank within the colony until the age of 8. The greatest reproductive success occurs between the ages of 9-12 years, and males die by the age of 14.

The female phocid reproductive cycle is characterized by parturition, a short lactation period (4-50 days), copulation near the end of lactation, embryonic diapause (~3 months), and active fetal growth (~9 months). In most temperate species, implantation occurs during late summer-early autumn when light levels are decreasing, and pupping occurs during the spring, when light levels are increasing. However, an irregular pattern is seen among gray seals. Gray seals in the United Kingdom give birth during the fall, and implantation occurs during the spring. Implantation of the embryo occurs after the moult, when female energy reserves are at a minimum.

Figure 1 Gray seals on the ice in Northumberland Strait, Canada. The male is in the foreground, the female in the middle, and the white pup in the background.

Embryonic diapause provides females a mean of terminating reproduction if conditions are poor before her investment becomes too costly. It also leads to synchronization of reproductive activity.

The characteristic phocid lactation strategy consists of building up energy reserves throughout the year, fasting during lactation, and lactating for a short period. The utilization of fat reserves to satisfy their own energy requirements and the costs of providing milk for her pup has favored selection for large body size because energy stores scale to Mass1’0-1’19, whereas metabolic requirements scale to Mass0,5. Thus an increased body size increases energy-storing capabilities at a greater rate than increasing mass-specific energy requirements. This has led to a larger body size in phocid females than among otariid females (phocid females: mean = 229 kg, median = 141 kg; otariid females: mean = 80 kg, median = 55 kg). The need to build up energy reserves over the year probably adds about 12% to the daily energy requirements of a female phocid, but it also allows the spatial and temporal separation of feeding and reproduction.

To minimize the metabolic overhead associated with lactation, phocids have shortened the lactation period to 4-50 days instead of the months seen in otariids and odobenids. This is achieved by remaining beside the pup, providing more opportunities for the pup to suckle, and producing a very fat-rich milk, which increases the energy transfer per volume of milk consumed. In elephant seals, the fat content is veiy low at the beginning of lactation (~10%), but increases to about 50% fat by midlactation. In harp, gray, and Weddell seals, the milk fat content increases from around 40% to between 50 and 65% fat by midlactation, whereas in hooded seals there is relatively little change in fat content of the milk (55-68%) over the short 4-day lactation period (Fig. 2).

Stability of the whelping habitat and vulnerability to predation appear to be two important factors that have influenced the duration of lactation within the phocid group. Pups on unstable, drifting pack ice nurse for only 4 days in the hooded seal to as much as 30 days among the crabeater and Ross seals (mean = 18 days). In contrast, the longest lactation periods are found among the fast-ice-breeding Weddell, Baikal, and ringed seals (mean = 57 days). The lengthy lactation period among the very small ringed and Baikal seals may be related to their small size and their relative inability to store and deliver energy quickly to their offspring (Fig. 3). The Weddell seal, which weighs around 450 kg, is almost four times heavier than the diminutive ringed seal. The lengthy nursing period of Weddell seal pups may keep the young away from the fast-ice edges where their exposure to aquatic predators such as leopard seals and killer whales would be greater. The duration of lactation among land-breeding phocids is intermediate to that of the fast-ice and pack-ice animals, with an average of 32 days.

Figure 2 Newborri hooded seal pup with its mother weighing about 20 kg (A) and a weaned pup 4 days old weighing 44 kg (B). Behind the newborn, note the small balls (“silver dollars”) of fetal hair on the ice that were ejected with the placenta at birth.

The “fasting strategy” is certainly characteristic of lactation in the largest phocids such as the elephant seals and in the hooded seal. Facultative feeding occurs among female Weddell, bearded, harp, and gray seals, whereas feeding appears to be obligatory among the smaller phocids (^ 100 kg), such as harbor and ringed seals. Feeding may be necessary because females are unable to store sufficient energy to satisfy their own energy requirements, plus energy required for lactation. The need to continue foraging during lactation means that females must leave their pups in a safe area while they forage or the pup must accompany the female. In both instances, the spatial separation between whelping sites and foraging areas is limited. In the ringed seal, females scrape out lairs beneath the snow to haul out in. Females leave their pups to feed under the ice but remain close enough to help the pup move to an alternate lair if a predator approaches. Among harbor seals, foraging acivitv is restricted during the early stages of lactation. In large groups, as lactation advances, some females leave their pups unattended while they forage. In areas where only small groups are seen, the pups may follow the females over extensive distances of as much as 30 km away from the original haul-out site.

Figure 3 Female ringed seal with her pup on fast ice in Svalbard, Nonvai

Fewer studies have examined male energy expenditures during breeding, due in part to the difficulties associated with handling large, dangerous, and aggressive animals or their inaccessibility in the case of males that spend much of their time in water. Daily energy expenditures of males during the breeding season are much lower than those ol lemales because they do not incur the costs of milk production. However, once females wean their pups they resume feeding. This contrasts with males, who continue fasting to maximize their access to successively receptive females as the breeding season advances. Elephant, gray, and hooded seals appear to terminate breeding activity when fat levels have declined to levels similar to those observed in females. This suggests that the overall reproductive effort is similar between the two sexes.

At birth, phocid neonates are larger than otariid neonates. When female body size is taken into account, phocid and otariid mass at birth represents about 10% of their mother’s mass. The pups are quite lean at birth, with a fat content of 5-8%. Notable exceptions are hooded, harbor, and bearded seals, which are larger relative to other species, with a mass at birth equal to about 12-13% of the maternal mass. Harbor, hooded, and bearded seal pups also differ from otariid and other phocid pups by the presence of a thin blubber layer at birth. Fat content represents 11-14% of the total body mass in harbor and hooded seal pups at birth. Phocid pups gain weight rapidly, achieving a weaning mass two to five times their birth mass in a period of 4-50 days, but mass at weaning is relatively constant across species, being equivalent to 25-30% of the mother’s mass. Among hooded, harp, and gray seal pups. 65-75% of the milk energy is deposited, primarily as fat. Elephant, hooded, harp, ringed, and grav seal pups are 40-50% fat at weaning, whereas species with very active pups, such as Weddell. bearded, and harbor seals, may contain only 34-37% fat at weaning. The rate of mass gain is inversely related to the duration of the lactation period when expressed relative to the female’s metabolic mass. The lowest rates of relative mass gain are seen among Hawaiian monk seals, bearded, harbor, and ringed seals, species where the pups are verv active and begin entering the water early during lactation. Ice-breeding neonate phocids. such as harp, ringed, ribbon, Caspian. Baikal, and largha seals, are born with a white, relatively long fur called lanugo (Fig. 3). The white color mav provide some protective camouflage on the white snow from predators. However, the lanugo may be more effective in its role as an insulator, particularly to the verv voimg pup who has not yet developed a thick layer of blubber for insulation. The structure and color of this fur permits short-wave energy received from the sun to be transmitted through the fur. where it is absorbed bv the dark skin. It also traps heat energy radiated from the animal’s skin and thus acts like a greenhouse, heating up the air trapped within the fur, but limiting heat loss to the outside air. Among species where the young enter the water very soon after birth (e.g., harbor, bearded, and hooded seals), the young are born with a thin layer of blubber, and the lanugo is shed or moulted within the uterus. This is because blubber acts as a much better insulator in water than fur. Among harbor seals, 5-30% of the pups are born with a white lanugo, depending on the region, but this is quicklv replaced by a grayish pelage similar to that ol adults. In bearded seals, shedding of the lanugo begins in utero, but is completed after birth. In hooded seals, the fetal fur is expelled in small clumps oil the ice with the placenta; these are referred to as silver dollars bv commercial sealers. At birth the pups are covered by blue (dorsal) and silver (ventral) fur that is much thicker and longer than the adult fur, and at this stage the pups are known as bluebacks (Fig. 2). Hooded seal pups differ from harbor and bearded seals in that they do not enter the water until they are weaned. However, in this species lactation lasts for onlv 4 days. The remaining species that whelp on the ice in the Northern Hemisphere tend to give birth to pups with a white lanugo, which may afford some protection against surface predators. Gray seals have their pups on both the land and on the ice. but the pups are born with a white lanugo (Fig. 1). Neonates of southern ice-breeding seals, such as Weddell, crabeater (Lobodon carcinophaga), leopard (Hydmrga leptonyx), and Ross seals (Ominatophoca rossii), are born with a gray, brown, or grayish-brown pelage. Southern ice-breeding phocids are not exposed to surface predators other than humans and hence the white lanugo may not be required. Elephant and monk seal pups are born on land with a black pelage.

Pup mortality during the lactation period is normally quite low. Among land-breeding species, trampling and wounds caused by interactions between adults may encourage infection, which may result in death of the pup. This problem is more aggravated in crowded colonies where the number of interactions would increase. In Arctic ice-breeding species, predation by bears, foxes, and birds such as ravens (Corvtis sp.) and gulls (Larus sp.) in the case of ringed seal pups is an important source of pup mortality, although the effects of predation are reduced by the use of lairs. Ringed seal pups are also quite active and are capable swimmers at a very young age. However, swimming incurs a high metabolic cost due to the minimum blubber thickness. Repeated disturbance may affect growth and survival. Surface predators are not present in the southern polar regions, but leopard seals and killer whales are important marine predators. In the pack ice, pups may drown or be crushed as a result of storms causing the breakup and rafting of the ice.

IV. Mating Systems

The study of mating systems among phocids has relied heavily on behavioral observations of animals in the breeding areas. Male reproductive success has been evaluated by a male’s ability to monopolize females or by the number of copulations observed. However, DNA techniques have suggested that the evaluation of reproductive success may be more complex, with the existence of alternative mating strategies within a population. In captive harbor seals, behavioral observations during courtship were not reliable indices of paternity, whereas in one population of gray seals, large males sired significantly fewer pups than would otherwise have been indicated from their observed mating opportunities. Females tended to produce several pups fathered by the same male, who in many cases was not the large attendant male.

Phocids breeding on land prefer islands or isolated beaches, where threats from predation are reduced. The combination of habitat limitations and synchronization of reproductive activity encourages the aggregation of females. Males are not involved in caring for the pup. Therefore the best strategy for males is to copulate with as many females as possible, whereas the strategy of females is to successfully rear her pup. Males will attempt to prevent other males from having access to females. In phocids, this may involve defending a geographical area, but if the female moves, the male will follow to defend a new space around the female. The number of females that can be defended is limited by habitat features and the skills of defending males. Large, open beaches are more difficult for a male to control than more topographically irregular sites, where geographic barriers will aid established males in limiting the approach of intruding males. Reproductive success will also be affected by the fighting and signaling ability of males and how long they can remain beside females without leaving to feed. In male hooded seals, a series of displays involving the inflatable nasal sac and nasal septum are often associated with the approach of other males (Fig. 4). Not all approaches result in combat, suggesting that some signaling occurs. The gradual evolution toward large size observed in females, which permitted the separation of reproduction and feeding, would also have operated on males as well. Larger males could spend more time ashore fasting. Larger males would also be favored over small males in combat, although experience and individual skill development would also be contributing factors. The greatest degree of polygyny seen among phocids is exhibited by the elephant seals, who may defend harems containing upward of 100 females. Southern elephant seal males may weigh up to 3700 kg, whereas northern elephant seal males may reach 2300 kg. In both species the males are typically five to six times larger than the females. Males arrive on the whelping area just before the females and the most successful males remain on the beaches fasting until the last females leave about 3 months later.

In other species the development of polygyny is more variable. Gray seals copulate on land and occasionally in water. Males at 350 kg are about 50% larger than females. In some areas in the British Isles, they control access to up to 8 females, whereas in the open beaches and ice-breeding areas in Canada, males are only able to control access to 1 to 3 females. Less is known about the structure of mating systems of phocids that copulate primarily in water. The development of polygyny is limited by the three-dimensional nature of the marine environment. Among hooded seals, the marked sexual dimorphism observed in many terrestrial mating species is also observed. Male hooded seals weigh up to 440 kg, whereas females reach about 290 kg. The hooded seal male begins to defend one female about midway through the short 4-day lactation period (Fig. 4). Once the pup is weaned, he accompanies the female into the water, mates with her, and then returns to the ice and will attempt to establish himself beside another female. Because pupping occurs over a 2- to 3-week period, males have opportunities for multiple matings during that period. Mating success of a male is affected by his ability to defend access to females against other males and by the amount of time he can spend on the ice before his energy reserves are depleted. Among the remaining phocids that copulate in the water, little difference in body size is seen between males and females; in some cases, such as bearded and Weddell seals, the females appear to be slightly larger. In these cases, smaller size may favor underwater agility. The mating system of harp seals has been referred to as promiscuous, but little information is available. Males do haul out, but no displays or fighting are observed on the ice. Extensive vocal activity within harp seal whelping patches has been recorded, and groups of males are observed often patrolling leads, vocalizing and diving. It is possible that male harp seals are displaying to females, suggesting more of a lek-type system, but there is insufficient data to comment further. Among ringed seals, the presence of predators in the fast ice, such as bear s, foxes, and humans, selects against aggregation, whereas the need to continue feeding during lactation, in an area generally considered to have low productivity, would also be a contributing factor. In this species, some underwater vocal activity has been recorded, but unlike the underwater vocalizations of the widely dispersed bearded seal that can be heard over distances of 25 km, the underwater vocalizations of the ringed seal are relatively weak, limiting their use as a signal to potential mates. However, the males emit a strong odor during the breeding season due to the enlargement and increased secretion activity of sebaceous and apocrine glands in the muzzle region. The strong odor may serve as a signal to inform both females and other males that a breathing hole is used or belongs to a particular male. In harbor seals, the females move with their pups between haul-out sites and foraging areas. Males are unable to defend females or sites against other males. As the time that females will become receptive approaches, males reduce the size of the range that they occupy, but remain in the water, making repeated short dives that are associated with underwater vocal displays. Some males establish themselves near haul-out sites and some near foraging areas used by females, whereas others appear to establish themselves on transit routes between haul-out sites and foraging areas. It has been suggested that a “lekking” type of mating system occurs in this species. In the Antarctic Weddell seal, males appear to defend underwater territories around breathing holes and cracks.

Figure 4 Two male hooded seals fighting on pack ice in the Gulf of St. Lawrence, Canada. Note the inflatable sac on the male on the left.

V. Foraging

Many early studies relied on stomach content material from hunted animals, fecal collections, and entrapments in fishing gear to provide information on diving and foraging activity. During the last decade, major technological advances have provided researchers with satellite transmitters, time-depth recorders, stomach temperature probes, and video recorders to study diving and foraging activity.

Phocids feed on a wide variety of prey, including invertebrates, such as amphipods, mysids, squid, and krill, and vertebrate prey, such as fish. Birds have been recorded in the diet of some species such as the leopard seal and harp seal. Leopard seals also prey on other seal species, and cannibalism has been reported in gray seals. Diet composition may change seasonally, geographically, and with age. Newly weaned pups of ringed and harp seals begin foraging on zooplankton in their initial attempts to forage independently and then become more piscivorous as their skills develop. Phocids feed primarily on smaller prey that can be consumed whole, but large prey may be taken. Under certain conditions where prey are very abundant or accessible, e.g., when fish are caught in nets, seals may consume only pieces from fish.

Little is known about factors affecting prey choice. Research has indicated that feeding preferences in harp and harbor seals occur for particular types and sizes of prey that may be independent of local abundance. Harp seals digest capelin more efficiently than most other prey, and throughout their range capelin forms an important component of their diet, whereas other species such as commercially important Atlantic cod (Gadus morhua) form only a very minor component in the overall diet. While foraging, phocids must balance their intake of oxygen and the distribution of oxygen for locomotion, body maintenance, and processing of food (specific dynamic action or heat increment of feeding). Their approach to balancing these sometimes conflicting needs will influence their foraging strategy. A seal may process (digest) food while actively swimming and foraging. If it uses only aerobic metabolism, then the consumption of oxygen required to process the food will reduce the amount of time spent diving and collecting food. If the seal attempts to maintain the duration of diving, then the switch to anaerobic conditions will force the animal to rest at the surface until lactic acid levels are reduced. A second strategy is to forage and then spend time resting at the surface, hauled out on the ice or on land until food processing is completed. However, resting at the surface increases vulnerability to surface predators such as sharks or killer whales, whereas returning to shore or ice involves time lost due to transit and may limit the distances that foraging can occur away from haul-out sites. A third strategy involves foraging and then if successful, reducing locomotory costs by drifting during the surfacing phase of the dive, allowing food processing to occur. Many phocids may utilize the first two strategies. Weddell, ringed, harp, and hood seals are often seen hauled out on the ice and occasionally on land. Harbor and gray seals may forage in offshore areas, but rarely spend more than a few days away from haul-out sites. The third strategy appears to be utilized by elephant seals, who spend almost 8-9 months of the year at sea.

Foraging activity has been examined in detail in elephant seals. In northern elephant seals, females are dispersed over a broad geographic area across the northeastern Pacific from the coast to as far west as 150°W, but tend to remain between 44° and 52°N. Foraging occurs both offshore and during transit between inshore and offshore areas. Diurnal changes in diving depths are observed, indicating that they are foraging on vertically migrating prey in the pelagic and mesopelagic environment. Their principal prey are mesopelagic squid and fish. Males utilize a different foraging strategy by foraging little while en route to particular foraging areas along continental margins off the stage of Washington to as far north as the Aleutian Islands. Once on site, repeated, uniform flat-bottomed dives predominate diving, with little diurnal variability, suggesting intensive foraging activity, possibly on benthic prey such as energy-rich elasmobranchs and cyclostomes (sharks, skates, ratfish, hagfish). While at sea, both species dive continuously, spending almost 90% of their total time at sea submerged, leading to the suggestion that they should be called surfacers instead of divers. At the opposite end of the size spectrum, a very different strategy is seen among harbor seals. Although capable of diving to depths of 500 m, harbor seals rarely dive deeper than 65 m and, in some studies, an average of 65% of diving activity occurs at depths of less than 4 m. Visual and telemetry data indicate that harbor seals in some areas spend most of their time very close to the coast in shallow water areas. Foraging distances rarely exceed 50 km away from haulout sites. Little difference is seen between males and females in dive depths and foraging distances away from haul-out sites outside of the breeding season.