Pinniped
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Pinnipeds (pronounced /ˈpɪnɪˌpɛdz/), commonly known as seals,[lower-alpha 1] are a widely distributed and diverse clade of carnivorous, fin-footed, semiaquatic, mostly marine mammals. They comprise the extant families Odobenidae (whose only living member is the walrus), Otariidae (the eared seals: sea lions and fur seals), and Phocidae (the earless seals, or true seals), with 34 extant species and more than 50 extinct species described from fossils. While seals were historically thought to have descended from two ancestral lines, molecular evidence supports them as a monophyletic lineage (descended from one ancestral line). Pinnipeds belong to the suborder Caniformia of the order Carnivora; their closest living relatives are musteloids (weasels, raccoons, skunks and red pandas), having diverged about 50 million years ago.
Pinnipeds | |
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Clockwise from top left: New Zealand fur seal (Arctocephalus forsteri), southern elephant seal (Mirounga leonina), Steller sea lion (Eumetopias jubatus), walrus (Odobenus rosmarus) and grey seal (Halichoerus grypus) | |
Scientific classification | |
Domain: | Eukaryota |
Kingdom: | Animalia |
Phylum: | Chordata |
Class: | Mammalia |
Order: | Carnivora |
Clade: | Pinnipedimorpha |
Clade: | Pinnipediformes |
Clade: | Pinnipedia Illiger, 1811[1] |
Subclades | |
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Range map |
Seals range in size from the 1 m (3 ft 3 in) and 45 kg (100 lb) Baikal seal to the 5 m (16 ft) and 3,200 kg (7,100 lb) southern elephant seal. Several species exhibit sexual dimorphism. They have streamlined bodies and four limbs that are modified into flippers. Though not as fast in the water as dolphins, seals are more flexible and agile. Otariids use their front limbs primarily to propel themselves through the water, while phocids and walruses use their hind limbs. Otariids and walruses have hind limbs that can be pulled under the body and used as legs on land. By comparison, terrestrial locomotion by phocids is more cumbersome. Otariids have visible external ears, while phocids and walruses lack these. Pinnipeds have well-developed senses—their eyesight and hearing are adapted for both air and water, and they have an advanced tactile system in their whiskers or vibrissae. Some species are well adapted for diving to great depths. They have a layer of fat, or blubber, under the skin to keep warm in cold water, and, other than the walrus, all species are covered in fur.
Although pinnipeds are widespread, most species prefer the colder waters of the Northern and Southern Hemispheres. They spend most of their lives in water, but come ashore to mate, give birth, molt or to avoid ocean predators, such as sharks and orcas. Seals mainly live in marine environments but can also be found in fresh water. They feed largely on fish and marine invertebrates; a few, such as the leopard seal, feed on large vertebrates, such as penguins and other seals. Walruses are specialized for feeding on bottom-dwelling mollusks. Male pinnipeds typically mate with more than one female (polygyny), although the degree of polygyny varies with the species. The males of land-breeding species tend to mate with a greater number of females than those of ice breeding species. Male pinniped strategies for reproductive success vary between defending females, defending territories that attract females and performing ritual displays or lek mating. Pups are typically born in the spring and summer months and females bear almost all the responsibility for raising them. Mothers of some species fast and nurse their young for a relatively short period of time while others take foraging trips at sea between nursing bouts. Walruses are known to nurse their young while at sea. Seals produce a number of vocalizations, notably the barks of California sea lions, the gong-like calls of walruses and the complex songs of Weddell seals.
The meat, blubber and skin of pinnipeds have traditionally been used by indigenous peoples of the Arctic. Seals have been depicted in various cultures worldwide. They are commonly kept in captivity and are even sometimes trained to perform tricks and tasks. Once relentlessly hunted by commercial industries for their products, seals are now protected by international law. The Japanese sea lion and the Caribbean monk seal have become extinct in the past century, while the Mediterranean monk seal and Hawaiian monk seal are ranked as endangered by the International Union for Conservation of Nature. Besides hunting, pinnipeds also face threats from accidental trapping, marine pollution, climate change and conflicts with local people.
The name "pinniped" derives from the Latin words pinna "fin" and pes, pedis "foot".[2] The common name "seal" originates from the Old English word seolh, which is in turn derived from the Proto-Germanic *selkhaz.[3]
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Cladogram showing relationships among the living pinnipeds, found in Berta, Churchill and Boessenecker (2018). The Southern Hemisphere eared seal clade is not fully resolved.[4] |
The German naturalist Johann Karl Wilhelm Illiger was the first to recognize the pinnipeds as a distinct taxonomic unit; in 1811 he gave the name Pinnipedia to both a family and an order.[5] American zoologist Joel Asaph Allen reviewed the world's pinnipeds in an 1880 monograph, History of North American pinnipeds, a monograph of the walruses, sea-lions, sea-bears and seals of North America. In this publication, he traced the history of names, gave keys to families and genera, described North American species and provided synopses of species in other parts of the world.[6] In 1989, Annalisa Berta and colleagues proposed the unranked clade Pinnipedimorpha to contain the fossil genus Enaliarctos and modern seals as a sister group.[7] Pinnipeds belong to the order Carnivora and the suborder Caniformia (known as dog-like carnivorans).[8] Of the three extant families, the Otariidae and Odobenidae are grouped in the superfamily Otarioidea,[9] while the Phocidae belong to the superfamily Phocoidea.[10] There are 34 extant species of pinnipeds,[4] and more than 50 fossil species of pinnipedimorphs.[11]
Otariids are also known as eared seals due to the presence of pinnae. These animals swim mainly using their well-developed fore-flippers. They can also "walk" on land by shifting their hind-flippers forward under the body.[12] The front end of an otariid's frontal bone protrudes between the nasal bones, with a large and flattened supraorbital foramen. An extra spine splits the supraspinatous fossa and bronchi that are divided in the front.[13] Otariids consist of two types: sea lions and fur seals; the latter typically being smaller in size with pointier snouts, longer fore-flippers and heavier fur coats.[14] Five genera and seven species (one now extinct) of sea lion are known to exist, while two genera and nine species of fur seal exist. While sea lions and fur seals have historically been considered separate subfamilies (Otariinae and Arctocephalinae respectively), genetic and molecular evidence has refuted this, indicating that the northern fur seal is basal to other otariids and the Australian sea lion and New Zealand sea lion are more closely related to Arctocephalus than to other sea lions.[4]
Odobenidae consists of only one living member: the modern walrus. This animal is noticeable from its larger size (exceeded only by the elephant seals), nearly hairless skin, flattened snout and long upper canines, known as tusks. Like otariids, walruses are capable of walking on land with their hind-flippers. When moving in water, the walrus relies on its hind-flippers for locomotion, while its fore-flippers are used for steering. In addition, visible ear flaps are not present in the species.[15][16] The epipterygoid of the jaw is well developed and the back of the nasal bones are horizontal. In the feet, the calcaneuses protrude in the middle.[13]
Phocids are known as true or "earless" seals. These animals lack external ear flaps and are incapable of positioning their hind-flippers to move on land, making them more cumbersome. This is because of their massive ankle bones and flatter heels. In water, true seals rely on the side-to-side motion of their hind-flippers and lower body to move forward.[12] The phocid's skull has thickened mastoids, puffed up entotympanic bones, nasal bones with a pointed tip in the back and a non-existent supraorbital foramen. The hip has a more converse ilium.[13] A 2006 molecular study supports the division of phocids into two monophyletic subfamilies: Monachinae, which consists of elephant seals, monk seals and Antarctic seals; and Phocinae, which consists of all the rest.[4][16]
Evolution
One popular hypothesis suggested that pinnipeds are diphyletic (descended from two ancestral lines), with walruses and otariids sharing a recent common ancestor with bears; and phocids sharing one with Musteloidea. However, morphological and molecular evidence support a monophyletic origin.[13] A 2021 genetic study found that pinnipeds are more closely related to musteloids.[17] Pinnipeds split from other caniforms 50 million years ago (mya) during the Eocene.[18] Fossil animals representing basal lineages include Puijila, of the early Miocene in Arctic Canada. It resembled a modern otter, but shows evidence of quadrupedal swimming—retaining a form of aquatic locomotion that led to those employed by modern pinnipeds. Potamotherium, which lived in the same period in Europe, was similar to Puijila but more aquatic.[19] The braincase of Potamotherium shows evidence that it used its whiskers to hunt, like modern seals.[20] Both Puijila and Potamotherium fossils have been found in lake deposits, suggesting that seal ancestors were originally adapted for fresh water.[19]
Enaliarctos, a fossil species of late Oligocene/early Miocene (24–22 mya) California, closely resembled modern pinnipeds; it was adapted to an aquatic life with flippers and a flexible spine. Its teeth were more like land predators in that they were more adapted for shearing. Its hind-flippers may have allowed it to walk on land, and it probably did not leave coastal areas as much as its modern relatives. Enaliarctos was likely more of a fore-flipper swimmer, but could probably swim with either pair.[13] One species, Enaliarctos emlongi, exhibited notable sexual dimorphism, suggesting that this physical characteristic may have been an important driver of pinniped evolution.[21] A closer relative of extant pinnipeds was Pteronarctos, which lived in Oregon 19–15 mya. As in modern seals, the maxilla or upper jaw bone of Pteroarctos intersects with the orbital wall. The extinct family Desmatophocidae lived 23–10 mya in the North Pacific. They had long skulls that with large orbits, interlocked zygomatic bones and rounded molars and premolars. They also were sexually dimorphic and may have been capable of swimming with both or either pair of flippers.[13] They are grouped with modern pinnipeds, but there is debate as to whether they are more closely related to phocids or to otariids and walruses.[22][4]
The ancestors of the Otarioidea and Phocidea diverged around 25 mya.[23] Phocids are known to have existed for at least 15 million years,[13] and molecular evidence supports a divergence of the Monachinae and Phocinae lineages around this time.[4] The fossil genera Monotherium and Leptophoca of southeastern North America represent the earliest members of Monachinae and Phocinae respectively.[13] Both lineages may have originated in the North Atlantic, and likely reached the Pacific via the Central American Seaway. Phocines mainly stayed in the Northern Hemisphere, while the monachines diversified southward.[4] The lineages of Otariidae and Odobenidae split around 20 mya.[23] The earliest fossil records of otariids are in North Pacific and dated to around 11 mya. Early fossil genera include Pithanotaria and Thalassoleon.[13] The Callorhinus lineage split the earlist, followed by the Eumetopias/Zalophus lineage and then the rest, which colonized the Southern Hemisphere.[13][4] The earliest fossils of Odobenidae—Prototaria of Japan and Proneotherium of Oregon—date to 18–16 mya. These primitive walruses had normal sized canines and fed on fish instead of mullusks. Later taxa like Gomphotaria, Pontolis and Dusignathus had longer canines on both the upper and lower jaw. The familiar long upper tusks developed in the genera Valenictus and Odobenus. The lineage of the modern walrus may have spread from the North Pacific to the North Atlantic through the Caribbean and Central American Seaway 8–5 mya, and then back to the North Pacific via the Arctic 1 mya, or to the Arctic and subsequently the North Atlantic during the Pleistocene.[13]
Pinnipeds have streamlined, spindle-shaped bodies with small or non-existent ear flaps, rounded heads, short muzzles, flexible necks, limbs modified into flippers and small tails.[24][25][26] The mammary glands and genitals can withdraw into the body.[24] Seals are unique among carnivorans in that their orbital walls are mostly shaped by the maxilla and are not contained by certain facial bones.[13] Compared to land carnivores, pinnipeds have fewer teeth, which are pointed and cone-shaped. They are adapted for holding onto slippery prey rather than shearing meat like the carnassials of other carnivorans. The walrus has unique tusks which are long upper canines.[27]
Pinnipeds range in size from the 1 m (3 ft 3 in) and 45 kg (100 lb) Baikal seal to the 5 m (16 ft) and 3,200 kg (7,100 lb) southern elephant seal. Overall, they tend to be larger than other carnivores.[24] Several species have male-biased sexual dimorphism that depends on how polygynous a species is: highly polygynous species like elephant seals are extremely sexually dimorphic, while less polygynous species have males and females that are closer in size, or, in the case of Antarctic seals, females are moderately bigger. Males of sexually dimorphic species also tend to have secondary sex characteristics, such as larger or more prominent heads, necks, chests, crests, noses/proboscis and canine teeth as well as thicker fur and manes.[28][29] Though more polygynous species tend to be sexually dimorphic, some evidence suggests that size differences between the sexes originated due to ecological differences, with polygyny developing later.[30][31]
Almost all pinnipeds have fur coats, the exception being the walrus, which is only sparsely covered. Even some fully furred species (particularly sea lions) are less furry than land mammals. Fur seals have lush coats consisting of an undercoat and guard hairs.[32] In species that live on ice, young pups have thicker coats than adults. The individual hairs on the coat, known collectively as lanugo, can trap heat from sunlight and keep the pup warm.[33] Pinnipeds are typically countershaded, and are darker colored dorsally and lighter colored ventrally, which serves to counter the effects of self-shadowing caused by light shining over the ocean water. The pure white fur of harp seal pups conceals them in their Arctic environment.[34] Several species have clashing patterns of light and dark pigmentation.[24][34] All fully furred species molt; the process of which may be quick or gradual depending on the species.[35] Seals have a layer of subcutaneous fat, known as blubber, that is particularly thick in phocids and walruses.[24][33] Blubber serves both to keep the animals warm and to provide energy and nourishment when they are fasting. It can constitute as much as 50% of a pinniped's mass. Newborn pups have a thin layer of blubber, but some species compensate for this with thick lanugos.[33]
The simple stomach of pinnipeds is typical of carnivores. Most species have neither a cecum nor a clear demarcation between the small and large intestines; the large intestine is comparatively short and only slightly wider than the small intestine. Small intestine lengths range from 8 times (California sea lion) to 25 times (elephant seal) the body length. The length of the intestine may be an adaptation to frequent deep diving, allowing for more room in the digestive tract for partially digested food. An appendix is absent in seals.[36] As in most marine mammals, the kidneys are divided into lobes and filter out excess salt.[37]
Locomotion
Pinnipeds have two pairs of flippers on the front and back, the fore-flippers and hind-flippers. Their elbows and ankles are not externally visible.[34] Pinnipeds are not as fast as cetaceans, typically swimming at 5–15 kn (9–28 km/h; 6–17 mph) compared to around 20 kn (37 km/h; 23 mph) for several species of dolphin. Seals are more agile and flexible,[38] and some otariids, such as the California sea lion, can make dorsal turns as the back of their heads can touch their hind flippers.[39] Pinnipeds have several adaptions for reducing drag. In addition to their streamlined bodies, they have smooth networks of muscle bundles in their skin that may increase laminar flow and cut through the water. The hair erector muscles are absent, so their fur can be streamlined as they swim.[40]
When swimming, otariids rely on their fore-flippers for locomotion in a wing-like manner similar to penguins and sea turtles. Fore-flipper movement is not continuous, and the animal glides between each stroke.[41][42] Compared to terrestrial carnivorans, the fore-limb bones of otariids are reduced in length, giving them less resistance at the elbow joint as the flippers flap;[43] the hind-flippers maneuver them.[44] Phocids and walruses swim by moving their hind-flippers and lower body from side to side, while their fore-flippers are mainly used for maneuvering.[42][45][16] Some species leap out of the water, and "ride" waves.[46]
Pinnipeds can move around on land, though not as well as terrestrial animals. Otariids and walruses are capable of turning their hind-flippers forward and under the body so they can "walk" on all fours.[47] The fore-flippers move along a transverse plane, rather than the sagittal plane like the limbs of land mammals.[48] Otariids create momentum by laterally swaying their heads and necks.[49][48] Sea lions have been recorded climbing up flights of stairs. Phocids lack the ability to walk on their hind-flippers, and must flop their bodies forward as their fore-flippers keep them stable. In some species, the fore-flippers may act like rowers pushing against the ground. Phocids can move faster on ice, as they can sled along.[50]
Senses
The eyes of pinnipeds are relatively large for their size and are positioned near the front of the head. Only the smaller eyes of the walruses are located on each side of the head;[51][52] since they forage at the bottom for sedentary mollusks.[51] A seal's eye is suited for seeing both underwater and in air. Most of retina is equidistant around the spherical lens. The cornea has a flattened center where refraction does not change between air and water. The vascular iris has a strong dilator muscle. A contracted pupil is typically pear-shaped, although the bearded seal's is more horizontal. Compared to deep-diving elephant seals, the iris of shallower species, such as harbor seals and California sea lions, does not change much in size between contraction and expansion.[53] Seals are able to see in darkness with a tapetum lucidum, a reflecting layer that increases sensitivity by reflecting light back through the rods.[54]
On land, pinnipeds are near-sighted in dim light. This is reduced in bright light as the retracted pupil decreases the ability of the lens and the cornea to refract (bend) light.[55] Polar living seals like the harp seal have corneas that are adapted to the bright light that reflects off snow and ice. As such, they do not suffer snow blindness.[56][55] Pinnipeds appear to have limited color vision as they lack S-cones.[57] Flexible eye movement has been documented in seals.[58] The walrus can project its eyes out from its sockets in both a forward and upward direction due to its advanced extraocular muscles and absence of an orbital roof.[16] The seal eye is durable as the corneal epithelium is hardened by keratin, and the sclera is thick enough to withstand the pressures of diving. Seals also secrete mucus from the lacrimal gland to protect their eyes. As in many mammals and birds, pinnipeds possess nictitating membranes.[59]
The pinniped ear is adapted for hearing underwater, where it can hear sound frequencies of up to 70,000 Hz. In air, hearing is somewhat reduced in pinnipeds compared to many terrestrial mammals. While their airborne hearing sensitivity is generally weaker than humans', they still have a wide frequency range.[60] One study of three species—the harbor seal, California sea lion and northern elephant seal—found that the sea lion was best adapted for airborne hearing, the elephant seal for underwater hearing and the harbor seal was equally adapted for both.[61] Although pinnipeds have a fairly good sense of smell on land,[62] it is useless under water as their nostrils are closed.[63]
Pinnipeds have well-developed tactile senses. Compared to terrestrial mammals, the moustache-like whiskers or vibrissae of pinnipeds have ten times more nerve connections, allowing them to effectively detect vibrations in the water.[64] These vibrations are generated, for example, when a fish swims through water. Detecting vibrations is useful when the animals are foraging, and may add to or even replace vision, particularly in darkness.[65][66] Harbor seals can follow hydrodynamic paths made by other animals minutes earlier, similar to a dog following a scent trail,[67][68] and even to discriminate the size and type of object responsible for the trail.[69]
Unlike terrestrial mammals, such as rodents, pinnipeds do not sweep their whiskers over an object when examining it, but can protract the hairs forward while holding them steady, maximizing their detection.[65][70] The vibrissa's angle relative to the flow seems to be the most important contributor to detection ability.[70] The whiskers of some otariids grow quite long—those of the Antarctic fur seal can reach 41 cm (16 in).[71] Walruses have the most vibrissae, at 600–700 individual hairs. These are important when searching for prey along the bottom. In addition to foraging, whiskers may also play a role in navigation; spotted seals appear to use them to detect breathing holes in the ice.[72]
Diving adaptations
To dive, a pinniped must first exhale much of the air out of its lungs and shut its nostrils and throat cartilages to protect the trachea.[73][74] The airways are supported by cartilaginous rings and smooth muscle, and the chest muscles and alveoli can completely deflate during deeper dives.[75][76] While terrestrial mammals are generally unable to empty their lungs, pinnipeds can reinflate their lungs even after respiratory collapse.[76] The middle ear contains sinuses that probably fill with blood during dives, preventing middle ear squeeze.[77] The heart of a seal is moderately flattened to allow the lungs to deflate. The trachea is flexible enough to collapse under pressure.[73] During deep dives, any remaining air in their bodies is stored in the bronchioles and trachea, which prevents them from experiencing decompression sickness, oxygen toxicity and nitrogen narcosis. In addition, seals can tolerate large amounts of lactic acid, which reduces skeletal muscle fatigue during intense physical activity.[77]
The circulatory system of pinnipeds is large and elaborate; retia mirabilia line the inside of the trunk and limbs, allowing for greater oxygen storage during diving.[78] As with other diving mammals, pinnipeds have large amounts of hemoglobin and myoglobin stored in their blood and muscles. This allows them to stay submerged for long periods of time while still having enough oxygen. Deep-diving species such as elephant seals have blood volumes that represent up to 20% of their body weight. When diving, they reduce their heart rate, and blood flow is mostly restricted to the heart, brain and lungs. To keep their blood pressure stable, phocids have an elastic aorta that dissipates some of the energy of each heartbeat.[77]
Thermoregulation
Pinnipeds keep warm by having large, thick bodies, insulating blubber and fur, and quick-burning metabolism.[79] In addition, the blood vessels in their flippers are adapted for countercurrent exchange; small veins surround arteries transporting blood from the body core, capturing heat from them.[80] While blubber and fur keep the seal warm in water, they can also overheat the animal when it is on land. To counteract overheating, many species cool off by covering themselves in sand. Monk seals may even dig up the cooler layers. The northern fur seal cools off by panting.[81]
Sleep
Pinnipeds spend many months at a time at sea, so they must sleep in the water. Scientists have recorded them sleeping for minutes at a time while slowly drifting downward in a belly-up orientation.[82] Like other marine mammals, seals sleep in water with half of their brain awake so that they can detect and escape from predators, as well as surface for air without fully waking. When they are asleep on land, both sides of their brain go into sleep mode.[83]
Living pinnipeds are widespread in cold oceanic waters; particularly in the North Atlantic, the North Pacific and the Southern Ocean. By contrast, the consistently warm Indomalayan waters have no seals.[84] Monk seals and some otariids live in tropical and subtropical waters. Seals usually require cool, nutrient-rich waters with temperatures lower than 20 °C (68 °F). Even in more tropical climates, lower temperatures and biological productivity may be provided by currents.[84][85] Only monk seals live in waters that generally lack these features.[84] The Caspian seal and Baikal seal are found in large landlocked bodies of water (the Caspian Sea and Lake Baikal respectively).[13]
As a whole, pinnipeds can be found in a variety of aquatic habitats, mostly coastal water, but also open ocean, deep waters near offshore islands, brackish waters and even freshwater lakes and rivers. The Baikal seal is the only exclusively freshwater species.[86] Pinnipeds also use a number of terrestrial habitats and substrates, both continental and island. In non-polar regions, they haul out on to rocky shores, sandy and pebble beaches, sandbanks, tidal flats or pools, and in sea caves. Some species also rest on man-made structures built along the coast or offshore. Pinnipeds may move further from the water using sand dunes or vegetation, or even rocky cliffs.[87] New Zealand sea lions may travel to forests 2 kilometres (1.2 mi) from the ocean.[88] In polar regions, seals haul out on to both fast ice and drift ice. Some even den underneath the ice, particularly in pressure ridges and crevasses.[89]