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Anonymous 2007

Created By: Jessica Khalili

[1] Family: Mustelidae, Weasels

[2] Description The only fully aquatic carnivore, and one of the smallest marine mammals, with plush fur, pawlike hands, and flipper-like feet. Tail is flattened dorso-ventrally. Noses of females are often scarred from aggressive males.

Dimensions 1.3-1.4m, 36cm, 18.0-45.0kg; / 1.1-1.4m, 27cm, 11.0-33.0kg 

[3] Endangered Status The Southern Sea Otter, a subspecies of the Sea Otter, is on the U.S. Endangered Species List. It is classified as threatened in California. Once an abundant species, the Sea Otter was so heavily hunted for its highly prized pelt that by 1911, when an international treaty forbade its massacre, it had nearly become extinct. The animal was not seen in California for many years, but in the spring of 1938, a herd appeared in the sea south of Carmel. Today the population there is perhaps 2,000. The southeast Alaska-Washington population seems to be holding steady, with the exception of the region where the Exxon Valdez oil spill wiped out thousands. The very large herds found in the Aleutian Islands have lost some 70 percent of their numbers in recent years, and the Aleutian population is now a candidate species for endangered status. Killer Whales are believed to be the culprits, feeding on Sea Otters because their traditional prey species, the Northern Sea Lion, has become rarer. There is an ongoing controversy between fishermen and conservationists concerning the Southern Sea Otter. Conservationists want to keep the animal on the Endangered Species List to ensure its protection, but fishermen want to control the Sea Otter in order to limit damage to abalone populations.

Breeding Females breed at about 4 years and have a single young annually after a gestation period of about 6 months. 

[4] Habitat Beaches, shorelines & estuaries, Offshore waters

Range California, Northwest, Western Canada, Alaska

Discussion Forages solitarily (females with their pups), but often rests and socializes in groups called “rafts” that are readily observable from shore. Rafts in south are small (fewer than 12) but hundreds of males may congregate in the north. Foraging dives last from a few seconds to 4 minutes, and prey items are brought to the surface to eat. Sea Otters typically float on their back and handle invertebrate prey on their belly, using rocks as tools to open hard invertebrates. Recovering from massive hunting at turn of century, still threatened. Lives in shallow coastal waters.
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Anonymous 2006

Created By: Jessica Khalili

1) Query: I am on another story hunt - I am looking for otter stories that will go with my new Folkmanis River otter puppet. Have not been having an easy time of finding them on line - the stories are proving to be as slippery as the mammel they represent.

Cathy M. 9/28/06


a) There is a wonderful story called "The Otter's Children" in Stories for Telling by William R. White.

Yvonne Y. 9/29/06

b) I found a few references online you might want to check out. On one site of Thailand Law there was this reference: There were two otters who were close friends. They lived in a big river and always shared their food with each other. But once, one otter became greedy and did not want to share a fish, which he had caught, with his friend in a just manner. The argument arose between the friends, how much the one who caught the fish should share with his friend. Before, they had equal shares. But now, the first otter was willing to give only an insignificant part. At the time of the quarrel, a fox was passing by. They appealed to the fox to adjudicate the dispute. The fox first denied help, saying that he was busy and goes to the court of the king to make decisions. But eventually, he consented, providing that the parties to the dispute agree to be bound by the fox's decision. The otters agreed. The fox, then, gave the head of the fish to the one who caught it, and the tail to the other, leaving the rest for himself, and went his way. The otters felt sorry and concluded that it would have been better for them to settle the dispute by themselves.

I suspect this is the same story in this book by Sharon Creeden: "Indian Otters and the Fox" 79 Fair Is Fair 398/Creeden

And chapter eight in the books makes reference to otters. Half Human, Half Animal, Volume 2: More Tales of Werewolves and Related Creatures is a nonfiction book containing folklore from all over the world. It also includes extensive directories to werewolf (and other human-transforming-to-animal) novels, movies and pop culture miscellanea. It is aimed at an adult audience. Chaper 8 Other Mammals- Lore from Ireland, America, Switzerland, Malaysia, China, Japan, Rwanda, Uganda, Burundi, Cameroon, and Kenya. Werebeasts mentioned include badgers, weasels, wolverines, polecats, otters, and monkeys. This section has 7 legends.

c) There are many legends about the sea otter on the Northwest Coast. Here is a short tale, taken from the tag off of a Folkmanis puppet, "How Sea Otter Came to Be."


[1] There was once a lovely young woman who had a devoted brother. They lived in a village by the sea near the cliff dwelling of the powerful Bird Spirit of the north. One day, the Spirit came to the maiden and lured her to his nest to be his wife. There she remained, lonely and frightened, until, one night, her brother rescued her and brought her home. Furious at his loss, the Spirit then sent a raging blizzard to destroy the village huts, so that the villagers were forced to cast brother and sister out into the storm. They made their way to the coast to hide, but there a huge wave swept them out to sea. They wold have drowned, if the Sea Goddess had not taken pity on them. As it was, she turned them into graceful sea creatures, and gave them the gift of the thickest coat of all animals so that they would never be cold in the icy ocean. And that is how sea otters were created. The sister went east and began the otter clans that we know; the brother went west to start the otter herds of Siberia. If an otter, raised out of the water, watches you in your kayak, with a playful glint in its shining eyes, greet it kindly, for it is one of your furred brothers or sisters of the sea.

Adapted from a folktale of the Aleutian Islands.
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Anonymous 2012

Created By: Jessica Khalili

Sea Otter

[1] The sea otter (Enhydra lutris) is a marine mammal native to the coasts of the northern and eastern North Pacific Ocean. Adult sea otters typically weigh between 14 and 45 kg (30 to 100 lb), making them the heaviest members of the weasel family, but among the smallest marine mammals. Unlike most marine mammals, the sea otter's primary form of insulation is an exceptionally thick coat of fur, the densest in the animal kingdom. Although it can walk on land, the sea otter lives mostly in the ocean. 

[2] The sea otter inhabits offshore environments where it dives to the sea floor to forage. It preys mostly upon marine invertebrates such as sea urchins, various molluscs and crustaceans, and some species of fish. Its foraging and eating habits are noteworthy in several respects. First, its use of rocks to dislodge prey and to open shells makes it one of the few mammal species to use tools. In most of its range, it is a keystone species, controlling sea urchin populations which would otherwise inflict extensive damage to kelp forest ecosystems. Its diet includes prey species that are also valued by humans as food, leading to conflicts between sea otters and fisheries. 

[3] Sea otters, whose numbers were once estimated at 150,000–300,000, were hunted extensively for their fur between 1741 and 1911, and the world population fell to 1,000–2,000 individuals in a fraction of their historic range.[2] A subsequent international ban on hunting, conservation efforts, and reintroduction programs into previously populated areas have contributed to numbers rebounding, and the species now occupies about two-thirds of its former range. The recovery of the sea otter is considered an important success in marine conservation, although populations in the Aleutian Islands and California have recently declined or have plateaued at depressed levels. For these reasons the sea otter remains classified as an endangered species. 

[4] Kingdom: Animalia
Phylum: Chordata
Subphylum: Vertebrata
Class: Mammalia
Order: Carnivora
Family: Mustelidae
Subfamily: Lutrinae
Genus: Enhydra
Fleming, 1828
Species: E. lutris


The first scientific description of the sea otter is contained in the field notes of Georg Steller from 1751, and the species was described by Linnaeus in his Systema Naturae of 1758.[3] Originally named Lutra marina, it underwent numerous name changes before being accepted as Enhydra lutris in 1922.[4] [5] The generic name Enhydra, derives from the Ancient Greek en/εν "in" and hydra/ύδρα "water",[5] meaning "in the water", and the Latin word lutris, meaning "otter". [6] It was formerly sometimes referred to as the "sea beaver",[7] although it is only distantly related to beavers. It is not to be confused with the marine otter, a rare otter species native to the southern west coast of South America. A number of other otter species, while predominantly living in fresh water, are commonly found in marine coastal habitats. The extinct sea mink of northeast North America is another mustelid that adapted to a marine environment.


[6] The sea otter is the heaviest member of the family Mustelidae,[8][9] a diverse group that includes the thirteen otter species and terrestrial animals such as weasels, badgers, and minks. It is unique among the mustelids in not making dens or burrows, in having no functional anal scent glands,[10] and in being able to live its entire life without leaving the water.[11] The only member of the genus Enhydra, the sea otter is so different from other mustelid species that as recently as 1982, some scientists believed it was more closely related to the earless seals.[12] Genetic analysis indicates that the sea otter and its closest extant relatives, which include the African speckle-throated otter, Eurasian otter, African clawless otter and oriental small-clawed otter, shared an ancestor approximately 5 million years ago (mya).[13]

Fossil evidence indicates that the Enhydra lineage became isolated in the North Pacific approximately 2 mya, giving rise to the now-extinct Enhydra macrodonta and the modern sea otter, Enhydra lutris.[4] The sea otter evolved initially in northern Hokkaidō and Russia, and then spread east to the Aleutian Islands, mainland Alaska, and down the North American coast.[14] In comparison to cetaceans, sirenians, and pinnipeds, which entered the water approximately 50 mya, 40 mya, and 20 mya, respectively, the sea otter is a relative newcomer to a marine existence.[15] In some respects, however, the sea otter is more fully aquatically adapted than pinnipeds, which must haul out on land or ice to give birth.[16]


There are three recognized subspecies, which vary in body size and in some skull and dental characteristics.

The reintroduction effort off the Oregon coast was not successful. However, reintroductions in 1969 and 1970 off the Washington coast were very successful and sea otters have been expanding their range since. They have now entered the Strait of Juan de Fuca and can be found almost as far east as Pillar Point. Individuals have even been seen in the San Juan Islands and northern Puget Sound.

Physical Characteristics

[7] The sea otter is one of the smallest marine mammal species but is the heaviest mustelid.[11] Male sea otters usually 22 to 45 kg (49 to 99 lb) and are 1.2 to 1.5 m (4 to 5 ft) in length, though specimens to 54 kg (119 lb) have been recorded.[21] Females are smaller, weighing 14 to 33 kg (30 to 73 lb) and measuring 1.0 to 1.4 m (3 ft 3 in to 4 ft 7 in) in length.[22] Its baculum is, for the male otter's size, very large, massive and bent upwards, measuring 150 mm (6 in) in length and 15 mm wide (0.6 in) at the base.[23] 

[8] Unlike most other marine mammals, the sea otter has no blubber and relies on its exceptionally thick fur to keep warm.[24] With up to 150,000 strands of hair per square centimeter (nearly one million per sq in), its fur is the most dense of any animal.[25] The fur consists of long waterproof guard hairs and short underfur; the guard hairs keep the dense underfur layer dry. Cold water is thus kept completely away from the skin and heat loss is limited.[22] The fur is thick year-round, as it is shed and replaced gradually rather than in a distinct molting season.[26] As the ability of the guard hairs to repel water depends on utmost cleanliness, the sea otter has the ability to reach and groom the fur on any part of its body, taking advantage of its loose skin and an unusually supple skeleton.[27] The coloration of the pelage is usually deep brown with silver-gray speckles, but it can range from yellowish or grayish brown to almost black.[28] In adults, the head, throat, and chest are lighter in color than the rest of the body.[28] 

[9] The sea otter displays numerous adaptations to its marine environment. The nostrils and small ears can close.[29] The hind feet, which provide most of its propulsion in swimming, are long, broadly flattened, and fully webbed.[30] The fifth digit on each hind foot is longest, facilitating swimming while on its back, but making walking difficult.[31] The tail is fairly short, thick, slightly flattened, and muscular. The front paws are short with retractable claws, with tough pads on the palms that enable gripping slippery prey.[32] 

[10] The sea otter propels itself underwater by moving the rear end of its body, including its tail and hind feet, up and down,[30] and is capable of speeds of up to 9 km/h (5.6 mph).[8] When underwater, its body is long and streamlined, with the short forelimbs pressed closely against the chest.[33] When at the surface, it usually floats on its back and moves by sculling its feet and tail from side to side.[34] At rest, all four limbs can be folded onto the torso to conserve heat, whereas on particularly hot days the hind feet may be held underwater for cooling.[35] The sea otter's body is highly buoyant because of its large lung capacity – about 2.5 times greater than that of similar-sized land mammals[36] – and the air trapped in its fur. The sea otter walks with a clumsy rolling gait on land, and can run in a bounding motion.[31]

Long, highly sensitive whiskers and front paws help the sea otter find prey by touch when waters are dark or murky.[11] Researchers have noted that when they approach in plain view, sea otters react more rapidly when the wind is blowing towards the animals, indicating that the sense of smell is more important than sight as a warning sense.[37] Other observations indicate that the sea otter's sense of sight is useful above and below the water, although not as good as that of seals.[38] Its hearing is neither particularly acute nor poor.[39] 

[11] An adult's 32 teeth, particularly the molars, are flattened and rounded, designed to crush rather than cut food.[40] Seals and sea otters are the only carnivores with two pairs of lower incisor teeth rather than three.

[12] The sea otter has a metabolic rate two or three times that of comparatively sized terrestrial mammals. It must eat an estimated 25 to 38% of its own body weight in food each day in order to burn the calories necessary to counteract the loss of heat due to the cold water environment.[43][44] Its digestive efficiency is estimated at 80 to 85%,[45] and food is digested and passed in as little as three hours.[24] Most of its need for water is met through food, although, in contrast to most other marine mammals, it also drinks seawater. Its relatively large kidneys enable it to derive fresh water from sea water and excrete concentrated urine.[46]


The sea otter is diurnal. It has a period of foraging and eating in the morning, starting about an hour before sunrise, then rests or sleeps in mid-day.[47] Foraging resumes for a few hours in the afternoon and subsides before sunset, and there may be a third foraging period around midnight.[47] Females with pups appear to be more inclined to feed at night.[47] Observations of the amount of time a sea otter must spend each day foraging range from 24 to 60%, apparently depending on the availability of food in the area.[48] 

[13] The sea otter spends much of its time grooming, which consists of cleaning the fur, untangling knots, removing loose fur, rubbing the fur to squeeze out water and introduce air, and blowing air into the fur. To an observer it appears as if the animal is scratching, however sea otters are not known to have lice or other parasites in the fur.[49] When eating, the sea otter rolls in the water frequently, apparently to wash food scraps from its fur.[50]


[14] The sea otter hunts in short dives, often to the sea floor. Although it can hold its breath for up to five minutes,[29] its dives typically last about one minute and no more than four.[22] It is the only marine animal capable of lifting and turning over boulders, which it often does with its front paws when searching for prey.[50] The sea otter may also pluck snails and other organisms from kelp and dig deep into underwater mud for clams.[50] It is the only marine mammal that catches fish with its forepaws rather than with its teeth.[24] 

[15] Under each foreleg, the sea otter has a loose pouch of skin that extends across the chest. In this pouch (preferentially the left one), the animal stores collected food to bring to the surface. In this pouch they also keep a rock unique to each otter that is used to break open shellfish and clams.[51] There, the sea otter eats while floating on its back, using its forepaws to tear food apart and bring it to its mouth. It can chew and swallow small mussels with their shells, whereas large mussel shells may be twisted apart.[52] It uses its lower incisor teeth to access the meat in shellfish.[53] To eat large sea urchins, which are mostly covered with spines, the sea otter bites through the underside where the spines are shortest, and licks the soft contents out of the urchin's shell.[52] 

[16] The sea otter's use of rocks when hunting and feeding makes it one of the few mammal species to use tools.[54] To open hard shells, it may pound its prey with both paws against a rock on its chest. To pry an abalone off its rock, it hammers the abalone shell using a large stone, with observed rates of 45 blows in 15 seconds.[22] Releasing an abalone, which can cling to rock with a force equal to 4,000 times its own body weight, requires multiple dives.[22]

Social Structure

Although each adult and independent juvenile forages alone, sea otters tend to rest together in single-sex groups called rafts. A raft typically contains 10 to 100 animals, with male rafts being larger than female ones.[56] The largest raft ever seen contained over 2000 sea otters. To keep from drifting out to sea when resting and eating, sea otters may wrap themselves in kelp.[57]

A male sea otter is most likely to mate if he maintains a breeding territory in an area that is also favored by females.[58] As autumn is the peak breeding season in most areas, males typically defend their territory only from spring to autumn.[58] During this time, males patrol the boundaries of their territories to exclude other males,[58] although actual fighting is rare.[56] Adult females move freely between male territories, where they outnumber adult males by an average of five to one.[58] Males who do not have territories tend to congregate in large male-only groups,[58] and swim through female areas when searching for a mate.[59]

The species exhibits a variety of vocal behaviors. The cry of a pup is often compared to that of a seagull.[60] Females coo when they are apparently content; males may grunt instead.[61] Distressed or frightened adults may whistle, hiss, or in extreme circumstances, scream.[60]

Although sea otters can be playful and sociable, they are not considered to be truly social animals.[62] They spend much time alone, and each adult can meet its own needs in terms of hunting, grooming, and defense.[62]

Reproduction and Lifestyle

[17] Sea otters are polygynous: males have multiple female partners. However, temporary pair-bonding occurs for a few days between a female in estrus and her mate.[50] Mating takes place in the water and can be rough, the male biting the female on the muzzle – which often leaves scars on the nose – and sometimes holding her head under water.[8][63]

Births occur year-round, with peaks between May and June in northern populations and between January and March in southern populations.[64] Gestation appears to vary from four to twelve months, as the species is capable of delayed implantation followed by four months of pregnancy.[64] In California, sea otters usually breed every year, about twice as often as sea otters in Alaska.[65] 

Birth usually takes place in the water and typically produces
a single pup weighing 1.4 to 2.3 kg (3 to 5 lb).[66] Twins occur in 2% of births; however, usually only one pup survives.[8] At birth, the eyes are open, ten teeth are visible, and the pup has a thick coat of baby fur.[67] Mothers have been observed to lick and fluff a newborn for hours; after grooming, the pup's fur retains so much air that the pup floats like a cork and cannot dive.[68] The fluffy baby fur is replaced by adult fur after about thirteen weeks.[3]

Nursing lasts six to eight months in Californian populations and four to twelve months in Alaska, with the mother beginning to offer bits of prey at one to two months.[70] The milk from a sea otter's two abdominal nipples is rich in fat and more similar to the milk of other marine mammals than to that of other mustelids.[71] A pup, with guidance from its mother, practices swimming and diving for several weeks before it is able to reach the sea floor. Initially the objects it retrieves are of little food value, such as brightly colored starfish and pebbles.[51] Juveniles are typically independent at six to eight months, however a mother may be forced to abandon a pup if she cannot find enough food for it[72] and at the other extreme, a pup may nurse until it is almost adult size.[66] Pup mortality is high, particularly during an individual's first winter – by one estimate, only 25% of pups survive their first year.[72] Pups born to experienced mothers have the highest survival rates.[73] 

[18] Females perform all tasks of feeding and raising offspring, and have occasionally been observed caring for orphaned pups.[74] Much has been written about the level of devotion of sea otter mothers for their pups – a mother gives her infant almost constant attention, cradling it on her chest away from the cold water and attentively grooming its fur.[75] When foraging, she leaves her pup floating on the water, sometimes wrapped in kelp to keep it from floating away;[76] if the pup is not sleeping, it cries loudly until she returns.[77] Mothers have been known to carry their pup for days after the pup's death.[69]

Females become sexually mature at around three or four years of age and males at around five; however, males often do not successfully breed until a few years later.[78] A captive male sired offspring at age 19.[66] In the wild, sea otters live to a maximum age of 23 years,[22] with average lifespans of 10–15 years for males and 15–20 years for females.[79] Several captive individuals have lived past 20 years, and a female at the Seattle Aquarium died at the age of 28 years.[80] Sea otters in the wild often develop worn teeth, which may account for their apparently shorter lifespans.

Population and Distribution

[19] Sea otters live in coastal waters 15 to 23 meters (50 to 75 ft) deep,[82] and usually stay within a kilometer (⅔ mi) of the shore.[83] They are found most often in areas with protection from the most severe ocean winds, such as rocky coastlines, thick kelp forests, and barrier reefs.[84] Although they are most strongly associated with rocky substrates, sea otters can also live in areas where the sea floor consists primarily of mud, sand, or silt.[85] Their northern range is limited by ice, as sea otters can survive amidst drift ice but not land-fast ice.[86] Individuals generally occupy a home range a few kilometers long, and remain there year-round. 

The sea otter population is thought to have once been 150,000 to 300,000,[7] stretching in an arc across the North Pacific from northern Japan to the central Baja California Peninsula in Mexico. The fur trade that began in the 1740s reduced the sea otter's numbers to an estimated 1,000 to 2,000 members in thirteen colonies. In about two-thirds of its former range, the species is at varying levels of recovery, with high population densities in some areas and threatened populations in others. Sea otters currently have stable populations in parts of the Russian east coast, Alaska, British Columbia, Washington, and California, and there have been reports of recolonizations in Mexico and Japan.[88] Population estimates made between 2004 and 2007 give a worldwide total of approximately 107,000 sea otters.


Currently, the most stable and secure part of the sea otter's range is Russia.[93] Before the 19th century there were around 20,000 to 25,000 sea otters in the Kuril Islands, with more on Kamchatka and the Commander Islands. After the years of the Great Hunt, the population in these areas, currently part of Russia, was only 750.[89] As of 2004, sea otters have repopulated all of their former habitat in these areas, with an estimated total population of about 27,000. Of these, about 19,000 are in the Kurils, 2000 to 3500 on Kamchatka and another 5000 to 5500 on the Commander Islands.[89] Growth has slowed slightly, suggesting that the numbers are reaching carrying capacity.[89]


Alaska is the heartland of the sea otter's range. In 1973, the sea otter population in Alaska was estimated at between 100,000 and 125,000 animals.[94] By 2006, however, the Alaska population had fallen to an estimated 73,000 animals.[90] A massive decline in sea otter populations in the Aleutian Islands accounts for most of the change; the cause of this decline is not known, although orca predation is suspected.[95] The sea otter population in Prince William Sound was also hit hard by the Exxon Valdez oil spill, which killed thousands of sea otters in 1989.[50]

British Columbia and Washington

Along the North American coast south of Alaska, the sea otter's range is discontinuous. Although a remnant population of sea otter survived off Vancouver Island into the twentieth century, it died out despite the 1911 international protection treaty, with the last sea otter taken near Kyuquot in 1929. From 1969 to 1972, 89 sea otters were flown or shipped from Alaska to the west coast of Vancouver Island. This population expanded to over 3,000 as of 2004, and their range on the island's west coast expanded from Cape Scott in the north to Barkley Sound to the south.[96] In 1989, a separate colony was discovered in the central British Columbia coast. It is not known if this colony, which had a size of about 300 animals in 2004, was founded by transplanted otters or by survivors of the fur trade.[91]

In 1969 and 1970, 59 sea otters were translocated from Amchitka Island to Washington. Annual surveys between 2000 and 2004 have recorded between 504 and 743 individuals, and their range is in the Olympic Peninsula from just south of Destruction Island to Pillar Point.[3]

In British Columbia and Washington, sea otters are found almost exclusively on the outer coasts. They can swim as close as 6 feet off shore along the Olympic coast. Reported sightings of sea otters in the San Juan Islands and Puget Sound almost always turn out to be northern river otters which are commonly seen along the seashore. However, biologists have confirmed isolated sightings of sea otters in these areas since the mid-1990s.[3]


The spring 2007 sea otter survey counted 3,026 sea otters in the central Californian coast, down from an estimated pre-fur trade population of 16,000.[92][97] California's sea otters are the descendants of a single colony of about 50 southern sea otters discovered near Big Sur in 1938;[98] their principal range is now from just south of San Francisco to Santa Barbara County.[97] In the late 1980s, the U.S. Fish and Wildlife Service relocated about 140 Californian sea otters to San Nicolas Island in southern California, in the hope of establishing a reserve population should the mainland be struck by an oil spill. To the surprise of biologists, the San Nicholas population initially shrank as the animals migrated back to the mainland.[99] As of 2005, only 30 sea otters remained at San Nicholas,[100] thriving on the abundant prey around the island.[99] The plan that authorized the translocation program had predicted that carrying capacity would be reached within 5 to 10 years.

When the Fish and Wildlife Service implemented the translocation program, it also attempted to implement "zonal management" of the Californian population. To manage the competition between sea otters and fisheries, it declared an "otter-free zone" stretching from Point Conception to the Mexican border. In this zone, only San Nicolas Island was designated as sea otter habitat, and sea otters found elsewhere in the area were supposed to be captured and relocated. These plans were abandoned after it proved impractical to capture the hundreds of otters which ignored regulations and swam into the zone.[101] However, after engaging in a period of public commentary in 2005, the Fish and Wildlife Service has yet to release a formal decision on the issue.[100]

Sea otters were once numerous in San Francisco Bay.[102] Historical records reveal that the Russian-American Company snuck Aleuts into San Francisco Bay multiple times, despite the Spanish capturing or shooting them while hunting sea otters in the estuaries of San Jose, San Mateo, San Bruno and around Angel Island.[103] The founder of Fort Ross, Ivan Kuskov, finding otter scarce on his second voyage to Bodega Bay in 1812, sent a party of Aleuts to San Francisco Bay where they met another Russian party and an American party, and caught 1,160 sea otters in three months.[104] By 1817 sea otters in the area were practically eliminated and the Russians sought permission from the Spanish and the Mexican governments to hunt further and further south of San Francisco.[105] Remnant sea otter populations may have survived in the bay until 1840, when the Rancho Punta de Quentin was granted to Captain John B. R. Cooper, a sea captain from Boston, by Mexican Governor Juan Bautista Alvarado along with a license to hunt sea otters, reportedly then prevalent at the mouth of Corte Madera Creek.[106]

Although the southern sea otter's range has continuously expanded from the remnant population of about 50 individuals in Big Sur since protection in 1911, in the last two years the otter population and its range have contracted.[107] As of spring 2010 the northern boundary has moved from about Tunitas Creek to a point 2 km southeast of Pigeon Point, and the southern boundary has moved from approximately Coal Oil Point to Gaviota State Park.[108] Recently a toxin called microcystin, produced by a type of cyanobacteria (Microcystis), seems to be concentrated in the shellfish that otters eat, poisoning them. Cyanobacteria are found in stagnant freshwater enriched with nitrogen and phosphorus from septic tank and agricultural fertilizer runoff, and may be flushed into the ocean when streamflows are high in the rainy season.[109][110] A record number of sea otter carcasses were found on California's coastline in 2010, with increased shark attacks an increasing component of the mortality.[111]

Otters were observed twice in Southern California in 2011, once near Laguna Beach and once at Zuniga Point Jetty, near San Diego. These are the first documented sightings of otters this far south in 30 years.[112]


The last native sea otter in Oregon was probably shot and killed in 1906. In 1970 and 1971, a total of 95 sea otters were transplanted from Amchitka Island, Alaska to the Southern Oregon coast. However, this translocation effort failed and otters soon again disappeared from the state.[113]

In 2004 a lone male sea otter took up residence at Simpson Reef off of Cape Arago for six months. This male is thought to have originated from a colony in Washington, but disappeared after a coastal storm.[114]

The most recent sighting of a sea otter off the Oregon coast took place 18 February 2009, in Depoe Bay, Oregon. The lone male sea otter could have traveled from either California or Washington.



[20] Sea otters consume over 100 different prey species.[116] In most of its range, the sea otter's diet consists almost exclusively of marine invertebrates, including sea urchins, a variety of bivalves such as clams and mussels, abalone, other mollusks, crustaceans, and snails.[116] Its prey ranges in size from tiny limpets and crabs to giant octopuses.[116] Where prey such as sea urchins, clams, and abalone are present in a range of sizes, sea otters tend to select larger items over smaller ones of similar type.[116] In California, it has been noted that sea otters ignore Pismo clams smaller than 3 inches (7 cm) across.[117]

In a few northern areas, fish are also eaten. In studies performed at Amchitka Island in the 1960s, where the sea otter population was at carrying capacity, 50% of food found in sea otter stomachs was fish.[118] The fish species were usually bottom-dwelling and sedentary or sluggish forms, such as Hemilepidotus hemilepidotus and family Tetraodontidae.[118] However, south of Alaska on the North American coast, fish are a negligible or extremely minor part of the sea otter's diet.[3][119] Contrary to popular depictions, sea otters rarely eat starfish, and any kelp that is consumed apparently passes through the sea otter's system undigested.[120]

The individuals within a particular area often differ in their foraging methods and their prey types, and tend to follow the same patterns as their mothers.[121] The diet of local populations also changes over time, as sea otters can significantly deplete populations of highly preferred prey such as large sea urchins, and prey availability is also affected by other factors such as fishing by humans.[3] Sea otters can thoroughly remove abalone from an area except for specimens in deep rock crevices,[122] however, they never completely wipe out a prey species from an area.[123] A 2007 Californian study demonstrated that in areas where food was relatively scarce, a wider variety of prey was consumed. However, surprisingly, the diets of individuals were more specialized in these areas than in areas where food was plentiful.[99]

As A Keystone Species

[21] Sea otters are a classic example of a keystone species; their presence affects the ecosystem more profoundly than their size and numbers would suggest. Sea otters keep the population of certain benthic (sea floor) herbivores, particularly sea urchins, in check. Sea urchins graze on the lower stems of kelp, causing the kelp to drift away and die. Loss of the habitat and nutrients provided by kelp forests leads to profound cascade effects on the marine ecosystem. North Pacific areas that do not have sea otters often turn into urchin barrens, with abundant sea urchins and no kelp forest.[8]

Reintroduction of sea otters to British Columbia has led to a dramatic improvement in the health of coastal ecosystems,[124] and similar changes have been observed as sea otter populations recovered in the Aleutian and Commander Islands and the Big Sur coast of California[125] However, some kelp forest ecosystems in California have also thrived without sea otters, with sea urchin populations apparently controlled by other factors.[125] The role of sea otters in maintaining kelp forests has been observed to be more important in areas of open coast than in more protected bays and estuaries.[125]

In addition to promoting growth of kelp forests, sea otters can also have a profound effect in rocky areas that tend to be dominated by mussel beds. They remove mussels from rocks, liberating space for competitive species and thereby increasing the diversity of species in the area.[125]


Predation of sea otters does occur, although it is not common. Many predators find the otter, with their pungent scent glands, distasteful. Young predators may kill an otter and not eat it. Leading mammalian predators of this species include orcas and sea lions; bald eagles also prey on pups by snatching them from the water surface.[54] On land, young sea otters may face attack from bears and coyotes. In California, bites from sharks, particularly great white sharks, have been estimated to cause 10% of sea otter deaths and are one of the reasons the population has not expanded further north.[126] It is believed that the great white shark is their primary predator and dead sea otters have been found with injuries from shark bites, although there is no evidence that sharks actually eat them.[126] An exhibit at the San Diego Natural History Museum states that cat feces from urban runoff carries parasites to the ocean and kills sea otters.

Relationship With Humans

Fur Trade

Sea otters have the thickest fur of any mammal. Their beautiful fur is a main target for many hunters. Archaeological evidence indicates that for thousands of years, indigenous peoples have hunted sea otters for food and fur.[7] Large-scale hunting, part of the Maritime Fur Trade, which would eventually kill approximately one million sea otters, began in the 18th century when hunters and traders began to arrive from all over the world to meet foreign demand for otter pelts, which were one of the world's most valuable types of fur.[7]

In the early 18th century, Russians began to hunt sea otters in the Kuril Islands[7] and sold them to the Chinese at Kyakhta. Russia was also exploring the far northern Pacific at this time, and sent Vitus Bering to map the Arctic coast and find routes from Siberia to North America.[127] In 1741, on his second North Pacific voyage, Bering was shipwrecked off Bering Island in the Commander Islands, where Bering and many of his crew died.[127] The surviving crew members, which included naturalist Georg Steller, discovered sea otters on the beaches of the island and spent the winter hunting sea otters and gambling with otter pelts.[127] They returned to Siberia having killed nearly 1000 sea otters, and were able to command high prices for the pelts.[127] Thus began what is sometimes called the "Great Hunt", which would continue for another hundred years. The Russians found the sea otter far more valuable than the sable skins that had driven and paid for most of their expansion across Siberia. If the sea otter pelts brought back by Bering's survivors had been sold at Kyakhta prices they would have paid for one tenth the cost of Bering's expedition[128]. In 1775 at Okhotsk sea otter pelts were worth 50-80 rubles as opposed to 2.5 rubles for sable.

Russian fur-hunting expeditions soon depleted the sea otter populations in the Commander Islands, and by 1745 they began to move on to the Aleutian Islands. The Russians initially traded with the Aleuts inhabitants of these islands for otter pelts, but later enslaved the Aleuts, taking women and children hostage and torturing and killing Aleut men to force them to hunt. Many Aleuts were either murdered by the Russians or died from diseases that the hunters had introduced.[130] The Aleut population was reduced, by the Russians' own estimate, from 20,000 to 2,000.[131] By the 1760s, the Russians had reached Alaska. In 1799, Emperor Paul I consolidated the rival fur hunting companies into the Russian-American Company, granting it an Imperial charter and protection, and a monopoly over trade rights and territorial acquisition. Under Aleksandr I the administration of the merchant-controlled Company was transferred to the Imperial Navy, largely due to the alarming reports by naval officers of native abuse, and in 1818 the indigenous peoples of Alaska were granted civil rights equivalent to a townsman status in the Russian Empire.[132]

Other nations joined in the hunt in the south. Along the coasts of what is now Mexico and California, Spanish explorers bought sea otter pelts from Native Americans and sold them in Asia.[130] In 1778, British explorer Captain James Cook reached Vancouver Island and bought sea otter furs from the First Nations people.[133] When Cook's ship later stopped at a Chinese port, the pelts rapidly sold at high prices, and were soon known as "soft gold". As word spread, people from all over Europe and North America began to arrive in the Pacific Northwest to trade for sea otter furs.[133]

Russian hunting expanded to the south, initiated by American ship captains, who sub-contracted Russian supervisors and Aleut hunters [134] in what is now Washington, Oregon, and California. Between 1803 and 1846, 72 American ships were involved in the otter hunt in California, harvesting an estimated 40,000 skins and tails, compared to only 13 ships of the Russian-American Company, which reported 5,696 otter skins taken between 1806-1846.[135] In 1812 the Russians founded an agricultural settlement at what is now Fort Ross in northern California as their southern headquarters.[133] Eventually, sea otter populations became so depleted that commercial hunting was no longer viable. In the Aleutian Islands, commercial hunting had stopped by 1808, as a conservation measure imposed by the Russian-American Company.[136] Further restrictions were ordered by the Company in 1834.[136] When Russia sold Alaska to the United States in 1867, the Alaska population had recovered to over 100,000, but Americans resumed hunting and quickly extirpated the sea otter again.[137] Prices rose as the species became rare: During the 1880s, a pelt brought $105 to $165 in the London market, however by 1903 a pelt could be worth as much as $1,125.[66] In 1911, Russia, Japan, Great Britain (for Canada) and the United States signed the Treaty for the Preservation and Protection of Fur Seals, imposing a moratorium on the harvesting of sea otters.[138] So few remained, perhaps only 1,000–2,000 individuals in the wild, that many believed the species would become extinct.[3]

Recovery and Conservation

During the 20th century, sea otter numbers rebounded in about two-thirds of their historic range, a recovery that is considered one of the greatest successes in marine conservation.[139] However, the IUCN still lists the sea otter as an endangered species, and describes the significant threats to sea otters as oil pollution, predation by orcas, poaching, and conflicts with fisheries – sea otters can drown if entangled in fishing gear.[1] The hunting of sea otters is no longer legal except for limited harvests by indigenous peoples in the United States.[140] Poaching was a serious concern in the Russian Far East immediately after the collapse of the Soviet Union in 1991, however it has declined significantly with stricter law enforcement and better economic conditions.[93]

The most significant threat to sea otters is oil spills.[54] Sea otters are particularly vulnerable, as they rely on their fur to keep warm. When their fur is soaked with oil, it loses its ability to retain air, and the animal quickly dies from hypothermia.[54] The liver, kidneys, and lungs of sea otters also become damaged after they inhale oil or ingest it when grooming.[54] The Exxon Valdez oil spill of 24 March 1989 killed thousands of sea otters in Prince William Sound, and as of 2006 the lingering oil in the area continues to affect the population.[141] Describing the public sympathy for sea otters that developed from media coverage of the event, a U.S. Fish and Wildlife Service spokesperson wrote:

As a playful, photogenic, innocent bystander, the sea otter epitomized the role of victim ... cute and frolicsome sea otters suddenly in distress, oiled, frightened, and dying, in a losing battle with the oil.[3]
The small geographic ranges of the sea otter populations in California, Washington, and British Columbia mean that a single major spill could be catastrophic for that state or province.[3][44][50] Prevention of oil spills and preparation for the rescue of otters in the event of one are major areas of focus for conservation efforts. Increasing the size and the range of sea otter populations would also reduce the risk of an oil spill wiping out a population.[3] However, because of the species' reputation for depleting shellfish resources, advocates for commercial, recreational, and subsistence shellfish harvesting have often opposed allowing the sea otter's range to increase, and there have even been instances of fishermen and others illegally killing them.[142]

In the Aleutian Islands, a massive and unexpected disappearance of sea otters has occurred in recent decades. In the 1980s, the area was home to an estimated 55,000 to 100,000 sea otters, but the population fell to around 6,000 animals by 2000.[101] The most widely accepted, but still controversial, hypothesis is that orcas have been eating the otters. The pattern of sea otter disappearances is consistent with a rise in orca predation, however there has been no direct evidence that orcas prey on sea otters to any significant extent.[95]

Another area of concern is California, where recovery began to fluctuate or decline in the late 1990s.[143] Unusually high mortality rates amongst adult and sub-adult otters, particularly females, have been reported.[92] Necropsies of dead sea otters indicate that diseases, particularly Toxoplasma gondii infection and acanthocephalan parasite infection, are a major cause of sea otter mortality in California.[144] The Toxoplasma gondii parasite, which is often fatal to sea otters, is carried by wild and domestic cats and by opossums, and may be transmitted by domestic cat droppings flushed into the ocean via the sewage system.[144][145] Although it is clear that disease has contributed to the deaths of many of California's sea otters, it is not known why the Californian population is apparently more affected by disease than populations in other areas.[144]

Sea otter habitat is preserved through several protected areas in the United States, Russia and Canada. In marine protected areas, polluting activities such as dumping of waste and oil drilling are typically prohibited.[146] There are estimated to be more than 1,200 sea otters within the Monterey Bay National Marine Sanctuary, and more than 500 within the Olympic Coast National Marine Sanctuary.[147][148]

Economic Impact

Some of the sea otter's preferred prey species, particularly abalone, clams, and crabs, are also food sources for humans. In some areas, massive declines in shellfish harvests have been blamed on the sea otter, and intense public debate has taken place over how to manage the competition between sea otters and humans for seafood.[149]

The debate is complicated by the fact that sea otters have sometimes been held responsible for declines of shellfish stocks that were more likely caused by overfishing by humans, disease, pollution, and seismic activity.[50][150] Shellfish declines have also occurred in many parts of the North American Pacific coast that do not have sea otters, and conservationists sometimes note that the existence of large concentrations of shellfish on the coast is a recent development resulting from the fur trade's near-extirpation of the sea otter.[150] Although many factors affect shellfish stocks, sea otter predation can deplete a fishery to the point that it is no longer commercially viable.[149] There is a consensus among scientists that sea otters and abalone fisheries cannot co-exist in the same area,[149] and the same is likely true for certain other types of shellfish as well.[101]

There are many facets to the interaction between sea otters and the human economy that are not as immediately felt. Sea otters have been credited with contributing to the kelp harvesting industry via their well-known role in controlling sea urchin populations; kelp is used in the production of diverse food and pharmaceutical products.[151] Although human divers harvest red sea urchins both for food and to protect the kelp, sea otters hunt more sea urchin species and are more consistently effective in controlling these populations.[152] The health of the kelp forest ecosystem is significant in nurturing populations of fish, including commercially important fish species.[151] In some areas, sea otters are a popular tourist attraction, bringing visitors to local hotels, restaurants, and sea otter-watching expeditions.

Role In Human Cultures

For many maritime indigenous cultures throughout the North Pacific, especially the Ainu in the Kuril Islands, the Koryaks and Itelmen of Kamchatka, the Aleut in the Aleutian Islands and a host of tribes on the Pacific coast of North America, the sea otter has played an important role as a cultural as well as material resource. [22]  In these cultures, many of which have strongly animist traditions full of legends and stories in which many aspects of the natural world are associated with spirits, the sea otter was considered particularly kin to humans. The Nuu-chah-nulth, Haida, and other First Nations of coastal British Columbia used the warm and luxurious pelts as chiefs' regalia. Sea otter pelts were given in potlatches to mark coming-of-age ceremonies, weddings, and funerals.[55] The Aleuts carved sea otter bones for use as ornaments and in games, and used powdered sea otter baculum as a medicine for fever.

[23] Among the Ainu, the otter is portrayed as an occasional messenger between humans and the creator.[155] The sea otter is a recurring figure in Ainu folklore. A major Ainu epic, the Kutune Shirka, tells the tale of wars and struggles over a golden sea otter. Versions of a widespread Aleut legend tell of lovers or despairing women who plunge into the sea and become otters.[156] These links have been associated with the many human-like behavioral features of the sea otter, including apparent playfulness, strong mother-pup bonds and tool use, yielding to ready anthropomorphism.[157] The beginning of commercial exploitation had a great impact on the human as well as animal populations – the Ainu and Aleuts have been displaced or their numbers are dwindling, while the coastal tribes of North America, where the otter is in any case greatly depleted, no longer rely as intimately on sea mammals for survival.[158]

Since the mid-1970s, the beauty and charisma of the species have gained wide appreciation, and the sea otter has become an icon of environmental conservation.[143] The round, expressive face and soft furry body of the sea otter are depicted in a wide variety of souvenirs, postcards, clothing, and stuffed toys.

Aquarium And Zoos

Sea otters can do well in captivity, and are featured in over 40 public aquariums and zoos.[160] The Seattle Aquarium became the first institution to raise sea otters from conception to adulthood with the birth of Tichuk in 1979, followed by three more pups in the early 1980s.[161] In 2007, a YouTube video of two sea otters holding paws drew 1.5 million viewers in two weeks, and currently has over 17 million views.[162] Filmed five years previously at the Vancouver Aquarium, it was YouTube's most popular animal video at the time, although it has since been surpassed. The lighter-colored otter in the video is Nyac, a survivor of the 1989 Exxon Valdez oil spill.[163] Nyac died in September 2008, at the age of 20.

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Yeates Et Al 2007

Created By: Jessica Khalili

As the smallest and one of the most recently evolved marine mammals, sea otters face physiological challenges rarely encountered by larger, more derived aquatic species. To examine the effect of these challenges on foraging costs and resultant daily energy budgets, we measured the energetics of resting, grooming, diving and foraging for adult, male sea otters. The energy expended for these different behaviors as determined from open flow respirometry was then standardized across activity budgets measured for wild sea otters to estimate field metabolic rates (FMR). We found that the metabolic rate of captive otters performing single dives ranging in duration from 40 to 192 s was 17.6±0.5 ml O2 kg–1 min–1 and only 1.3 times resting rates. This rate increased significantly if the animals foraged during submergence. The cost of a foraging dive for sea otters was nearly twice that predicted for phocid seals, which was attributed in part to elevated locomotor costs associated with buoyancy and swimming style. Our behavioral studies indicate that wild sea otters spend the greatest proportion of the day feeding and resting, with the largest daily energy expenditure (6.1±1.1 MJ day–1) associated with foraging. The resulting mean FMR for wild sea otters based on the energy expended for all behaviors was 15.7±2.7 MJ day–1 and matched predicted FMR values based upon a regression of known FMR values for other marine mammals across a range of body sizes. This was achieved by counterbalancing elevated foraging costs with prolonged periods of rest on the water surface.

Among mammals, sea otters represent one of the most recent lineages to re-enter the marine environment (Berta and Sumich, 1999). Whereas pinnipeds and cetaceans have maintained aquatic lifestyles for over 50–60 million years, sea otters have been fully aquatic for only 1–3 million years. [1] A consequence of these different evolutionary histories is that sea otters appear to lack some of the more derived adaptations equated with a fully aquatic lifestyle typical of cetaceans and pinnipeds. Such adaptations include insulation in the form of blubber that can also act as an energy store, a well-developed dive response that facilitates oxygen conservation when submerged (Kooyman, 1989), counter-current heat exchangers to retain and dissipate heat through thermal windows (Williams and Worthy, 2002), and enhanced water conserving mechanisms, e.g. complex nasal turbinates (Huntley et al., 1984), reniculated kidneys (Williams and Worthy, 2002). Of these, only the latter two are known for sea otters. In view of this, it is reasonable to presume that marine living may be more energetically challenging for sea otters in comparison to other marine mammal species.

Materials and methods
Study design
This study combined data obtained from both captive and free-ranging sea otters Enhydra lutris Linnaeus 1758. All metabolic measurements, including assessment of aerobic and anaerobic diving costs, were conducted on captive otters at Long Marine Laboratory (University of California at Santa Cruz) from January 2002 to April 2006. Field observations, which were conducted along the central coast of California between March 2001 and July 2003, were designed to evaluate the activity patterns and routine diving parameters (dive frequency and duration) of wild sea otters under free-ranging conditions. All measurements on wild otters were obtained near Point Piedras Blancas. This area of coastline is characterized by dense but patchy kelp forests, strong seasonal upwelling and diverse benthic invertebrate species. The sea otter population in this area has been established since the late 1950s and individuals feed close to shore on sub-tidal and inter-tidal invertebrates (Riedman and Estes, 1991) enabling foraging patterns and activity budgets to be determined visually. Water temperature along the coast ranges from 10°C to 19°C seasonally.

Captive studies
Two adult, male sea otters were used for the metabolic trials (Table 1). Both animals had been in captivity for 1 year prior to training and experimental measurements, and were maintained in outdoor fiberglass holding pools (4.2 m×1.2 m or 6 m×1.5 m; diameter × depth). Fresh seawater was continuously added at a minimum of 227 l min–1. Water temperature varied with ambient ocean temperature along the coast. The captive animals were fed a mixed diet of commercially obtained frozen squid (Loligo opalescens), surf clam (Spisula solidissima), cod (Macruronus novaelandiae) and tiger prawns (Panaeus vannamei) presented in 4–7 meals per day. Diets were supplemented with commercially available live cancer crabs (Cancer spp.), mussels (Mytilus edulis) and clams (Spissula spp). Animals were weighed weekly to the nearest 0.1 kg using a platform scale (Arlyn 320D, Rockaway, NY, USA).

This challenge is especially apparent when evaluating the allocation of energy and the cost of various behaviors performed by sea otters. For example, sea otters exhibit comparatively high resting metabolic rates that range from 2.8 to 3.2 times the levels predicted for a terrestrial mammal of similar size (Iverson, 1972; Morrison et al., 1974; Costa, 1978; Costa and Kooyman, 1982). Although marine mammals generally exhibit higher resting metabolic rates than do terrestrial mammals (Costa and Williams, 1999), even within this group the sea otter represents an extreme. Weddell seals Leptonychotes weddellii (Williams et al., 2004b), grey seals Halichoerus grypus (Sparling and Fedak, 2004), bottlenose dolphins Tursiops truncatus (Williams et al., 2001) and California sea lions Zalophus californianus (Hurley and Costa, 2001) demonstrate resting metabolic rates that average 1.5–2.0 times the levels predicted by Kleiber (Kleiber, 1975) for terrestrial mammals. This difference between predicted and measured rates is approximately half that observed for the sea otter.

Likewise, thermoregulatory costs are comparatively high for the sea otter and are influenced by body size and a terrestrial form of insulation. In general, the magnitude of heat transfer depends upon the surface area-to-volume ratio of the animal, the gradient between core temperature and environmental temperature, and the insulating barrier between the body core and surrounding environment (Dejours, 1987). Compared to larger marine mammals, sea otters have a higher surface area from which to lose heat relative to the tissue volume from which to produce or retain heat. Furthermore, unlike other marine mammals that rely on a thick, internalized blubber layer for insulation, sea otters prevent excessive heat loss to the water through an air layer trapped against the skin by an exceptionally dense fur covering (Tarasoff, 1974; Williams et al., 1992). A potential disadvantage of this form of insulation is compression of the air layer as the otter dives, thereby reducing the insulating quality of fur at depth when the animal forages. Together these features result in elevated thermal energetic costs for sea otters that must be compensated for by activity, shivering or by the heat produced during the processing of food (Costa and Kooyman, 1984).

It follows that sea otters must consume a comparatively large amount of food to meet these elevated energetic demands. Typically, sea otters ingest 20–25% of their body mass in prey items per day (Kenyon, 1969; Costa and Kooyman, 1982) spending 23–50% of the day foraging (Estes et al., 1986; Ralls and Siniff, 1990; Tinker, 2004). In comparison, similarly sized carnivorous terrestrial mammals and larger marine mammals routinely consume 5–14% of their body mass in food each day spending as little as 14% of the day hunting (Schaller, 1972; Shane et al., 1986; Gorman et al., 1998; Williams et al., 2004b).

Although the necessity for elevated feeding rates in sea otters has been recognized (Kenyon, 1969; Costa and Kooyman, 1982), few studies have addressed the energetic costs associated with maintaining such high rates of food intake. Neither the cost of individual dives nor the metabolic rates resulting from prolonged foraging sessions by sea otters has been determined. Furthermore, potential oxygen conserving mechanisms characteristic of other foraging marine mammals have not been investigated. In view of this lack of information and the importance of foraging costs in daily activity and energy budgets (Stephens and Krebs, 1986), we measured the energetic cost of diving and foraging in adult male sea otters. The relative contribution of costs associated with capturing, consuming and assimilating different types of prey was determined. These data were then compared to the energy expended for resting, grooming and swimming by this mammal. By combining the energetic costs for these different behaviors with an activity budget for wild sea otters, we then calculated a field metabolic rate for free-ranging otters that was compared to values reported for other marine-living mammals.

Oxygen consumption and energetic costs
Energetic costs of different activities were determined from measurements of oxygen consumption by the captive otters. Both animals were trained over a period of 12 months to rest or make voluntary dives and then surface beneath a clear acrylic dome (1.3 m×0.7 m×0.5 m; length × width× peak height) that floated on the water. All measurements followed the methods of Williams et al. (Williams et al., 2004b) using an open-flow respirometry system for aquatic mammals. Air was pulled through the dome at a rate of 180–190 l min–1 by a mass flow controller (Flow kit 500H, Sable Systems, Henderson, NV, USA). Sub-samples of dome exhaust were drawn through a series of three columns filled with a desiccant (Drierite, W. A. Hammond Drierite, Xenia, OH, USA) and a CO2 scrubber (Baralyme, Chemetron Medical Division, Allied Healthcare Products, St Louis, MO, USA) at a rate of 500 ml min–1 before entering an oxygen analyzer (model FC1-B, Sable Systems). The air flow was adjusted so that the oxygen content of the dome remained above 20.10% for all trials. Oxygen content of the dome exhaust was logged every 2.0 s on a laptop computer. Flow rates were corrected to STPD prior to calculating the rate of oxygen consumption using equation 4b from Withers (Withers, 1977).

Oxygen consumption of the otters was determined under four conditions: (1) resting quietly on the water surface, (2) grooming, (3) following serial foraging dives, and (4) following single non-foraging dives. The animals were post-absorptive (by fasting overnight) during the resting and single dive trials, and post-prandial for all other metabolic tests to simulate energetic status in the wild. For resting measurements, the otters floated beneath the metabolic dome in shallow holding pools. The lowest oxygen consumption measured over a continuous 5 min period during 10–20 min trials was used.

Foraging costs were determined by measuring oxygen consumption following prey-searching dives. Foraging trials were conducted in a 9.1 m deep, 4 m diameter seawater storage tower with the metabolic dome sealed on the surface of the water. To facilitate viewing otter behavior during submergence, four underwater video cameras (Lorex model CVC-699, Strategic Vista International Inc., Markham, Ontario, Canada) were mounted inside the tank. A rocky substrate and 3–5 kg of live crabs (Cancer spp.), live mussels (Mytilus edulis) or 1.0–1.4 kg of the otters' mixed diet (commercial squid, surf clams, tiger prawns and cod) were added to the bottom of the tank to simulate foraging conditions in the wild. On each test day an otter was placed in the tank and allowed to forage by making repeated dives to the bottom to collect prey items. Following collection of the food items the otters surfaced beneath the metabolic dome while handling and consuming prey. The duration of foraging trials was determined by the otter and ranged from 60–145 min. Oxygen consumption during grooming, which included vigorous rubbing and pleating of the fur, was recorded opportunistically during the inter-dive periods of the foraging trials.

In addition to the serial foraging dives, one otter (no. 180) was trained to perform single non-foraging dives and then rest under the metabolic dome upon surfacing. The resulting values for oxygen consumption rate (V̇O2) were used to assess locomotor costs associated with diving. During these trials, the otter dove to a target at the bottom of the tank at 9.1 m and remained at depth until receiving the signal to return and surface beneath the metabolic dome. Upon returning, the otter rested beneath the dome and was rewarded with small pieces of food, which required minimal handling and totaled less than 0.3 kg over a 10–20-min period while the post-dive oxygen consumption was monitored.

Oxygen consumption rate was calculated using DATACAN V (Sable Systems International, Henderson, NV, USA) by summing the amount of oxygen used during a specific behavior (i.e. resting, grooming) divided by the duration of the behavior. For foraging trials, metabolic rate was calculated by summing the amount of oxygen used during the entire foraging bout (including diving, post-dive recovery, prey manipulation and consumption of prey items) divided by the duration of the bout. Single dive metabolic rates were calculated according to Castellini et al. (Castellini et al., 1992) by summing the amount of oxygen used during the post-dive recovery period and dividing by the duration of recovery. The end of the recovery period was defined as the point in time when V̇O2 returned to within 10% of resting values. To evaluate locomotor costs (the amount of oxygen consumed for performing a single dive), maintenance costs (measured as resting metabolic rate) that were incurred during the dive and subsequent recovery period were subtracted from the total oxygen consumed during recovery assuming that maintenance costs remained constant throughout the dive (Scholander, 1940; Hurley and Costa, 2001). An observer with a stopwatch recorded surface and sub-surface intervals for all metabolic trials.

Plasma lactate concentration
To assess potential anaerobic contributions to diving metabolism, plasma lactate concentration was measured for resting and diving sea otters. Prior to the tests, the animals were trained to enter a protected contact box specifically designed for blood sampling. The otter rested dorsally recumbent while a clear acrylic door was partially lowered, leaving the caudal third of the otter's body exposed. Blood samples were drawn from the popliteal vein (approximately 1 cm from the femoral condyles) using a 22-gauge needle and a 12-ml syringe while the otter rested inside of the box. On different days, the same procedure was performed immediately following 9.1-m dives in the water tower that varied in duration. Blood samples were transferred to sterile tubes (Becton Dickinson Vacutainer, Franklin Lakes, NJ, USA) containing a glycolytic inhibitor (sodium fluoride and potassium oxalate) for plasma lactate concentration analysis. The samples were immediately refrigerated until further processing (<15 min post blood draw). Each vial was centrifuged for 10 min (2500 r.p.m.) and the plasma transferred to a new sterile tube. Sub-samples were immediately shipped overnight on cold packs to the University of California, San Diego, USA (Comparative Neuromuscular Laboratory) for determination of plasma lactate concentration (using a YSI Sport 1500, Yellow Springs, OH, USA).

Field studies
Eleven free-ranging, adult male otters were used in assessments of daily activity budgets in the wild (Table 1). The otters were captured and tagged along the San Simeon (CA, USA) coastline between March 2001 and October 2002. Each otter was captured by re-breather equipped SCUBA divers using Wilson Traps (Ames et al., 1986), and transported to mobile veterinary surgical facilities onshore.

The otters were weighed to the nearest 0.1 kg using a platform scale (Arlyn 320D, Rockaway, NY, USA) and sedated for implantation of a radio tag. Anesthesia was induced using an intramuscular injection of fentanyl (Elkins-Sinn, Cherry Hill, NJ, USA; 0.5–0.11 mg kg–1 body mass) in combination with diazepam (Abbot Laboratories, North Chicago, USA; 0.010–0.053 mg kg–1). Anesthesia was maintained with an isoflourane gas and oxygen mixture (Williams and Siniff, 1983; Monson et al., 2001). The otters were surgically implanted with an intra-abdominal VHF radio transmitter (7.6 cm×10.2 cm×2.5 cm, ∼120 g; Advanced Telemetry Systems Inc., Isanti, MN, USA) following standardized procedures (Williams and Siniff, 1983; Monson et al., 2001). The transmitters were allowed to float freely in the abdominal cavity and provided consistent signals for 1–3 years.

For identification in the field, colored plastic tags (Temple Tags, Temple, TX, USA) were attached into the webbing of the hind flippers and a passive integrated transponder (PIT) chip was inserted under the skin of the right inguinal area. At the completion of all procedures, an intramuscular injection of naltrexone (Wildlife Pharmaceuticals, Fort Collins, CO, USA; 0.053 mg ml–1) was given as an antagonist to ensure that the animals were alert prior to release. Once the otters were active, they were released close to their original capture site or from the nearby shore.

Activity budgets
Daily activity budgets of wild otters were determined between July 2001 and July 2003 using a combination of direct observation and radio telemetry. During daylight hours direct observations were used in conjunction with telemetry. The otters were visually monitored from shore using a 50× spotting scope (Questar Inc., New Hope, PA, USA). The temporal pattern of the VHF signal from the implanted radio tag enabled us to assign behavior, according to published methods (Loughlin, 1980; Ralls and Siniff, 1990). During hours of darkness, activity was assessed from the changes in the character of the transmitted radio signals. For example, implanted tags in resting otters produced a constant, uninterrupted signal, whereas those from active animals that were not feeding or resting produced a constant pulse of variable strength. When otters were actively feeding, radio signals were interrupted while the animals were submerged and steady while the animal consumed prey at the surface.

The instantaneous behavior of focal animals was recorded at 10-min intervals over 24-h recording sessions. [2] Behaviors were classified as resting, grooming (including somersaulting in the water, vigorously rubbing and pleating the fur), foraging (including eating on the water surface and actively diving) or swimming. Behaviors that did not fall into one of these classifications were categorized as `other' (e.g. interacting with conspecifics).

Daily activity budgets were calculated as the total number of 10-min intervals assigned to each behavior. Periods when the radio transmitter signal was poor were classified as `unknown' behaviors. These unknown periods were removed prior to analysis. Thus, the calculated daily activity budgets represent the proportions of known activities across 24 h. To reduce the potential for bias (i.e. if any one behavior was more likely to be classified as unknown), our analyses are limited to sessions in which ⩽10% of the intervals were classified as `unknown'. This restriction reduced our sample size from 11 to six adult otters for the determination of activity budgets (Table 2) and subsequent field metabolic rates.

Dive duration
The duration of individual dives was measured by two methods. During daylight, duration was assessed visually and then timed by an observer with a stopwatch. During the night, dive duration was determined by timing the interval between VHF radio transmitter signals as described above.

Energy budgets and field metabolic rate
Daily energy requirements for individual otters were calculated by combining the activity budgets of the six wild otters with activity-specific energetic costs from the captive otters. Costs were determined from the V̇O2 of each behavior determined during the captive animal trials and supplemented with data for submerged and surface swimming from Williams (Williams, 1989). All oxygen consumption rates were converted to energetic demand (MJ day–1) using a factor of 20.083 kJ l–1 O2 (Schmidt-Nielsen, 1997). To estimate total daily energy expenditure, the energetic rates for individual behavioral categories were summed according to measured activity budgets over 24-h periods. The resulting value was termed the field metabolic rate (FMR) and did not take into account air or water temperatures during the time of observation.

It was not possible to measure oxygen consumption for some behaviors that were observed in the wild (interacting with conspecifics, simultaneous surface swimming and grooming). Therefore, the mean V̇O2 of surface swimming (29.6 ml O2 min–1 kg–1) (Williams, 1989), subsurface swimming (17.55 ml O2 min–1 kg–1) (Williams, 1989), and grooming and foraging (this study), was used to generally represent the cost of `other' behaviors.

Statistical analysis
Statistical analyses were performed using SYSTAT 10.2 (Systat Software Inc. Richmond, CA, USA). Multiple comparisons of independent samples were made using a multifactor ANOVA, unless otherwise stated. The type-I error rate for all tests was set to α=0.05. Comparisons between individual captive otters under each experimental condition were made using a two-sample t-test. A least squares non-linear regression was used to describe total oxygen consumption in relation to dive time as determined by best fit multiple regression comparisons (Systat Software Inc. Richmond, CA, USA). Lastly, data for field metabolic rate and body mass were log transformed and a least-squares allometric regression developed. All results are reported as mean ± 1 s.d.

Dive duration of captive and wild otters
To ensure that laboratory foraging dives reasonably simulated feeding dives by wild otters, routine dive duration and surface intervals of free-ranging otters in coastal areas were compared to dives in the seawater storage tank. The total period of submergence was recorded for 2055 foraging dives by wild otters in a 10 m deep coastal zone (as indicated by bathymetry maps), and compared with 287 dives performed by the captive sea otters in the 9.1 m deep tower. Total foraging dive duration ranged from 1 to 193 s for captive otters and from 1 to 240 s for the wild sea otters. Mean foraging dive durations for wild and captive otters were 60.5±39.1 s and 65.2±45.1 s, respectively (Fig. 1), and were not significantly different (t=1.7, P=0.08).

Oxygen consumption and energetic costs
All metabolic experiments were conducted on different days; therefore separate trials were assumed to be independent data points. Because resting metabolic data for the two otters were not statistically different (t=2.2, P=0.69), the data for both animals were combined. Mean resting metabolic rate (RMR) for sedentary otters floating on the water surface was 13.3±0.9 ml O2 kg–1 min–1 (N=23 trials) and was similar to previously published values [11.7–13.5 ml O2 kg–1 min–1 (Morrison et al., 1974; Costa and Kooyman, 1982; Williams, 1989)]. No relationship was detected between water temperature and resting metabolism over the range of 13°C to 17°C examined in the present study (N=23 trials, r2=0.09, P=0.70).

Diving, grooming and foraging resulted in an increase in V̇O2 over resting levels (Fig. 2), with the resulting metabolic rates differing significantly among all activity states (resting, grooming, foraging and diving one-way ANOVA, F=411.7, P0.001). The highest mean metabolic rate measured for any behavior was during post-dive, post-prandial grooming periods and averaged 29.4±2.6 ml O2 kg–1 min–1 (N=11 trials); this was 2.2 times the value measured for resting.

Diving costs
For single dives ranging in duration from 40 to 192 s, post-dive recovery oxygen consumption increased non-linearly with dive duration according to the relationship where oxygen recovery is the amount of oxygen required for performing a single dive in ml O2 and dive duration is in s (Fig. 3). Because resting oxygen consumption was factored out for these calculations, the resulting values represent the amount of oxygen utilized for performing the dive above that required for supporting maintenance functions. This assumes no change in the level of maintenance metabolism throughout the dive.

The rate of oxygen consumption during single dives did not vary during these trials. Mean metabolic rate for single dives, 17.6±0.5 ml O2 kg–1 min–1 (N=11 trials), was only 1.3 times resting values (Fig. 2), and is similar to the level reported for horizontal submerged swimming by sea otters (Williams, 1989).

As might be expected because of the number of different behaviors involved, energetic costs were higher for foraging dives than for the single, non-foraging dives (Figs 2 and 4). Foraging bout duration for the captive otters ranged from 60 to 145 min and consisted of multiple dives and post-dive recovery periods that included prey handling and consumption. Metabolic rates measured during these bouts differed marginally between prey items. For otters foraging on live cancer crabs metabolic rate averaged 22.2±1.3 ml O2 kg–1 min–1 (N=7), which decreased to 20.1±2.7 ml O2 kg–1 min–1 (N=4) for mussels and 21.4±1.3 ml O2 kg–1 min–1 (N=8) for a mixed diet (Fig. 4). Statistically, there was no effect of prey type (F=1.25, P=0.20) or otter (F=1.83, P=0.20) on metabolic rate for the crab or mixed diet trials, nor was there an interaction effect between prey type and otter (two-way ANOVA, F=3.29, P=0.10). Owing to a low sample size, mussel trials were excluded from these statistical comparisons. The average foraging metabolic rate for all otters and prey types was 21.6±1.7 ml O2 kg–1 min–1 (N=19).

Plasma lactate concentration
Increased anaerobic metabolism, as manifested by an elevation in plasma lactate concentration, was not observed in the captive diving sea otters in this study. The concentration of plasma lactate was variable and ranged from 0.33 to 1.65 mmol l–1 in resting sea otters (mean = 0.97±0.46 mmol l–1; N=6). These lactate levels were considerably higher than observed for other marine mammals including bottlenose dolphins (Williams et al., 1993) and Weddell seals (Kooyman et al., 1980; Kooyman et al., 1983; Guppy et al., 1986) whose resting values typically average 0.5 mmol l–1.

Owing to the variation in resting levels it was not possible to detect a change in plasma lactate concentration with diving. Post-dive lactate concentration for single dives of 30–100 s ranged from 0.3 to 1.1 mmol l–1 and did not exceed the range for resting values in the captive otters. In general, no correlation between lactate concentration and dive duration was found in this study (r2=0.07, P=0.6).

To ensure that the blood sampling method did not contribute to elevated lactate levels during the resting trials we also tested blood samples obtained from anesthetized sea otters. Lactate levels were similarly elevated relative to other resting marine mammals for both sampling methods. The mean lactate level for anesthetized otters was 0.91±0.21 mmol l–1 (N=4).

Activity budgets
Twenty activity observation sessions comprising over 300 h of monitoring were completed on 11 free-ranging sea otters. The greatest proportion of the day for wild sea otters was spent feeding and resting (Table 2) and was similar to previously reported activity budgets for California sea otters (Estes et al., 1986; Ralls and Siniff, 1990; Tinker, 2004).

For the six otters with the most complete records, over 75% of the day was taken up with feeding and resting, 8.5±6.8% with swimming, 9.1±1.9% grooming, and 7.3±5.8% of the day involved `other' behaviors (Table 2). Rather than randomly dispersed across the day, these behaviors occurred in predictable sequences (Yeates, 2006). Typically, a prolonged period of rest was followed by foraging bouts interspersed with short periods of grooming. [3] The resulting behavioral cycle for wild otters consisted of resting, then grooming and foraging, followed by another grooming session and finally back to resting. The duration of these sequences varied with the individual otter, and occurred throughout the day and night.

Energy budgets and field metabolic rate
Based on the activity budgets and energetic costs described above, we calculated the daily energy expenditure for each behavior and the subsequent field metabolic rate of wild California sea otters (detailed in Table 3). We found that the largest energetic expenditure for sea otters, 6.1±1.1 MJ day–1, was associated with foraging (Table 4). In comparison, resting was a relatively low cost behavior but constituted a large proportion of the day. As a result, sea otters on average spent 4.2±1.0 MJ day–1 to support resting periods. High energy behaviors such as grooming and swimming were often of short duration. The amount of energy spent grooming, swimming and performing other behaviors including interacting with conspecifics was 2.4±0.4 MJ, 1.6±0.4 MJ and 1.4±1.4 MJ, respectively. Together, these latter activities required a total of 5.4 MJ day–1. When summed, the field metabolic of wild sea otters was 15.7±2.7 MJ day–1 (Table 4).

Energetic cost of diving and foraging in the smallest marine mammal
For any carnivorous mammal, foraging entails a variety of energetic costs including those associated with body maintenance functions, locomotion, as well as the energy expended in the handling and processing of food (Stephens and Krebs, 1986; Kramer, 1988). In view of the exceptionally high costs associated with these physiological and behavioral functions for sea otters (Morrison et al., 1974; Costa and Kooyman, 1982; Costa and Kooyman, 1984; Williams, 1989), it is not surprising that the cost of foraging was also high for this marine mammal (Fig. 2).

Comparisons with other species of wild marine mammals are difficult since few studies have examined the metabolic costs of diving and foraging for this group with the exception of phocid seals. However, when the data for sea otters are compared to this limited data set, we find that the smallest marine mammal demonstrates higher relative and absolute costs for both diving and foraging. In the present study, the metabolic rate of sea otters performing single dives ranging in duration from 40 to 192 s was 17.6 ml O2 kg–1 min–1. This compares with 4.5 to 5.7 ml O2 kg–1min–1 for phocid seals including juvenile and adult grey seals weighing 41 to 128 kg (Sparling and Fedak, 2004) and adult 390 kg Weddell seals (Castellini et al., 1992). These differences remain even when the disparity in body mass between the otters and seals is taken into account. The predicted diving costs for a 25 kg seal based on an allometric regression for diving costs in relation to phocid body mass from the previous studies is 7.7 ml O2 kg–1 min–1, a value that is less than half that measured for the sea otters.

A wide variety of factors probably contribute to the higher diving costs observed for sea otters compared to phocid seals. These include differences in (1) swimming style, (2) buoyancy, (3) the metabolic effects of food processing and (4) thermoregulation. We can examine each of these for sea otters by subdividing the total cost of a foraging dive into its components as shown in Fig. 4. From these calculations, maintenance costs, as defined by resting metabolic rate, constituted over 60% of the diving costs for this species. Locomotor costs for performing the dive accounted for 16.6–19.4% of total diving costs, leaving 20.3–20.7% of the energy expended in a foraging dive to support hunting behaviors (e.g. searching for prey at depth) and prey handling and consumption at the surface.

From this calculation, maintenance functions represent the major energy expenditure for foraging sea otters, and would likely be reduced if these animals initiated a dive response when submerged. Weddell seals performing extended (>14 min) dives beneath the Antarctic sea ice (Castellini et al., 1992), as well as elephant seals (Webb et al., 1998a), grey seals (Sparling and Fedak, 2004) and California sea lions (Hurley and Costa, 2001) resting and diving in a laboratory setting demonstrate a decrease in metabolic rate during prolonged submergence. Thus, energetic costs for pinnipeds resting on the water surface are 10–48% higher than total submergence costs for the animals voluntarily swimming or diving in a pool. If sea otters followed a similar trend, the oxygen consumed during the dive (Fig. 3) would have been lower than that measured during resting (Fig. 2), and the relative contribution of maintenance costs to the total cost of a dive would have been smaller. Alternatively, a dive response and or hypometabolism may be occurring in sea otters, but it is not detectable because the possible costs associated overcome the effects of being positively buoyant during shallow dives.

It is unclear to what extent, if at all, sea otters reduce foraging costs through oxygen conserving mechanisms associated with hypometabolism, bradycardia and decreased peripheral blood flow that constitute the dive response reported for other marine mammals (Scholander, 1940; Kooyman, 1989). In marine-adapted species, the response can be pronounced and serve as a means for extending the duration of a dive (Scholander, 1940). Owing to the relatively short dive durations of sea otters (Fig. 1) and the size of on board oxygen stores (Kooyman, 1989), such a response may not be critical during foraging in productive coastal areas. Using our measured diving metabolic rates (Fig. 2) and published values of total oxygen storage capacity for sea otters (Lenfant et al., 1970), the calculated aerobic dive limit (Kooyman et al., 1983) for an adult sea otter ranges from 2.9 to 4.3 min (180–275 s) depending on whether the animal dives with a full or half-full lung of air. This range represents the extreme upper limit of dive durations observed for wild sea otters (Fig. 1), and indicates that sea otters are able to dive aerobically during routine foraging dives along coastal California.

Under the experimental conditions of the present study, we found that a significant portion of the total diving cost for sea otters could be attributed to the energy required for locomotion (Fig. 4). Because of its small body mass, proportionally high buoyancy (Tarasoff and Kooyman, 1973) and transitional style of propulsion, sea otters demonstrate larger transport costs for swimming than reported for other marine mammals (Williams, 1999). Therefore, high locomotor costs during diving might be expected.

Several behavioral options allow more derived marine mammals to reduce locomotor costs by simply avoiding active swimming. These include the use of ballast and buoyancy control (Webb et al., 1998b; Cashman, 2002), as well as controlled gliding on ascent or descent (Williams et al., 2000). For sea otters, exceptionally large lungs and air in the fur (Tarasoff and Kooyman, 1973) make the animal buoyant. This characteristic undoubtedly contributes to the high cost of diving by increasing the physical forces that must be overcome to reach depth. Using biomechanical models, Cashman (Cashman, 2002) demonstrated that the California sea otter does not reach neutral buoyancy within the diving depths observed for wild coastal otters (Tinker et al., 2007). As a result, the animal must rely on locomotor power to overcome buoyancy when locating prey at depth. This energetically costly task is circumvented in larger or deeper-diving marine mammals by passive gliding aided by negative buoyancy (Williams et al., 2000). Alternate behavioral strategies such as carrying ballast or decreasing lung volume enable adult otters to reduce buoyancy in the water column (Cashman, 2002). Presumably, this behavior will also serve to reduce locomotor costs, particularly during deeper foraging dives.

The final energetic cost associated with foraging is the energy expended during hunting and food processing. In the wild, sea otters feed on a wide variety of invertebrate prey that require specific capture, collection and handling techniques (Kenyon, 1969; McCleneghan and Ames, 1976; Jolly, 1997; Tinker, 2004). The collection of prey can involve digging in sediments or pulling items from rocky substrates, which result in different handling times. Ingestion also involves different tasks. Otters consuming mussels and clams crush the shells with their incisors as well as hammer one mussel against another (Wolrab, 2003). By contrast, otters preying on crabs will tear the legs and claws from the large carapace prior to consuming the meat (Wolrab, 2003).

Despite these varied tasks, we observed no significant difference between the energetic costs associated with foraging on different types of prey in the present study (Fig. 4). In general, the cost of handling and processing prey contributed approximately 20% to the total cost of a foraging dive for sea otters feeding on crab, mussels or a mixed diet. Of these, there was a general, although not significant, trend for higher energetic costs when the otters fed on crabs.

Another energetically expensive factor associated with prey processing is the heat increment of feeding (HIF). [4] In sea otters, the energy required for digesting and absorbing food following a meal, the HIF, results in a prolonged increase in resting metabolism (Costa and Kooyman, 1984). The maximum increase in post-prandial oxygen consumption reported in the previous study occurred approximately 82 min after a 1.5 kg meal. By contrast, Weddell seals demonstrate an HIF response during the post-dive recovery period immediately following ingestion of Antarctic silverfish (Williams et al., 2004b). In both species, the HIF response may last for several hours depending on prey type, the size of the meal, and foraging patterns. For sea otters, changes in core body temperature during and after a dive (Yeates, 2006), and post-dive defecation indicate that digestion and assimilation of prey occurred within foraging bouts during the trials. Thus, HIF response probably contributes to the energetic cost of prey handling by foraging sea otters.

Foraging costs and the daily energy requirements of wild sea otters
When the energetic costs of various behaviors are summed according to the activity budget of wild sea otters (Tables 2, 3, 4), the resulting mean estimated daily energetic cost for an adult male is 15.7±2.7 MJ day–1. Surprisingly, this level of energy expenditure for sea otters was nearly identical to predicted values based on an allometric regression for the field metabolic rate (FMR) of a wide variety of marine mammals including otariids, phocid seals and large and small odontocetes (Fig. 5) (Williams et al., 2004a). Thus, the sea otter values did not differ from predicted values of FMR based upon a regression of marine mammal FMR values against body size, despite comparatively high foraging costs observed in the present study.

One explanation for this is related to differences in the activity budgets for foraging marine mammals. Unlike actively foraging pinnipeds (Costa and Gales, 2003) and cetaceans (Shane et al., 1986; Baird et al., 2005) that spend the major portion of the day transiting to foraging areas or diving, sea otters spend 40–49% of the day resting motionless on the water surface (Ralls and Siniff, 1990) (Table 2). Were the otter to maintain activity levels typical of other marine mammals, FMR would be significantly higher due to the high energetic cost of swimming (Fig. 2).

In summary, the marine environment would initially appear to be energetically challenging for sea otters because of its small size, exceptional buoyancy, and costly style of swimming. Without the benefit of many of the energy conserving mechanisms reported for other marine mammals, we expected total daily energetic costs to be elevated for sea otters relative to other marine mammals. Instead, energetically costly behaviors were counterbalanced in part by prolonged periods of rest that composed up to 49% of the sea otter's day. Thus, by budgeting behavior as well as the costs associated with each, wild sea otters are able to maintain a daily energetic balance similar to that of larger, more derived marine mammals.
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Thomas 1996

Created By: Jessica Khalili

The growth of the southern sea
otter population has been steady, but
slow in comparison to Alaskan subspecies,
and range expansion in California
has faltered. Slower growth is occurring
in California despite birth rates
comparable to those in Alaska, so biologists
have reasoned that mortality is
hindering the growth of the California
population (Riedman and Estes 1990;
see Estes et al., this issue). In order to
investigate this issue, research efforts
have been directed toward identifying
the causes of death in southern sea
Several major causes of mortality
in the southern population were recognized
in the past and are currently being
addressed. These include protections
from overharvesting and accidental entanglements
in fishing gear, as well as
oil spill prevention and contingencies.
Still to date, the problem of slow population
growth and expansion persists.
The California Department of Fish
and Game has studied sea otter mortality
since 1968. A salvage network,
maintained through the cooperation of
State and Federal agencies and scientific
institutions, verified beach-cast carcasses
and examined them to estimate
the causes of death. By 1989 nearly
1700 dead sea otters had been documented
(see Table 1; Ames et al. 1983,
unpublished data; Riedman and Estes
1990). Substantial mortality from net
drownings was identified and the prevalence
of trauma from predators, shooting, fighting and mating activities were
documented. Pup abandonment and a
variety of miscellaneous conditions and
diseases were recorded. Since 1992,
laboratory diagnostic efforts at the National
Wildlife Health Center (NWHC),
Madison, Wisconsin, supplemented the
stranding network's activities in California,
so that knowledge about the
causes of mortality has been further
refined. It is these recent perspectives
on the causes of mortality in the southern
seaotter that are outlined here, along
with consideration of their implications
for sea otters and the Pacific marine

Causes of mortality

Since 1992 approximately 50 southern
sea otter carcasses per year were
examined at the NWHC as part of a 5
year intensive necropsy study. Carcasses
were selected for the NWHC
study on the basis of good postmortem
condition from the approximately 110
to 160 carcasses found per year in California.
At the NWHC, microscopic
examination supplemented gross examination
of the carcasses and a variety of
laboratory techniques in bacteriology,
virology, parasitology, and toxicology
were conducted to arrive at a diagnosis.
By this means a greater proportion of
the animals with inapparent causes of
death were diagnosed. Only a prelirninary
analysis of the 1992-95 data has
been done, but some interesting patterns
are emerging from the 195 cases studied (and additional
samples have been collected through 1996).
The proportionate
causes of mortality identified at the NWHC bore
similarities to past data
but also had interesting
differences. Sea otter mottallties from 1968-1989 (n=1,680), fungal, or bacterial dis- taken from Ames 1983 and Riedman and Estes 1990.
eases caused the deaths
of 38.5% of the sea otters
examined at the NWHC. Twenty percent
died from traumatic injuries. Another
10% were emaciated at death and
no specific cause for their debility could
be identified. Miscellaneous conditions,
such as neoplasia, or gastrointestinal or
urinary obstructions, accounted for
13% of the mortality. In 18.5% of the
animals no cause of death could be
Traumatic causes, emaciation and
a variety of miscellaneous conditions
were similar to those described in sea
otters in the past. Ames summarized the
causes and distribution of traumatic injuries
in sea otters examined from 1968
to 1989 (as presented in Riedman and
Estes 1990). The most frequently identified
cause of trauma in the past was
shark attack (Ames andMorejohn 1980);
the shark-bitten sea otters were collected
throughout the range but the largest
proportion were found north of Point
Sur. In the recent study shark attack
was also the most frequently diagnosed
source of trauma (7% of all mortality,
n=14), and more than 70% of the sharkbitten
sea otters were found north of
Point Sur. In the past, gunshot injuries
were documented predominately south
of Cambria. Ames speculated that the
frequency of shark attacks in the northern
extent of the range and gunshot
mortalities in the south may have an
impact on range expansion (as presented
in Riedman and Estes 1990). Gunshot
was diagnosed in 4% (n=8) of the sea
otters in the recent study but these cases
were equally distributed between the
range south of Cambria and north of
Point Sur.

Infectious disease

The high frequency of infectious
diseases (38.5%, n=75) was unexpected.
Many of these diseases were reported
but uncommon in the past. Peritonitis
induced by acanthocephalan parasites
(see below) was the diagnosis for 14%
(n=27) of the sea otters examined at the
NWHC, comprising the single most frequent cause of death, as well as the most
frequent infectious disease. Most (67%,
n=18) cases of acanthocephalan peritonitis
occurred in pups or juvenile sea
otters. Peritonitis occurs when larval
acanthocephalan parasites that reside in
the intestine aberrantly migrate through
the intestinal wall allowing bacteria to
infect the abdominal cavity. Additionally,
in many of these cases, thousands
of acanthocephalans were embedded in
the intestinal wall, and there was profuse
bloody enteritis. The parasite causing
this condition, Polymorphus spp.,
belongs to one of two genera of acanthocephalans
found in southern sea otters
(there is a current taxonomic dispute
on the Polymorphus species identification).
The other, Corynosoma
enhydri, was found frequently but
caused no detectable deleterious effects.
Acanthocephalans are transmitted to sea
otters through invertebrate intermediate
hosts. The spectrum of invertebrate
hosts of Polymorphus spp. is unknown.
Polymorphus spp. were reported in small
numbers (2-206 per otter) in 10% of the
southern sea otters examined by
Hennessy and Morejohn (1977). Both
the prevalence and intensity of
Polymolphus spp. infections appear substantially
greater in recent years.
Protozoal encephalitis was the
cause of death in 8.5% (n=17) of the sea
otters examined at the NWHC. This is
the first report of this organism or disease
in sea otters. Most (88%, n=15) of
the affected otters were adults or subadults.
Otters with encephalitis had no
gross evidence of the condition but,
microscopically, inflammation in the brain was associated with intermediate
stages of protozoal parasites. The characterization
of this disease syndrome
was confounded by the fact that the
protozoan (Toxoplasma gondii) was isolated
from the brains of sea otters with
and without encephalitis. Immunohistochemical
tests indicated that a second
protozoan was present in some of the
cases, suggesting that two agents may
be involved. In each year of the recent
study, encephalitis cases were restricted
to the spring and summer. The means of
transmission of these agents to sea otters
is unknown. The typical infectious
stage, the oocyst, of T. gondii is shed in
the feces of a species-specific definitive
host, the cat. Intermediate stages of
several protozoan agents are found in
animal tissues and may also be directly
infectious if ingested. The intermediate
stage of T. gondii is found in a wide
variety of vertebrates including humans
world wide, but serious illness from
the infection is sporadic. Illness is
more common in the very young, aged,
or as a complication of impaired immune
Eight cases of coccidioidomycosis
(4% of all mortality), a systemic infection
caused by the fungus, Coccidioides
immitis, were diagnosed from 1992-95
(Thomas et al. 1996). Only one case
had been reported previously, in 1976
(Cornell et al. 1979); this may be an
emerging problem. The affected sea
otters were adult or subadult. All 8 sea
otters, and the prior case in 1976, were
found at the southern end of the range at
San Luis Obispo County. The disease,
also known as San Joaquin Valley fever,
is endemic in certain arid regions of
the Southwest U.S., notably the Central
Valley of California. This fungus grows
in soil to form arthrospores that produce
disease when inhaled by susceptible
individuals. Coccidioidomycosis most
often manifests itself in the respiratory
tract, but many organs, including the
brain, may be affected. A wide variety
of species, including humans, are susceptible
to coccidioidomycosis. The
results of exposure vary, depending on
both species and individual factors, from
no ill effects to death. In all sea otter
cases the infection was widely disseminated
to affect multiple organs.
The deaths of 12% (n=23) of the
otters were attributed to various bacterial
infections. The affected sea otters
were all adult or subadult. Bacterial
infections were manifested primarily as
pneumonia, heart valve infection, abscess
or septicemia. The origins of
infection were likely to be inhalation or
traumatic injuries, but were inapparent
in most cases. Bacterial infections occurred
as individual cases with no apparent
links among them, so direct transmission
between sea otters was unlikely.
The most frequently isolated bacteria
were different strains and species of
Streptococcus, but the agents varied
widely and mixed infections in the same
individual were common.
Significance of disease

The implications of the recent
necropsy results appear complex. Past
mortality surveys suggested that the influences
of "natural" (that is, not directly
human-inflicted) mortality might
be significant (Ames et al. 1983). The
preliminary data presented here corroborate
that mortality from natural
causes, specifically infectious diseases,
is occurring at a high rate. Disease
mortality is not only frequent but some
diseases appear to be on the rise while
others are newly reported. Several of
the diseases are predominately affecting
prime age, breeding adults. Taken
in total, the findings regarding infectious
disease mortality appear to bear
some disturbing implications for sea
otters. The immediate questions are
whether this frequency is truly unusual
and whether it is remediable. In comparison to endangered terrestrial
top-level predators, these results
are unusual, and, at the moment,
there is no comparable data available
for other, more vigorous sea otter populations.
The NWHC is carrying out
similar mortality studies on gray wolves
(Canis lupus) in the Great Lakes Region
and for the red wolf (Canis rufus)
reintroduction program. In these terrestrial
species the greatest proportion of
mortality (55% for gray wolves and
42% for red wolves) is accidentally or
intentionally human-inflicted by shooting,
trapping, poisoning, or vehicle
trauma. Infectious diseases cause a
relatively minor proportion of the mortality
in these species, at a rate of 9% in
gray wolves and 8% in red wolves.
The question of whether the sea
otter's disease mortality has a remedy is
not readily answered in our current state
of knowledge. Missing details about
the transmission cycles of the more frequently
encountered diseases may provide
the keys to effective control measures.
Before focusing on the transmission
cycles of individual diseases, it
may be useful to consider the underlying
significance of a high rate of infectious
disease from a broad perspective.
In order to exhibit a high frequency and
variety of infectious disease mortality,
are southern sea otters highly vulnerable
to many diseases or are they undergoing
high rates of exposure?
A state of general susceptibility is
suggested by the variety of infections
encountered in sea otters. Unusual vulnerability
is also suggested by the fact
that otter deaths are repeatedly attributed
to diseases that are expected to
cause only sporadic mortality in other
species. Generalized vulnerability to
infections implies that immune function
is ineffective. Although assessing
and understanding the exact mechanisms
of immune function impairment is complicated,
in general, immunologic defects
may be congenital or have a genetic
basis, or arise from certain viral
infections, environmental toxins, or malnutrition.
The factors that affect the rates of
infectious disease exposure in sea otters
differ among the different diseases encountered.
The potential sources of the
disease agents and means of exposure
differ, as do the reasons why an apparent
increase or emergence might be
taking place. Exposure rates may be
linked to population density for certain
diseases but density-independent for
others. Identification of the key factors
that affect exposure and the significance
of each disease in relationship to
population dynamics will be important
distinctions to make if we are to
arrive at effective mortality-reduction
Polymorphus spp.
Over the last 5 years the prevalence
and intensity of Polymorphus spp. infections
in otters and the frequency of
extraintestinal migration of
acanthocephala has increased. In order
to understand this increase in deleterious
Polymorphus spp. infections in sea
otters, we need to examine the predatorprey
dynamics of the definitive host
species (sea birds) and probable intermediate
hosts (crabs). It is this predator-
prey relationship that the
Polymorphus spp. depend upon for
completion of the life cycle. Preliminary
data suggest that Emerita analoga
and Blepharipoda sp. of crab are two
intermediate hosts for this acanthocephalan,
however there may be more invertebrate
species involved. Birds such as
gulls, scoters and sea ducks prey upon
infected crabs and harbor the egg-producing
adult Polymorphus spp. The
eggs are deposited with feces into the
environment. Sea otters can become
infected with the Polymorphus spp., by
eating the infected crabs, however, the
sea otter is a dead-end host and no eggproducing
acanthocephalans have
been found. Abiotic or biotic factors
that influence the population densities
and predator-prey interactions of
the bird, invertebrate hosts, or sea
otters could affect the risk of infection
in sea otters.
There are three broad facets to examine
to determine why increases may
be occurring in otters.
( I ) Factors impacting birdpopulations.
A larger infected bird population
(as higher prevalence and/or higher
acanthocephalan burdens) could be due
to factors that caused an increase in
certain sea bird populations, or factors
inducing bird aggregations (for example,
beach utilization by humans, distribution
and management of landfills, aggregation
of crab species or other food
(2) Factors influencing intermediate
hostpopulations. A larger infected
intermediate host community (as increased
prevalence and/or larval acanthocephalan
burdens) could be related
to an increase in infected birds that
contaminate the beaches with feces and
acanthocephalan eggs. Add to this the
complicating fact that some
acanthocephala species alter their intermediate
host's behavior, thereby increasing
the risk of predation so that birds
prey disproportionately on infected
crabs. Certain conditions such as a rise
in water temperature and phytoplankton
proliferation can favor the survival
of crab offspring, thereby providing a
larger intermediate host community for
potential infection.
(3) Factors affecting the sea otter
population. A food habit change by
some sea otters could increase their
predation on infected crustaceans. This
prey selection might occur if more optimal
prey items were unavailable or they
may be taken by inexperienced or incapacitated
sea otters that seek easier prey
such as Emerita and Blepharipoda.
A combination of two or more of
the above factors may be interacting to
cause an increase in the parasitism of
the sea otter. Given the complexity of
the ecology influencing the predatorprey
dynamics, several species of invertebrates
and vertebrates need to be
considered in order to identify the factors
influencing the sea otter's
Polymorphus spp. infections.
Eradicating Polymolphus spp. from
the normal bird and invertebrate hosts
would be impossible. However, a reversal
of the sea otter's current mortality
trend from Polymorphus spp. is feasible
if we could reduce the prevalence of this
parasite. Effective management strategies
may be to disperse the responsible
bird species or increase the availability
of alternate uninfected prey species to
sea otters. However, before such management
strategies can be developed
basic questions must be answered, including which crab species act as intermediate
hosts, which beaches have
highly infected intermediate or definitive
host communities, and what factors
correlate with the distribution of infected
sea otters.
Toxoplasma gondii
The source of Toxoplasma gondii
exposure to sea otters is most likely
oocysts from cat feces. [1] Transmission
by preying on infected intermediate
hosts is unlikely because only warmblooded
animals have been reported as
intermediate hosts, and the sea otter is
reported only rarely to eat birds.
otters could ingest oocysts in water contaminated
with cat feces through runoff
from beach soils, or possibly by
eating filter feeding invertebrates that
are transporting oocysts in their alimentary
tracts. If oocysts are entering the
water via sewage effluent, the contamination
of the marine ecosystem could be
much greater than just that from beach
or adjacent shoreline run-off. This
would be an important source to identify
and is potentially manageable. To
investigate the connection between sewage
disposal and otter exposure, the
survivability of oocysts through local
sewage treatment systems and the viability
of oocysts in sea water should be
evaluated. Temporal studies could determine
whether peaks in contamination
correlate with seasonal patterns of
disease. Laboratory studies could be
designed to investigate whether crabs
and other crustaceans could act as
phoretic agents in the transmission of T.
gondii to sea otters. Vertical transmission
of T. gondii from mother to offspring
can cause abortion in sheep,
goats, and humans. Toxoplasmosis in
the very young sea otter may be underrepresented
in post mortem sampling
because carcasses of fetuses or neonates
are less likely to be found
(Riedman and Estes 1990).
Toxoplasmosis, may be more than
the other diseases, raises concern about
the sea otter's general ability to resist
disease. Infection with T. gondii does
not always cause disease in the host.
Disease and death more often occurs in
animals that are vulnerable due to age,
irnrnuno-compromise, or in species (e.g.,
Australian marsupials or arboreal New
World monkeys) that evolved isolated
from felids or their feces. Subadult and
adult sea otters, not just the young or
aged, had protozoal encephalitis, so age
does not appear to be an important factor. 
[2] Sea otter immune competence has
not been well studied, so its status to
date is unknown.
Regarding the species
experience with T. gondii, there is little
information. Most reports of T. gondii
infection of marine mammals are from
captive animals. However, reports of
this protozoan causing disease in the
wild northern fur seal (Callorhinus
ursinus) (Holshuh et al. 1985), the West
Indian manatee (Trichechus manatus)
(Buergelt and Bonde 1983) and five
species of dolphin (Di Guardo et al.
1995) indicate that other wild marine
mammals are also exposed to T. gondii.
Regardless of whether resistance to toxoplasmosis
is an individual or species
phenomenon, we can evaluate the sea
otter's degree of susceptibility by evaluating
the frequency of exposure. Such
studies would help discern if most otters
are exposed to T. gondii and resist
disease or if the few that are exposed
break with disease.
Coccidioides immitis
The occurrence of infections by the
soil-associated fungus, Coccidioides
immitis, in the marine environment is
puzzling. The means of transmission to
sea otters presumably is similar to that
in other species, specifically by
inhalation of airborne arthrospores.
Recurrent dry winds from the east may
disperse the spores from the soil in
endemic sites around the city of San
Luis Obispo or in the San Joaquin Valley.
Coccidioidal spores survive and may
even grow in salt water, so the
accumulation of spores in the marine
environment has also been postulated
(Dzawachiszwili et al. 1964). The
apparent increase in prevalence of
coccidioidomycosis in sea otters since
1992 may be due to the application of
more sensitive diagnostic methods, but
it coincides with a marked increase in
human cases in 1991 to 1993. The
human outbreak was tentatively
attributed to unusual weather and
environmental conditions rather than
human-related factors, so occurrence in
sea otters may lend support to that
hypothesis. Prospects for control of this
disease in sea otters are not promising, but
knowledge about coccidioidomycosis
prevalence has predictive value that may
particularly apply to the population in
the southern extent of range.
Many of the infectious diseases of
concern in southern sea otters are not
species specific; they may affect other
marine mammals, sea birds and human
beings. Some of the epizootiologic factors
that potentially play a role in promoting
disease emergence or frequency
in otters also may have broad effects in
the marine environment. The successful
recovery of the southern sea otter
population is of immediate concern, but
obstacles to their recovery could have
wider implications for the marine ecosystem. 
[3] The sea otter could be a sensitive
indicator of the health of the Pacific
near-shore marine ecosystem.

Conclusions and recommendations

The following series of recommendations
are proposed as means to assess
the impact and implications that have
arisen from investigations into sea otter
(1) Complete the 5 year intensive
necropsy study. The 5 year database
under development at the NWHC will
be completed at the end of 1996. The
recent health and mortality data have
undergone only preliminary evaluation.
Further analyses for age, gender, and
temporal and geographic differences are
necessary to distinguish significant patterns
and compare with previous data.
(2) Analyze the population data.
Further examination of recent necropsy
data by integration with other mortality
and demographic data may provide valuable
insight into the significance of disease
and the role of mortality in population
recovery. The relationship between
the various infectious disease conditions
and population dynamics needs to
be explored. Identification of mortality
factors with the greatest potential for
limiting population growth should guide
research priorities.
(3) Identify key factors in the disease
cycles. The key to reducing mortality in the southern sea otter may be
found by identifying critical points at
which important disease transmission
cycles can be interrupted by knowledge-
based management strategies. The
greatest gaps involve the transmission
of acanthocephalan peritonitis and protozoal
encephalitis. Elucidation of disease
cycles may also provide a measure
of the role of human intervention or
human responsibility in the emergence
of sea otter disease.
(4) Develop comparative data.
Comparison with similar data from a
more vigorous sea otter population
would provide another means to assess
the significance of mortality and various
mortality factors to the southern sea
otter population. The best comparison
would include both the causes and rates
of mortality.
(5) Continue mortality monitoring.
Continuation of a mortality monitoring
system is the basis for identifying
trends, investigating, and interpreting
the patterns in sea otter mortality. The
activities of the sea otter stranding network
are critical to that end.
(6) Evaluate the rates of disease
exposure. By comparing the rates of
disease exposure to the rates of disease
mortality we can evaluate the general
vulnerability of the southern sea otter to
infectious disease.
(7) Assess immunefunction. Evaluation
of the adequacy of the wild southern
sea otter's immune function is a
means to investigate whether generalized
vulnerability to infectious disease
(8) Assess environmental contaminant
exposure. Otter tissue analyses for
organochlorine compounds and heavy
metals were discontinued in 1980. No
serious threats to sea otter health were
revealed in these early analyses. Evaluation
of recent environmental contaminant
burdens in sea otters in correlation
with mortality factors is a means to
assess the current role of toxic contaminants in sea otter disease vulnerability,
debility, or neoplasia.
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Kreuder Et Al 2001

Created By: Jessica Khalili

ABSTRACT[1] Detailed postmortem examination of southern sea otters (Enhydra lutris nereis)
found along the California (USA) coast has provided an exceptional opportunity to understand
factors influencing survival in this threatened marine mammal species.
In order to evaluate recent
trends in causes of mortality, the demographic and geographic distribution of causes of death in
freshly deceased beachcast sea otters necropsied from 1998–2001 were evaluated. Protozoal encephalitis,
acanthocephalan-related disease, shark attack, and cardiac disease were identified as
common causes of death in sea otters examined. While infection with acanthocephalan parasites
was more likely to cause death in juvenile otters, Toxoplasma gondii encephalitis, shark attack,
and cardiac disease were more common in prime-aged adult otters. Cardiac disease is a newly
recognized cause of mortality in sea otters and T. gondii encephalitis was significantly associated
with this condition. Otters with fatal shark bites were over three times more likely to have preexisting
T. gondii encephalitis suggesting that shark attack, which is a long-recognized source of
mortality in otters, may be coupled with a recently recognized disease in otters. Spatial clusters
of cause-specific mortality were detected for T. gondii encephalitis (in Estero Bay), acanthocephalan
peritonitis (in southern Monterey Bay), and shark attack (from Santa Cruz to Point An˜ o
Nuevo). Diseases caused by parasites, bacteria, or fungi and diseases without a specified etiology
were the primary cause of death in 63.8% of otters examined. Parasitic disease alone caused
death in 38.1% of otters examined. This pattern of mortality, observed predominantly in juvenile
and prime-aged adult southern sea otters, has negative implications for the overall health and
recovery of this population.
Key words: Acanthocephalan, cardiac disease, Enhydra lutris nereis, Sarcocystis neurona,
shark predation, southern sea otter, Toxoplasma gondii.


Evidence linking anthropogenic stressors
to unusual patterns of disease and mortality
in marine mammals has accumulated
over the past decade (Ross et al., 1996;
Harvell et al., 1999; Fair and Becker, 2000;
Daszak et al., 2001). Habitat degradation,
pollutants, municipal runoff, global climate
change, and overharvest of marine
resources are likely to have complex effects
that both directly and indirectly affect
marine mammal health. [2] Southern sea
otters (Enhyrda lutris nereis) are a useful
indicator of near-shore marine ecosystem
health because they are heavily exposed to
human activity in coastal California (USA)
and they commonly remain in one geographically
localized area for most of their
Despite legal protection since 1911
and unlike sympatric California sea lions
(Zalophus californianus), northern elephant
seals (Mirounga angustirostris), and
harbor seals (Phoca vitulina) in California
(Carretta et al., 2001), southern sea otters
have made a slower than expected recovery
after hunting drastically reduced their
numbers prior to the 20th century (Estes,
1990). Annual counts of sea otters over
their entire range in California have declined
since 1995 with the current count
at slightly over 2,000 animals (U.S. Geological
Survey, unpubl. data). Birth rates in
California sea otters appear similar to
those observed in other, rapidly growing
otter populations (Riedman et al., 1994;
Monson et al., 2000), suggesting that increased
mortality may be causing the slow
recovery rate in the California population.
A high percent of mortality due to infectious
disease was detected in detailed
necropsies of southern sea otters from 1992–95, which raised concern over the
general susceptibility of this species to infection
and subsequent mortality (Thomas
and Cole, 1996). Furthermore, some diseases
were newly recognized as important
causes of mortality in sea otters, and several
pathogens were implicated that were
not expected to cause considerable mortality
in a free-ranging marine wildlife species,
such as protozoal encephalitis, acanthocephalan
peritonitis, and coccidioidomycosis
(Thomas and Cole, 1996). Continued
monitoring of these newly recognized
diseases in sea otters is essential, not only
in light of the recent population decline,
but also because techniques used to diagnose
causes of death in sea otters have improved
with time. Furthermore, detailed
evaluation of specific patterns of mortality
in sea otters may have broad implications
for overall ecosystem health and may improve
our understanding of the processes
that promote disease in a marine mammal
population. In order to evaluate the recent
pattern of mortality in sea otters, the demographic
and geographic distribution of
causes of death for freshly deceased sea
otters found along the California coast between
1998 and 2001 were evaluated.

Carcass collection and evaluation
Sea otter carcasses were recovered through
a large-scale stranding network conducted by
the California Department of Fish and Game
(CDFG), the United States Geological Survey
(USGS), the Monterey Bay Aquarium (MBA),
and The Marine Mammal Center (TMMC).
Collaborating veterinary pathologists at
CDFG’s Marine Wildlife Veterinary Care and
Research Center (MWVCRC, Santa Cruz, California)
and the University of California (UC)
School of Veterinary Medicine (Davis, California)
examined three of four freshly dead otters;
every fourth carcass was sent to the National
Wildlife Health Center (Madison, Wisconsin,
USA). Necropsy findings from otters examined
at MWVCRC/UC from February 1998 through
June 2001 were included in these analyses.
Stranding location for all otters was determined
at the time of carcass recovery. Otters
were assigned the corresponding latitude and
longitude value of their stranding location to
the nearest 0.5 km increment along a smoothed
California coastline. Stranding locations were
also categorized as north or south based on
their relation to Cape San Martin (358899N,
1218469W), which is at the center of the southern
sea otter range. Age class was determined
at necropsy and was estimated as follows: juveniles—
milk teeth present (younger than 1
yr), subadults—unworn adult dentition (approximately
1–3 yr old), prime-aged adults—
adult dentition with evidence of some tooth
wear (approximately 4–9 yr old), and aged
adults—marked tooth wear (approximately 10
yr and older). When evaluating age as a risk
factor for specific causes of death, age classes
were collapsed into a juvenile category (juveniles
and subadults) and an adult category
(prime-aged adults and aged adults). Pregnancy
and lactation status were recorded for females
at necropsy.
Only otters that were in good postmortem
condition (dead for ,4 days) were included in
this study. Otters heavily scavenged prior to
necropsy and those with incomplete histopathology
were excluded. For otters that stranded
alive but were subsequently euthanized or died
while undergoing rehabilitation, the pathologic
conditions that were the likely cause of stranding
were reported. Otters that remained in rehabilitation
for longer than 4 wk were excluded.
All otters received a complete gross necropsy,
as well as microscopic examination of
major tissues including heart, lung, liver, kidney,
spleen, stomach, small intestine, colon,
omentum, multiple lymph nodes, skeletal muscle,
spinal cord, and brain. Tissue sections were
placed in 10% neutral buffered formalin, paraffin-
embedded, sectioned at 5 mm, and stained
with hematoxylin and eosin for examination by
light microscopy. Acanthocephalan parasites
known to infect sea otters (Hennessy and Morejohn,
1977) were identified to genus by overall
size and proboscis morphology at gross necropsy
(Amin, 1992). Laboratory evaluation of
bacterial, fungal, and parasite samples and toxicologic
screening for domoic acid were performed
when indicated. Swabs for bacterial
culture were collected from heart, blood, intestinal
tract, and lung, plated on tryptic soy
agar with 5% sheep blood, MacConkey agar,
and XLT-4 agar (Hardy Diagnostics, Santa Maria,
California). Plates were incubated at 37 C.
Bacterial isolates were identified by the Microbiology
Laboratory at the UC Veterinary Medical
Teaching Hospital (Davis, California) using
standard biochemical and molecular techniques.
Tissues swabs collected from necropsied
otters with suspected fungal infections
were also submitted to the Microbiology Laboratory.
Samples were placed on wet mounts for the direct observation of spherules. Samples
were also cultured on inhibitory mold agar with
chloramphenicol (Hardy Diagnostics) and incubated
at 30 C in air for 3 wk. If fungal growth
occurred, gross colonial morphology was evaluated
and a lactophenol cotton blue preparation
(Hardy Diagnostics) was made for microscopic
examination of arthroconidia for the
identification of Coccidioides immitis (St Germain
and Summerbell, 1996). Suspect C. immitis
positive cultures were submitted to a specialty
laboratory for confirmation (D. Pappagianis,
Microbiology and Immunology, UC Davis
School of Medicine, Davis, California). On
histopathology, C. immitis was identified by the
presence of round (5–50 mm in diameter),
thick-walled spherules containing endospores.
Death was attributed to domoic acid intoxication
when substantially elevated levels of domoic
acid were detected in urine (Scholin et
al., 2000) and gross or histologic lesions suggestive
of another cause of mortality were absent.
Domoic acid was initially detected by receptor-
binding assay (Dr. Vera Trainer, National
Oceanic and Atmospheric Administration,
Northwest Fisheries Science Center, Environmental
Conservation Division, Marine Biotoxin
Program, Seattle, Washington, USA) and, when
possible, results were confirmed by liquid chromatography-
tandem mass spectroscopy (Dr.
Francis Van Dolah, National Oceanic Atmospheric
Administration, Center for Coastal Environmental
Health and Biomolecular Research,
Marine Biotoxin Program, Charleston,
South Carolina, USA).
Encephalitis was determined to be a primary
cause of death when moderate to severe inflammation
of the cerebral and/or cerebellar
neuropil was present on histopathology (Fig.
1a). This criterion was chosen because moderate
encephalitis was identified histologically in
otters undergoing rehabilitation with recurrent
seizures and severe neurologic dysfunction.
Protozoal infection with either Toxoplasma
gondii or Sarcocystis neurona was determined
to be the cause of encephalitis when protozoal
stages were directly visualized within inflammatory
foci in the neuropil on histopathology
(Fig. 1) and/or when laboratory tests confirmed
infection through isolation of protozoa from
brain tissue (Miller et al., 2001b). Antibody titers
to T. gondii and S. neurona were not used
to diagnose these parasites as the cause of encephalitis
because positive titers do not distinguish
between past exposure and active infection.
Otters with encephalitis but without histopathologic
or laboratory confirmation of protozoal
infection were diagnosed with encephalitis
of unconfirmed cause.
Trauma noted at necropsy was attributed to
shark attack when shark tooth fragments were
recovered from wounds or when multiple stablike
lacerations in soft tissue or scratches, characteristic
of contact with serrated shark teeth,
were detected on underlying bone or cartilage
(Ames and Morejohn, 1980) (Fig. 2). Similarly,
trauma was attributed to boat strike in cases
with soft tissue lacerations and fractures or cuts
in underlying bone in a pattern consistent with
a propeller injury (Ames and Morejohn, 1980).
Severe blunt trauma suggestive of a high speed
collision with a boat hull was also attributed to boat strike. Cases were diagnosed with trauma
or lacerations of unknown cause when clear evidence
for shark attack or boat strike was not
Causes of death were rigorously standardized
so that the primary cause identified for each
otter was the most substantial injury or illness
initiating the sequence of events leading directly
to death. Otters were assigned two equally
weighted primary causes of death if two unrelated
and independent conditions were each
severe enough to have caused death. Contributing
causes of death were noted only if pathologic
conditions were identified that added to
the probability of death, but were not part of
the primary disease complex. To ensure independence
of primary and contributing causes
of death, diagnoses of conditions were based
solely on the severity of the individual lesions
regardless of other conditions present.
Statistical analyses
Proportionate mortality, noted as a percent,
was used to identify the major causes of death
in sea otters from 1998 to 2001. Cause-specific
proportionate mortality was calculated as the
proportion of otters with a specific condition as
the primary cause of death among all otters
that met the inclusion criteria during the study
period. Distribution of the four most common
causes of death among sex and age classes was
evaluated by the standard two-sided chi square
test of independence using statistical software
(Epi Info Version 6, Centers for Disease Control
and Prevention, Atlanta, Georgia, USA).
One-sided chi-square test of independence was
used to test associations between each of the
four most common primary causes of death and
the common contributing causes of death with
at least nine cases each. If age or sex were significantly
associated with a primary cause of
death, associations among primary and contributing
causes of death were stratified by the significant
variable (age or sex), and the association
was evaluated for each stratum. For dichotomous
distributions with an expected frequency
less than five, the Fisher exact test
(Fisher, 1935) was calculated using statistical
software (SPSS Base 10.0, SPSS Inc., Chicago,
Illinois, USA). When appropriate, strength of
the association was estimated by the odds ratio.
Geographic and temporal clustering of overall
carcass retrieval and temporal clustering of
each primary cause of death were evaluated by
the scan test (Carpenter, 2001). This test evaluates
whether carcass retrieval was uniform using
the binomial distribution to estimate the
probability of the maximum observed number
of cases within sequential distances of 5 km, 10
km, 15 km, and 20 km for geographic clustering
and within 1, 2, 3 and 4 mo for temporal
clustering. These spatial and temporal periods
were specified because increased carcass retrieval
within these time periods was considered
biologically significant based on sea otter
behavior and habitat use. Geographic clustering
of specific primary causes of death was evaluated
only for the four most common primary
causes of death with 10 cases or more. Specifically,
the spatial scan statistic (Kulldorf and
Nagarwalla, 1995) was used to test whether a
primary cause of death was randomly distributed
along the coastline where sea otters carcasses
were recovered. The Bernoulli model
was selected for this procedure, which used the
case and control approach to adjust for differential retrieval of carcasses along the coastline.
In this manner, stranding locations for each
specific cause of death were compared to locations
for otters with all other causes of death.
A Monte Carlo iterative technique was used to
determine distribution of the likelihood ratio
test statistic (Kulldorf and Nagarwalla, 1995).

Between February 1998 and June 2001,
105 sea otter carcasses met our inclusion
criteria and received a complete necropsy
and diagnostic work up in order to determine
the cause of death. Of these otters,
27 were alive at the time of stranding but
died or were euthanized at rehabilitation
centers. Sea otter carcass retrieval was spatially
clustered along the coastline during
our study period. Both Monterey Bay and
Estero Bay had significant (P,0.01) clusters
of beachcast carcasses. No carcasses
were retrieved from the remote and rocky
140 km long coastal segment in the center
of the sea otter range south of Yankee
Point (368489N, 1218949W) to north of San
Simeon Point (358639N, 1218199W). Overall
carcass retrieval was not temporally
clustered during the study period. Carcasses
recovered consisted predominantly
of prime-aged adults (46.7%), with fewer
juveniles (29.5%), subadults (11.4%), and
aged adults (12.4%). Distribution of primary
causes of death among sex and age
classes is shown in Table 1. While 25 different
primary causes of death were identified,
53.3% of otters (56/105) died from
one of four major causes: T. gondii encephalitis,
acanthocephalan parasite infection,
shark attack, or cardiac disease. Acanthocephalan
infection, cardiac disease, and
T. gondii encephalitis were also recognized
as common contributing causes of death
(Table 1).
Encephalitis due to T. gondii was one of
the two leading causes of mortality identified
in sea otters during the time period
studied. This condition, characterized by
moderate to severe, multifocal, non-suppurative
and necrotizing meningoencephalitis
(Fig. 1), was a primary cause of death
in 16.2% of the otters examined and was
a contributing factor in another 11.4% of
otters examined. A marginally significant
spatial cluster of T. gondii encephalitis cases
was detected in a 25 km area at the
southern end of Estero Bay in central California
(P50.06, centered at 358319N,
1208889W, Fig. 3). Half of the otters (8/16)
recovered in this section of Estero Bay
were determined to have T. gondii encephalitis
as the primary cause of death.
Encephalitis caused by S. neurona was
characterized by severe, necrotizing,
mixed non-suppurative and suppurative
encephalitis, which was often most severe
in the cerebellum and brainstem. Encephalitis
due to S. neurona was the primary
cause of death identified in 6.7% of otters,
all of which were detected during spring
months (March through May). Cases were
significantly clustered temporally in the
spring of 2001 (P50.01). Purely suppurative
encephalitis was detected in only one
sea otter, but the primary cause of death
in this case was attributed to facial bite
wounds, which caused a ganglioneuritis
and ascending infection with Archanobacterium
phocae. Encephalitis of unknown
or unconfirmed cause was a primary cause
of death for another 4.8% of otters examined.
Overall, encephalitis of all types
caused death in 28% of otters examined
and contributed to death in another 18%
of otters.
Similar in proportionate mortality to T.
gondii encephalitis, infection with acanthocephalan
parasites was a primary cause
of death in 16.2% of otters examined, and
this parasite contributed to death in another
9.5% of otters. Septic peritonitis, caused
by migrating Profilicollis spp., was the
most common consequence of heavy acanthocephalan
infection (Fig. 4). This type of
peritonitis was the primary cause of death
in 14.3% (15/105) of otters examined and
was 3.5 times more likely to have caused
death in juveniles and subadults than
adults or aged adults (two-sided chi square
test, P50.03). Acanthocephalan infection
either directly caused, or was a contributing
factor for, death in 40% (17/43) of the juvenile and subadult otters examined. A
geographic cluster of acanthocephalan
peritonitis was detected at the southern
end of Monterey Bay (P50.02, centered at
368609N, 1218889W, Fig. 3). In this 1.8 km
area, five of six carcasses recovered had
acanthocephalan peritonitis as a primary
cause of death, while only one case was
expected if this condition had been distributed
evenly across locations where carcasses
were recovered along the coast. The
sixth carcass recovered in this area had
acanthocephalan peritonitis as a contributing
cause of death.
Shark-inflicted mortality was detected in
13.3% of otters examined. All cases had
bite wounds that were consistent with attack
by white sharks (Carcharodon carcharias,
Fig. 2). A significant spatial cluster
of otters attacked by sharks was noted in
the 80 km stretch of coastline from Point
An˜ o Nuevo to Santa Cruz (P50.02, centered
at 378119N, 1228339W, Fig. 3). In this
area, six of 10 otters recovered were killed
by sharks, while only 1.3 cases of shark attack
were expected had this condition
been distributed evenly in areas where
carcasses were recovered. Histopathologic examination of brain tissue from shark-attacked
otters revealed that eight of 14 otters
(57%) attacked by sharks had pre-existing
encephalitis. Otters with moderate
to severe T. gondii encephalitis were 3.7
times more likely to be attacked by sharks
than otters without this condition (one-sided
Fisher exact test, P50.05). Shark-inflicted
mortality was not significantly associated
with acanthocephalan infection,
cardiac disease, or emaciation.
Cardiac lesions in otters were newly recognized
during this study period and cardiac
disease was diagnosed as a primary
cause of death in 13.3% of otters examined.
Cardiac lesions consisting of mild to
severe non-suppurative (lymphocytic)
myocarditis (Fig. 5) were a common finding
in otters examined (n541). These lesions
were considered a cause of death
only when myocarditis was accompanied
by a grossly enlarged, rounded, dilated,
and thin walled heart (Fig. 5) and/or
strong evidence for congestive heart failure
(pulmonary edema, pleural and peritoneal
effusion, and hepatic congestion).
Nearly all cardiac disease cases were observed
in prime-aged adults or aged adults,
and this condition was 3.5 times more likely
to be a primary cause of death in females
than males (two-sided chi square
test, P50.04). Severe nose wounds were found in half of the otters (7/14) with cardiac
disease as a primary cause of death.
Nose wounds are commonly acquired by
females during mating (Staedler and Riedman,
1993) but also result from intraspecific
aggression in males. Both male otters
with severe nose wounds had cardiac disease
as a primary cause of death (one-sided
Fisher exact test, stratified on sex,
P,0.01) and five of nine female otters with
severe nose wounds had cardiac disease as
a primary cause of death (one-sided Fisher
exact test, stratified on sex, P50.01). In all
cases, severe nose wounds were acute or
subacute and seemed to have occurred after
development of cardiac disease. While
significant localized geographic clusters of
cardiac disease cases were not detected,
otters with this condition were 5.6 times
more likely to be recovered from the
southern half of the California sea otter
range (two-sided chi square test, P,0.01),
which is also where the cluster of T. gondii
encephalitis was detected. Otters diagnosed
with cardiac disease were 2.9 times
more likely to have concurrent T. gondii
encephalitis than otters without cardiac
disease (one-sided chi square test,
P50.01). Cardiac disease was not associated
with any other common contributing
cause of death.
While emaciation was not determined
to be a primary cause of death in any otters
examined, emaciation was identified
as a contributing cause of death in 15% of
otters. Emaciation was most significantly
associated with cardiac disease (one-sided
Fisher exact test, P50.01) and was 3.2 times more likely to be a contributing
cause of death in females than males (twosided
chi square test, P50.03). Of 27 adult
and aged adult females that were necropsied,
nine were confirmed to be lactating
at the time of death. Most lactating females
(7/9) were emaciated at death and
four of nine lactating females had cardiac
disease as a primary cause of death.
Infectious diseases (caused by parasites,
bacteria, and fungi) and diseases without a
specified etiology (cardiac disease, intestinal
disease, and encephalitis of unconfirmed
cause) were implicated as a primary
cause of death in 63.8% of otters examined.
Disease was most commonly a primary
cause of death in prime-aged adults
(n530) compared to juveniles (n519),
subadults (n510), and aged adults (n58).
Parasitic diseases alone, caused by T. gondii,
S. neurona, and Profilicollis spp, were
determined to be a primary cause of death
in 38.1% of the otters examined.


Encephalitis, caused by T. gondii and S.
neurona, was first recognized as a source
of mortality in sea otters only after detailed
necropsies were begun in 1992 (Cole et
al., 2000; Lindsay et al., 2000; Miller et al.,
2001a). Because encephalitis can only be
diagnosed by microscopic examination of
brain tissue, this cause of death was likely
missed in the past when carcasses were
not examined in such detail. However, the
reported percent of mortality attributed to
protozoal encephalitis appears to have increased
substantially over the short period
during which detailed examinations have
been undertaken. Of otters examined from
1992–95, 8.5% had protozoal encephalitis
while 22.9% of otters we examined had
protozoal encephalitis as a primary cause
of death. This apparent increase in prevalence
may be a consequence of improved
diagnostics, a difference in criteria for establishing
this diagnosis among laboratories
and pathologists, or temporal variation
in the occurrence of this disease. Other
causes of encephalitis should also be considered,
particularly for cases with an as
yet unconfirmed cause. However, the magnitude
of this most recent temporal trend
certainly warrants attention, particularly as
the increased prevalence of this condition
coincides with a period of population decline.
Protozoal infections in sea otters may be
examples of spillover of land-based pathogens
into the marine ecosystem because
the only identified definitive hosts for T.
gondii and S. neurona are felids and opossums
(Didelphis virginiana), respectively.
The spatial cluster of mortality due to T.
gondii encephalitis in Estero Bay may be
a consequence of local factors, such as increased
sea otter exposure to T. gondii, enhanced
parasite virulence, or increased sea
otter susceptibility in this particular area.
In a separate study, sea otter carcasses
found in Estero Bay had higher prevalence
of antibodies to T. gondii than otters sampled
elsewhere (Miller et al., 2002), suggesting
that mortality may be due to high
levels of parasite exposure. Seasonal peaks
of T. gondii encephalitis mortality in otters
were not detected even though coastal
freshwater runoff has been associated with
increased odds of exposure to T. gondii in
sea otters (Miller et al., 2002). Runoff is
highest during the winter rainy season and
spring in California. However, many unrecognized
environmental and host factors
could affect the timing of death from this
disease. Otters with S. neurona encephalitis,
which may be a more acutely severe
and rapidly progressive disease, stranded
only in spring months (March through
May), which follows maximal seasonal runoff
and coincides with the season when
opossums were more likely to shed sporocysts
(Rickard et al., 2001).
While infection with T. gondii is common
in terrestrial mammals, it is usually
subclinical in immune competent hosts
(Frenkel, 1988). Disseminated systemic
disease with severe brain infection is more
typical of immune suppressed humans,
such as HIV infected AIDS patients (Arnold
et al., 1997). Fatal T. gondii infections have been reported in neotropical marsupials
and nonhuman primates, which
evolved in ecologic isolation from domestic
cats (Frenkel, 1988). Expansion of domestic
cat and opossum populations and
decreased natural filtration of watershed
runoff through coastal estuaries may have
increased sea otter exposure to a pathogen
for which they are immunologically ill-prepared.
These protozoal pathogens are not
likely to have been abundant in the marine
environment centuries ago. The substantial
proportionate mortality caused by protozoal
encephalitis in juvenile and prime
aged adult otters is of concern, particularly
because T. gondii encephalitis was shown
here to be associated with two other important
causes of death, shark attack and
cardiac disease. If T. gondii infection increases
the risk of death from shark attack
or cardiac disease, this parasite may have
a complex but critical role in a high level
of mortality in sea otters.
Toxoplasma gondii infection may have
other deleterious effects that are difficult
to document by the methods used here.
Fetal infection with T. gondii is associated
with serious birth defects and a high frequency
of abortion in terrestrial animals
and humans. These effects would be difficult
to detect in free-living sea otters because
aborted fetuses and pups that die
shortly after birth are less likely to be
found in fresh condition. Underlying causes
for the perinatal mortality noted in recovered
pup carcasses could not be determined
but all were near full term pups
that died shortly after birth and none had
pathologic findings consistent with protozoal
The high prevalence of pre-existing T.
gondii encephalitis in shark attacked otters
suggests that otters with encephalitis may
exhibit aberrant behavior that renders
them more vulnerable to attack by sharks.
Otters with protozoal encephalitis frequently
exhibit fine muscle tremors, recurrent
seizures, dull mentation, and decreased
or abnormal motor function (M.
Murray, pers. comm.). Neurologic dysfunction
might cause otters to be less able
to evade attacks, to move offshore out of
the protected areas, or to attract shark attention
through abnormal movements and
seizures. Wounds inflicted upon otters by
sharks were typically large gashes with
minimal soft tissue removal, consistent
with open-mouth slashing or raking by
sharks (Fig. 2). This bite pattern is similar
to that seen when sharks attack humans
(Byard et al., 2000) and is not consistent
with a bite pattern used for intended prey.
Sharks feeding on pinniped prey often remove
large pieces of soft tissue (Lucas and
Stobo, 2000). The wound pattern observed
in otters suggests that they may not be intended
prey and the high percent of sharkattacked
otters with pre-existing encephalitis
is consistent with the hypothesis that
sharks are more likely to attack otters if
they are acting abnormally.
The area from Santa Cruz to Point An˜ o
Nuevo with high shark-related mortality in
sea otters is known for white shark predation
on pinnipeds (Long et al., 1996).
Shark-inflicted mortality has been longrecognized
as an important cause of mortality
in sea otters since carcasses were first
evaluated in 1968 and the number of
shark-bitten beachcast carcasses has varied
considerably by year (Ames et al., 1996).
However, the annual proportion of sharkattacked
sea otter carcasses relative to the
annual population count has increased
through time particularly during periods of
population decline (Estes et al., 2003). Because
interactions with sharks may be
modified by encephalitis in otters, prevalence
of shark attack may be linked to
prevalence of encephalitis. Both shark attack
and encephalitis may be under-represented
as a cause of death if carcasses
with penetrating wounds from shark bites
are more likely to sink than wash ashore
(Lucas and Stobo, 2000) or if otters are
consumed by sharks, although the latter
has never been observed.
Cardiac disease has not previously been
reported in sea otters and the substantial
percent of deaths attributed to cardiac disease was unexpected. Stress-related cardiac
disease has been documented in
stranded cetaceans (Turnbull and Cowan,
1998), but the contraction band-necrosis
of myocardium detected in dolphins and
whales differed from the pattern of nonsuppurative
myocarditis and gross cardiac
dilation observed in sea otters. The inflammatory
nature of the cardiac lesions noted
here suggests an infectious etiology although
infectious agents were not detected
during microscopic examination of sea
otter myocardium. Our observation that
otters with cardiac disease are more likely
to have concurrent T. gondii encephalitis
implies that these two conditions are causally
linked or are somehow coupled by an
unknown mechanism. Rare accounts of
myocarditis in animals infected with T.
gondii have been reported in dolphins
(Inskeep et al., 1990), a northern fur seal
(Callorhinus ursinus; Holshuh et al.,
1985), and a California sea lion (Zalophus
californianus; Migaki et al., 1977), although
disseminated toxoplasmosis with
protozoal cysts in cardiac myofibers were
observed in all cases. In humans, T. gondiirelated
cardiomyopathy has been documented
in AIDS patients (Matturri et al.,
1990) and immune-suppressed heart
transplant patients (Arnold et al., 1997).
Efforts are currently being directed at understanding
the immunopathology of toxoplasmosis
in sea otters, improving detection
methods for protozoal stages, and
evaluating other possible etiologies and
risk factors for cardiac disease.
Cardiac disease was a common cause of
death in female otters and was often associated
with severe nose wounds and
emaciation. Emaciation and severe nose
wounds may be a secondary consequence
of the debilitating effects of heart failure,
which could prevent afflicted otters from
foraging effectively and defending themselves
against aggressive males. Adult females
appear to be highly susceptible to
both mating trauma and emaciation, particularly
at the end of lactation, possibly
because they are at a nutritional disadvantage
after caring for a pup and entering
estrus, which attracts male attention. The
transition from pup care and lactation to
estrus and breeding appears to be a particularly
vulnerable period for adult female
sea otters in California.
Acanthocephalan peritonitis continues
to be a substantial cause of mortality in sea
otters, and the recent prevalence (16.2%)
is similar to the 14% reported from 1992–
95 (Thomas and Cole, 1996). Sand crabs
(Emerita analoga) and possibly spiny mole
crabs (Blepharipoda occidentalis) serve as
intermediate hosts for these acanthocephalan
parasites (Hennessy and Morejohn,
1977), and these crabs are found in predominantly
sandy habitat. It is therefore
likely that otters foraging in sandy bays will
have a high level of exposure to Profilicollis
spp. As expected, mortality due to acanthocephalan
peritonitis during this study
period was detected exclusively in carcasses
retrieved from Monterey Bay and Estero
Bay, both of which are largely sandy
habitat. While sand crabs may not be preferred
sea otter prey, they are abundant
and easy to capture. Juvenile otters may
ingest large numbers of these prey species
when they are first searching for suitable
home-range habitat and learning to forage
on their own, which may explain the high
level of exposure and subsequent mortality
in this age class.
Even though acanthocephalan peritonitis
is readily apparent at necropsy through
gross evidence of peritonitis associated
with parasites in the abdominal cavity, this
condition was reported only once in necropsies
performed on otters from 1968–76
(Hennessy and Morejohn, 1977), suggesting
that fatal acanthocephalan infections
may have increased in prevalence. The apparent
increased prevalence of acanthocephalan
peritonitis may reflect increased
host susceptibility to infection or increased
exposure through a shift in preferred prey
availability, intermediate host abundance,
foraging behavior, or habitat use. Southerly
otter range expansion into the predominantly
sandy habitat south of Point Estero is unlikely to have contributed substantially
to the higher prevalence of this
condition in recent years because 80% of
the otters with fatal acanthocephalan infections
from 1998–2001 were retrieved
from Monterey Bay, which has been occupied
by sea otters since the 1970s (Riedman
and Estes, 1990).
Domoic acid intoxication has not been
previously reported in sea otters and necropsy
findings and preliminary laboratory
tests suggest that domoic acid intoxication
was a primary cause of death in four otters
examined here. Domoic acid is a marine
biotoxin produced by Pseudonitzchia spp.
and is known to cause severe neurologic
dysfunction and death in California sea lions
(Scholin et al., 2000) and seabirds
(Work, 1993). Domoic acid exposure
caused characteristic brain and cardiac lesions
in sea lions (Scholin et al., 2000), and
histologic lesions associated with domoic
acid exposure in sea otters are currently
being evaluated. Domoic acid intoxication
may be established as a more common
cause of mortality in sea otters once diagnostic
capabilities are refined and
screening is performed more routinely.
Coccidioidomycosis, caused by the soil
fungus C. immitis was diagnosed as a primary
cause of death in only one otter (1%)
during our study period. In otters examined
from 1992–95, eight cases had severe
disseminated coccidioidomycosis (Thomas
and Cole, 1996), so there may be some
variation in mortality due to this pathogen.
Our approach of identifying more than
one primary cause of death in sea otters
with two equally severe, yet independent,
causes of death has resulted in slightly
higher proportionate mortality for some
conditions than if diagnoses had been limited
to one primary cause of death per otter.
This strategy allowed for an unbiased
account of important causes of death, but
the proportionate mortality reported here
may not be comparable to mortality studies
using more traditional methods. Also,
many of these causes of mortality may be
subject to substantial inter-annual variation
and other causes of mortality are likely
to be identified retrospectively as new
diagnostic techniques are developed and
implemented as screening tools.
In this study, carcasses were recovered
primarily along accessible sandy shores.
Sea otter carcasses are not likely to wash
ashore along rocky precipitous coastlines
and those that do are not likely to be recovered
while in fresh condition because
most of these areas are not readily accessible. 
[3] Therefore, very little is known of
causes of mortality in sea otters living
along the rocky and remote coastline in
the center of the sea otter range in California.

A directed search effort would be
necessary to collect fresh carcasses from
these unpopulated and inaccessible areas.
An estimated one-half of all recently deceased
sea otters were recovered as beachcast
carcasses, and one-fourth of these
were retrieved in adequately fresh condition
to allow detailed necropsy for specific
cause of death determination (Estes et al.,
2003). Based on these estimates and the
specific inclusion criteria for this study, approximately
one of ten deceased southern
sea otters was evaluated. Because the age
distribution of carcasses reported here
closely matches the age distribution of all
carcasses recovered recently (Estes et al.,
2003), the carcasses included in this study
are likely to be representative of all recovered
carcasses. Consequently, the major
causes of death reported here are probably
similar to what would be observed if detailed
cause of death information could be
obtained from decomposed or heavily
scavenged carcasses. While a relatively
high proportion of the population was
available for cause of death determination,
certain causes of death, such as drowning
due to accidental entanglement in fish
traps or nets, may be under-represented in
beachcast carcasses. These carcasses may
be less likely to float and wash ashore prior
to decomposing, and drowning is very difficult
to document even with detailed necropsy.
Therefore, the cause-specific proportionate
mortality reported here may not be directly referable to the southern
sea otter population.
Identification of pathogens responsible
for substantial morbidity and mortality in
sea otters and the geographic distribution
of these pathogens is an important first
step toward understanding the role of population
health in the recovery of this
threatened species. However to fully understand
the underlying mechanisms creating
the observed pattern of mortality,
factors that may be affecting nutrition, immune
system competency, and sources of
increased pathogen exposure must be evaluated.
Studies have detected elevated tissue
levels of potentially immunotoxic contaminants
in southern sea otters with infectious
disease (Kannan et al., 1998; Nakata
et al., 1998), but immune system
function in wild animals is difficult to measure
because species-specific tests must be
developed and validated for different age
The high percent of prime-aged adults
among beachcast sea otter carcasses in
California, and the very high prevalence of
disease noted in this age class are not consistent
with a healthy population destined
for recovery. Sea otter populations experiencing
a decline from increased levels of
mortality typically have a high percent of
prime-aged adults among beachcast carcasses
(Estes et al., 2003). Certainly, the
prevalence of acanthocephalan-related disease
in juveniles and the prevalence of T.
gondii encephalitis, cardiac disease, and
shark attack in prime aged adults have the
potential to exert a population-level effect
and may be limiting sea otter population
growth in California. The underlying processes
promoting increased levels of parasitic
disease in sea otters should be a focus
of future investigation. Special attention
should be given to non-native terrestrial
species that are endemically infected
with protozoal pathogens and have the capacity
to serve as a reservoir for persistent
exposure and infection in sea otters. Recovery
of the southern sea otter population
may face a significant challenge as this isolated
population struggles to expand in a
near-shore system that may have been substantially
altered in terms of prey abundance,
water quality, and pathogens in the
time since the near-extirpation and early
recovery of sea otters.
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