Biological Report 90 (14)

September 1990

The Sea Otter (Enhydra lutris):

Behavior, Ecology, and Natural· History

U.S. Department of the Interior

 Biological Report 90 (14)
September 1990

The Sea Otter (Enhydra lutris): Behavior,

Ecology, and Natural History

By

Marianne L. Riedman and James A. Estes

U.S. Department of the Interior

Fish and Wildlife Service
Washington, D.C. 20240
 \'

Biological Report
This publication series of the Fish and Wildlife Service comprises reports on the results of research, developments
in technology, and ecological surveys and inventories of effects of land-use changes on fishery and wildlife resources.
They may include proceedings of workshops, technical conferences, or symposia; and interpretive bibliographies.

Copies of this publication may be obtained from the Publication Unit, U.S. Fish and Wildlife
Service, 1849 C Street, N.W., Mail Stop 130-ARLSQ, Washington, DC 20240, or may be
purchased from the National Technical Information Service (NTIS), 5285 Port Royal Road,
Springfield, VA 22161.

ISSN 0895-1926
 Contents
Page
Abstract . . . . . . . . . . . . .
Evolution . . . . . . . . . . . . . 2
Phylogeny and Fossil Records 2
Environment . . . . . . . . . 4
Adaptations Associated with a Marine Existence 5
Classification and Taxonomy . 7
Classification of Sea Otters . 7
Subspecies of Sea Otters . 10
Morphology and Physiology 13
Body Measurements . . . 13
Lifespan and Age Determination . 14
Dentition . . . . . . . . . 15
Forelimbs and Hindlimbs . 15
Swimming Speeds 15
Sensory Organs . . . . . . 15
Internal Organs . . . . . . 20
Pelage and Grooming Behavior 20
Metabolism and Energetics . 21
Ecology . . . . . . . . . . 22
Habitat Characteristics . . . 22
Haul-out Behavior . . . . . 24
Role in Marine Communities . 25
Foraging Behavior and Diet . . . 31
Feeding and Diving Behavior 31
Food Stealing . . . . . . . . . 32
Tool Use . . . . . . . . . . . 33
Individual Variation in Diet and Foraging Tactics . 34
Diet in Alaska and the Soviet Union 36
Diet in California . . . . . . . . . . . . 41
Predation on Seabirds . . . . . . . . . 44
Effects of Paralytic Shellfish Poisoning 45
Activity Patterns and Time Budgets . 45
Social Organization and Behavior . . 48
Social Structure and Behavior . . 48
Communication and Vocalization 50
Sexual Segregation . . . . . . . . 53
Sex and Age Composition in California 53
Sex and Age Composition in Alaska . 54
Home Range and Movements 54
Reproduction . . . . . . . . . . 59
Seasonal Phases of Breeding 59
Mating Behavior . . . . . . 60
Reproduction in the Male . . 62
Reproduction in the Female 64

ii

.,____.,._. __ ~- - -- --- ·- ----- - - - - - - -- -~- -- --· ------- ------·--

 Population Dynamics . . . . . . . . . . . . . . 73
Historical Distribution and Abundance . . . 73
Status of the California Sea Otter Population 76
Demographic Variables Affecting Dynamics of the California Population 81
Sources of Documented and Potential Mortality . . . . . . . . . . . . . . . 83
Documented Mortality . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
Potential or Undocumented Sources of Mortality or Pathological Disorders 91
Potential and Documented Effects of Oil Contamination 93
Review of Sea Otter Reintroductions in North America 96
Introduction . . . 96
Alaska. . . . . . 96
British Columbia 97
Washington 99
Oregon . . . . . 100
California . . . . 100
Summary and Conclusions 102
Acknowledgments . . . 102
References . . . . . . . 103
Unpublished References 112
Index . . . . . . . . . . 117

lll

...
 The Sea Otter (Enhydra lutris): Behavior,
Ecology, and Natural History

by

Marianne L. Riedman
Monterey Bay Aquarium
Research Division
886 Cannery Row
Monterey, California 93940

and

James A. Estes
U.S. Fish and Wildlife Service
Institute of Marine Sciences
University of California
Santa Cruz, California 95064

ABSTRACT.-The sea otter (Enhydra lutris) represents a clade that separated from the primitive
lutrine carnivores by at least the upper Miocene. One extant species and three subspecies are
recognized. Many aspects of their morphology and physiology are unique among the lutrines but are
similar to the pinnipeds, probably reflecting selection and adaptation for marine living. Sea otters feed
on a broad range of benthic invertebrates and often limit prey populations. These interactions have
broad-ranging ecological and evolutionary consequences.
Sea otters use rocks or other hard objects as tools to break the exoskeletons of their invertebrate
prey; except for a number of primate species, this behavior is unique among mammals. There is growing
evidence that sea otters have highly individualized diets and patterns of foraging behavior. The species
senses and avoids paralytic shellfish toxin. Foraging activity and diurnal patterns seem to vary in
relation to population status and food availability. Sea otters are strongly polygynous. Adult males
defend contiguous territories from which they exclude other males, perhaps causing males to congre-
gate in suboptimal habitats or at the ends of a population's range. Daily movements usually encompass
a few kilometers, although otters occasionally move longer distances, and seasonal movements occur
among some age-sex classes in certain areas. Reproduction is weakly seasonal, with most young born
during late winter in California and early summer in Alaska. Females become sexually mature at about
3 years and typically give birth to a single pup each year thereafter.
Mortality is poorly known, although entanglement in fishing nets probably has limited the population
in central California. Undisturbed populations can increase at about 17-20% yr- 1, although the central
California population has never increased at >5-7% yr-l. Home range fidelity and postrelease dispersal
are probably the principal barriers to successful reintroductions. Reintroduced populations have been
established in southeast Alaska, British Columbia, and Washington. Similar efforts at other locations
were unsuccessful or their status is undetermined.

More than two decades have passed since Kenyon mid-to-late 1960's. Use of SCUBA diving gear has
(1969) published his comprehe[\sive monograph on the opened a whole new world to marine ecologists-this
sea otter in the eastern Pacific Ocean. Since that time, includes the shallow sea floor of the North Pacific rim,
several notable developments have contributed to a large where sea otters obtain most of their prey. Interactions
increase in knowledge about this interesting species. Un- among sea otters, sea urchins, and kelp beds compose a
dersea research did not really come into its own until the now well-known story to community ecologists, and
 2 BIOLOGICAL REPORT 90 (14)

nearly all this information has been assembled during the the preparation of this report (Riedman 1987). We subse-
past 15 years. Similarly, major technical advances in quently reasoned that much of what had been uncovered
radiotelemetry and other remote sensing methods have and synthesized in preparing the EIS would be of broad
been made during recent years. These techniques have and lasting interest, but that this information needed to be
permitted researchers to answer questions about the phys- made more readily available. Therefore, we decided to
iology, behavior, and population biology of free-ranging expand the review to include several important topics not
animals that were difficult (if not impossible) to answer covered in the original draft.
before. The use of radiotelemetry has provided important Our purpose is to provide a current review of the biol-
new information (most of which has been assembled ogy, ecology, and behavior of the sea otter. We also offer
during the past 6 or 7 years) concerning the movements, some of our own thoughts in the form of various synthe-
activity patterns, life history, and population dynamics of ses, interpretations, and previously unpublished data.
sea otters. This account is not an even-handed effort to review ev-
Effective procedures for field-marking sea otters were erything known about sea otters-although we have at-
unavailable at the time Kenyon's monograph was pub- tempted to cover the results of studies done in Alaska,
lished; researchers in the field therefore had no means of Canada, and the Soviet Union, we have emphasized the
maintaining longitudinal records of individual sea otters population and its habitat in central California. And al-
beyond the brief time visual contact with an animal could though, inevitably, we have touched on several of the
be kept. By the mid-1970's, State and Federal biologists management and conservation problems facing sea otters
had begun to develop and use hindflipper tags that al- (such as the conflicts with shellfisheries and concerns
lowed individual sea otters to be recognized in the field. about oil pollution) in large part we have chosen to omit
In addition, procedures and equipment for capturing sea these controversial and difficult issues.
otters have been greatly improved over the past several
years. These improvements have led to a significant shift
in behavioral studies, from the population as a whole, to Evolution
the individual level, in such areas as foraging behavior,
movements, social behavior, reproduction, and survival.
Perhaps the most significant development that has Phylogeny and Fossil Records
helped increase our knowledge of sea otters over the past
20 years was the growth of environmental awareness in Based on the observed dichotomy among species for-
the 1960's and 1970's, which gave rise to an elevated aging on fish or invertebrates, Pohle ( 1919) divided living
public concern for wildlife and, no doubt, passage of two otters into "fish-otters" and "crab-otters." He presumed
important Federal acts: the Marine Mammal Protection these groups to be distinct phylogenetic lineages. More
Act of 1972 and the Endangered Species Act of 1973. recently, based on dentition (van Zyll de Jong 1972) and
These, in tum, led to Federal and State agencies hiring cerebral morphology (Radinsky 1968), the nominal
additional people and spending more money to learn "crab-otters" were presumed to contain two lineages. By
about sea otters. Most of the large volume of published this view the fish-eating forms (represented by the extant
and unpublished work on sea otters that was generated in Lutra andPteronura) are primitive, and crab-eating forms
the United States during the past 15 years surely would were twice derived from the fish-eating lineage. In one
not have been done had it not been for this legislation. lineage, represented by extant species of Aonyx, shearing
In 1985, the Fish and Wildlife Service began to seri- ability of the camassials was retained. In the other, repre-
ously consider the possibility of reintroducing sea otters sented by the extant sea otter (Enhydra) and the extinct
to an area currently uninhabited. by otters in California to Enhydritherium andEnhydriodon, the carnassial shearing
reestablish a second population in order to ( 1) hasten function was lost to progressively improved crushing
recovery of the species from its legally threatened status ability; in addition, body size was much larger.
under the Endangered Species Act, and (2) provide scien- Cladistic relationships among the sea otters, other lutr-
tific information about the sea otter and its habitat that ine carnivores, and other mustelids have been proposed
seemed unobtainable by other reasonable means. Because by Berta and Morgan (1985). In their view, there are two
of the highly controversial nature of this proposal, it was lineages of sea otters: one leads to the extinct En-
decided that an environmental impact statement would be hydriodon, the other to the extinct Enhydritherium and
required, which in large part was prepared through a the extant Enhydra. Extinct lineages are known mainly
cooperative arrangement between the Fish and Wildlife from dental morphology and tooth fragments. All known
Service and the University of California at Santa Cruz. fossils of Enhydriodon are from Eurasia and Africa, with
One of us (M.R.) was contracted to write a review of three well-described species: E. sivalensis (Falconer
those aspects of sea otter biology deemed relevant to the 1868) from the Pliocene of India, E. falconeri (Pilgrim
reintroduction project. That document was a first step in 1931) from the late Miocene of India, and E. african us,

...'
·-·--··-·-------------------
 THE SEA OrrER: BEHAVIOR, EcoLOGY, AND NATURAL HisTORY 3

from several sites in Africa (Stromer 1931; Hen dey 1978). originated in the Old World. Its specific route of immigra-
In addition, several specimens with more poorly under- tion to North America remains unclear, although several
stood affinities have been provisionally assigned to En- possibilities have been suggested. One possibility is that
hydriodon, including Enhydriodon latipes (Pilgrim the lineage dispersed from Eurasia to North America by
1931) from the late Miocene of Greece, E. reevei (Newton way of the Bering Land Bridge. with a second phase of
1890) from the late Pliocene of England, and as yet un- dispersal from the Pacific Ocean to the Atlantic Ocean
named material from east Africa (Howell and Petter 1979). through the Central American Seaway between 6 and
Enhydritherium is known from the late Miocene of 8 million years ago. This view has one clade in the North
Europe and the late Miocene-middle Pliocene of North Atlantic represented by Enhydriodon reevei, and another
America (Berta and Morgan 1985). Two species have in the North Pacific that led to Enhydra from a form
been described: E.lluecai from the late Miocene of Spain resembling E. lluecai. A second possibility is that En-
(Villata Comella and Crusafont-Pairo 1945; Crusafont- hydriodon reevei dispersed from the North Atlantic to the
Pairo and Golpe 1962), and E. terraenovae from the late North Pacific by way of the Arctic Ocean. A specimen
Miocene (6-7 million years ago) to middle Pliocene similar to Enhydriodon reevei from the late Pliocene in
(3.2-3.7 million years ago) faunas of Florida and Califor- Alaska prompted Repenning (1983) to suggest that this
nia (Berta and Morgan 1985; Fig. 1). route of dispersal and subsequent evolution led to En-
The lineage dichotomies proposed by Berta and Mor- hydra in the North Pacific. A third possibility, apparently
gan (1985) are distinguished as follows: (1) sea otters favored by Berta and Morgan ( 1985), is that Enhydrither-
from other mustelids: P 1, lost: short, robust jaw; broad ium dispersed from Europe around the rim of the North
M 1, with low, inflated cusps; (2) Enhydriodon from En- Atlantic and into the Pacific by way of the Central Amer-
hydritherium: very large size; p-+ with isolated hypocone; ican Seaway in the late Miocene.
4
(3) Enhydritherium and Enhydra from Enhydriodon: P Repenning (1976a) wrote that " ... En hydra appears to
triangular, lacking parastyll; deep masseteric fossa termi- be a product of the Pacific and to have never escaped from
nating below M2; ventral border of ramus sharply up- there." The earliest occun·ence of Enhydra is still uncer-
turned and flattened posteriori y; M 1 metaconid larger tain. There are two records from the early Pleistocene: one
than proconid; and M1 with s~uared off talonid; (4) En- from Cape Blanco, Oregon (Leffler 1964 ), and the other
hydritherium from Enhydra: P protocone in anteromed- from Moonstone Beach, California (Repenning 1976a).
ial position; M1 metastylid present, lacking talonid; and Mitchell ( 1966) reported Enhydra from the Timms Point
(5) Enhydra is distinguished by having greatly inflated Silt Member of the San Pedro Formation, California, and
4
tooth cusps; P with reduced hypoconal crest; and M1 with dated the specimen (uncertainly) as late Pliocene-early
metastylid lost and metaconid extending far posteriorly. Pleistocene. On the basis of more recent marine micro-
Enhydritherium seem to have lived exclusively in or fossils from the area, Repenning ( 1976a) suggested that
near coastal marine habitats. Berta and Morgan (1985) an early Pleistocene date for this specimen is more likely.
based this conclusion on the absence of Enhydritherium One extinct species, Enhydra macrodonta (Kilmer
from other Hemphillian faunas in the interior of North 1972) has been described from the late Pleistocene of
America. From this fossil distribution, they surmised an California. The species was separated from the extant E.
epicontinental route of dispersal between the Atlantic and lutris on the basis of greater size of the posterior cheek
Pacific oceans, rather than by way of freshwater or terres- teeth, a longer tooth row, and a more generalized coronoid
trial habitats. process of the mandible.
The Enhydritherium-Enhydra lineage apparently In sum, the lutrine lineage that led to modem sea otters

Fig. 1. Cladogram of the Lutrinae (Berta and

Morgan 1985).
4 BIOLOGICAL REPORT 90 (14)

apparently diverged from the primitive otters late in the genera have been reported elsewhere in the world, and
Miocene or early in the Pliocene, 7 to 5 million years ago. only one of these (Phyllaria) is unknown from the North
Current evidence (Berta and Morgan 1985) suggests that Pacific. Furthermore, kelp radiations appear to be recent,
this lineage had a Eurasian origin, with various early and therefore probably occurred in an environment con-
forms having been widely 'distributed in Eurasia and taining sea otters or their early ancestors. Two kinds of
North America, and even extending into Africa. The mod- evidence support this contention, one of which is pale-
em sea otter (Enhydra) arose in the North Pacific at about oclimatological. The North Pacific was distinctly tropi-
the start of the Pleistocene-about 1 to 3 million years cal-subtropical as recently as the middle Miocene (Ad-
ago--and has since been confined to the North Pacific dicott 1970). Since the Bering Land Bridge was closed at
basin. that time, the northernmost extent of the Pacific basin was
probably too warm for most kelps-at least, all modem
species.
Environment Other evidence for recent kelp radiations comes from
kelp-associated faunas, which, unlike the kelps, left a
Two important events may have led to the evolution of good fossil record. One group of particular interest is the
sea otters as invertebrate predators in coastal marine limpets (Patellogastropoda), which are old and broadly
habitats. One was a global cooling trend at high latitudes distributed, and which left an excellent fossil record.
in the late Cenozoic. The southern distributional limit of Some limpet species are obligate associates on kelp
sea otters in the eastern Pacific coincided with areas of stipes. These limpets are recognizable by a saddle-shaped
coastal upwelling, and the associated distribution of kelp shell that enables them to fit tightly against cylindrically
forests (Kenyon 1969; Estes 1980). This distribution pat- shaped kelp stipes. Five species of saddle-shaped limpets
tern corresponds with the 20-22° winter minimum iso- are known from four subfamilies. All of these species
therm, which occurs at about latitude 23° north (Durham appeared in the Pleistocene (Carlton 197 6; Lindberg
1950). In the early Miocene, the 20-22° isotherm oc- 1976), although patellogastropod limpets are known from
curred at about latitude 50° north. Thus, with late Ceno- the Mesozoic. The other faunal group is the dugongid
zoic cooling, there was a southward expansion of the sirenians, which are old (early- to mid-Cenozoic) and
temperate zones, possibly providing a setting suitable for primarily tropical in distribution. This group gave rise to
the evolution of sea otters (Estes and Steinberg 1988). The coldwater kelp eaters: Dusisiren dewana by the middle to
other event of possible evolutionary significance to sea upper Miocene (Takahaski et al. 1986) andHydrodamalis
otters was widespread extinction of the odobenid pinni- by the mid-Pliocene in the North Pacific, culminating
peds in the Pliocene (Repenning 1976b). Many species, with the extinct Steller's sea cow (H. gigas), which was
in particular the dusignathine odobenids, were adapted to widely distributed in the North Pacific through the late
shallow-water, benthic foraging (Repenning 1976b). The Pleistocene-Recent (Domning 1978). Sea cows appar-
last of these, Pliopedia and Valenictus, overlapped spa- ently foraged on shallow sublittoral kelps or surface can-
tially and temporally with the earliest records of En- opy, and they also may have significantly influenced kelp
hydritherium. Repenning (1976b) suggested that forest ecosystems before their mid-1700's extinction,
extinction of these odobenids may have opened an which was evidently due to human exploitation.
environment for radiation of the Enhydritherium- Certain biogeographical patterns in marine plant-her-
Enhydra lineage. bivore interactions are consistent with the hypothesis that
The evolutionary consequences of sea otters, their an- kelp radiations occurred in a low-herbivory environment.
cestors, and ecologically similar species are poorly Much of the evidence is based on the idea that chemical
known. However, because modem sea otters are import- defenses (mainly through phenolic compounds) are the
ant predators in coastal communities, they well may have principal means whereby fleshy brown algae
played important roles in shaping the evolution of many (Phaeophyta) defend themselves against herbivory
coastal organisms. Estes and Steinberg (1988) suggested (Geiselman 1980; Geiselman and McConnell 1981;
that one such effect was a reduced intensity of herbivory, Steinberg 1984, 1985; Hay and Fenical 1988). In the
resulting from sea otter predation on herbivorous sea North Pacific, many of the common brown algae are
urchins, and speculate that this may have led to a poorly poorly defended by phenolics (Steinberg 1985, 1988;
defended marine flora in the North Pacific Ocean. Estes and Steinberg 1988). In addition, feeding, growth,
Spatial and temporal patterns in the evolution and radi- and reproductive success of strongylocentrotid echinoids
ation of kelps (Order Laminariales) are consistent with (an important-if not the most important-kelp herbivore
this hypothesis. The extant kelps have a clear geographic in the North Pacific) are strongly inhibited by phenolic
affinity for the North Pacific, as do sea otters and the compounds (Estes and Steinberg 1988). Conversely, in
dusignathine odobenids. Of the 27 presently recognized other temperate seas of the world, the brown algal floras
kelp genera, 26 occur in the North Pacific. Only eight kelp appear to be comparatively depauperate (e.g., South Af-
 THE SEA OTTER: BEHAVIOR. EcoLoGY. AND NATURAL HisTORY 5

rica and South America) or well defended by phenolic oped; otters frequently use their sensitive whiskers and
compounds (e.g., New Zealand and Australia). Steinberg paws to locate and capture prey beneath the surface.
(1989) reported that the diverse brown algal flora of Hearing in the sea otter is virtually unstudied; however,
northern New Zealand and southeastern Australia had in contrast to the pinnipeds and cetaceans, there is no evi-
high phenolic concentrations, and that echinoid herbi- dence of cranial modification for directional sound per-
vores in this area tended to be both less destructive grazers ception underwater (Repenning 1976b). Olfaction also is
and less affected by phenolic compounds than are the virtually unstudied in the sea otter. In contrast to the pinni-
strongylocentrotids in the North Pacific. peds, which have reduced olfactory sensitivity due to a
On the basis of these observations, Estes and Steinberg reduction in nasal turbinates, sea otters have well devel-
( 1988) hypothesized the following evolutionary scenario: oped turbinates, and acute olfactory sensitivity, typical of
Kelp species radiated recently in the North Pacific in an terrestrial carnivores, apparently has been retained. The
environment in which the intensity of herbivory was low social behavior of sea otters also suggests that scent produc-
due to predation on benthic invertebrate herbivores by sea tion and acute olfactory sensitivity are important in this
otters and perhaps the dusignathine odobenids. This re- species. Observations of California sea otters indicates
sulted in weakly coevolved plant-herbivore interac- that males may locate estrous females by following water-
tions-that is, there was little selective pressure for the borne scents across the ocean's surt·ace (M. L. Riedman,
plants to evolve defenses against herbivores, and conse- Monterey Bay Aquarium, Monterey, Calif., unpublished
quently, for the herbivores to accommodate to those de- data; C. Deutsch, University of California, Santa Cruz,
fenses. Sea otters and dusignathine odobenids never oc- Calif., personal communiction; J. E. Vandevere, 93 Via
curred outside the North Pacific, nor is there evidence that Ventura, Monterey, Calif., personal communication). Sea
predators of comparable influence now inhabit these otters entering a group of otters commonly perform a
areas or inhabited them in the past. As a result, popula- ritualized greeting with one or more of the group mem-
tions of herbivorous echinoids may not have been limited bers, probably involving some form of scent recognition.
by predation in these systems over evolutionary time. The sea otter has developed distinctive adaptations for
Thus, a more tightly coupled plant-herbivore interaction feeding on hard-shelled aquatic invertebrates. Shearing
may have coevolved outside the North Pacific. In other function of the cheek teeth. typical of other carnivores
words, plants developed extensive chemical defenses in (including piscivorous aquatic forms), has been lost in
response to abundant herbivores, and herbivores, in turn, favor of a crushing dentition. Furthermore, the muscula-
developed enhanced capacities to tolerate plant defenses. ture, skeletal anatomy, and neurological function of the
strong forelimbs apparently are modified for tactile sen-
sitivity and tool use associated with the detection, han-
Adaptations Associated with a dling, and consumption of prey (Radinsky 1968).
Marine Existence The sea otter is also characterized by adaptations for
pulmonary function and oxygen conservation associated
Marine mammals share several types of adaptations with diving in the marine environment. Sea otters are
associated with living in a marine environment-adap- capable of deep diving; the record depth is about 100 m
tions related to vision, hearing, olfaction, feeding, oxygen (Newby 1975). The large lungs (Fig. 2) maintain surface
conservation, thermoregulation, water balance, locomo- buoyancy and serve to increase oxygen storage capacity
tion, and reproduction. In general, the cetaceans, pinni- (Kooyman 1973 ); the blood has a higher buffering capac-
peds, and sirenians are substantially more specialized ity than that of nondiving mammals (Lenfant eta!. 1970).
than sea otters for an aquatic existence, having evolved In addition, Garshelis (1983) presented data that suggest
millions of years earlier than the otters. Although sea to us that sea otters may use anaerobic metabolism when
otters are the most recently evolved and least specialized unusually deep or long dives are required. Cartilagenous
group of marine mammals, they are the species most airways connect directly with the alveolar sacs, which
highly adapted for aquatic living belonging to the order insure patency until compression collapse. This structure
Carnivora (excluding pinnipeds). Adaptive trends in sea is also found in the pinnipeds and cetaceans but is absent
otters are summarized and discussed in greater detail in in Lutra (Kooyman 1973 ).
subsequent sections. Marine mammals have two modes of insulative heat
The sea otter's eyes appear to be adapted for both aerial conservation-blubber and fur. Blubber, which is used by
and underwater vision. According to Murphy et a!. the more highly specialized pinnipeds and cetaceans, is
\
(1990), sea otters are able to focus clearly both underwa- absent in sea otters. However, the sea otter's dense fur,
ter and in air by means of an excellent accommodative which is probably the most highly adapted and efficient
ability, which compensates for the loss of their corneal of any aquatic mammal, provides insulation against cold
power underwater. Tactile senses appear to be well devel- (1-16° C) ocean water. In addition. the sea otter's rapid
6 BIOLOGICAL REPORT 90 (14)

Fig. 2. Adult female sea otter skeleton. The last joint of each digit was removed and is missing (V. B.
Scheffer).
 THE SEA OTIER: BEHAVIOR. EcoLOGY. AND NATURAL HISTORY 7

metabolism-two to three times higher than a similar- patchy. The tendency for sea otters to rest in groups on
sized land mammal-helps it to generate heat. land or in water may also be related to the environmental
To facilitate water conservation and maintain a suitable constraint of limited suitable or preferred resting sites.
water balance in the marine environment, sea otters pos- Gregariousness may also have evolved as a protective
sess large, heavily lobulated kidneys that concentrate response to predation by species such as humans, white
urine. The ingestion of seawater by otters may also pro- sharks (Carcharodon carcharias), bald eagles (Haliaee-
mote urea elimination (Costa 1982). tus leucocephalus), coyotes (Canis latrans), and brown
The sea otter also has distinctive adaptations for aquatic bears ( Ursus arctos). Social exclusion from breeding
locomotion. The fifth digit of the hindlimbs (Fig. 3) is areas may also promote aggregation of young males.
extended to provide a flipperlike structure (Kenyon
1969). No other aquatic mammal in the order Carnivora
has such highly developed limb structures for aquatic Classification and Taxonomy
movement. The loosely articulated skeleton and loss of
the clavicle help provide the flexibility necessary for
grooming and movement in an aquatic environment. Dor- Classification of Sea Otters
soventral undulations of the entire body are used for rapid
aquatic locomotion (Sokolov and Sokolov 1970; Tarasoff The sea otter (Enhydra lutris) is the second-largest
et al. 1972). In contrast, aquatic motion in Lutra is mustelid, exceeded in size (body length) only by the giant
achieved by movements of the forelimbs and hindlimbs, Amazonian otter (Pteronura brasiliensis). However, it is
with little body motion. The aquatic form and movement the smallest marine mammal in the world, except for the
of sea otters are like those of the pinnipeds and cetaceans South American marine otter (Lutrafelina; also known as
rather than other carnivores. the sea cat or chungungo ). The sea otter represents 1 of
Sea otters share a number of reproductive features with about 12 species of otters that are distributed throughout
other marine mammal species-adaptations for giving the world.
birth and raising young in a marine environment. For The only other otter that lives exclusively in the ocean
example, sea otters nearly always give birth to a single is Lutra felina, which weighs only about 4 kg (Harris
young; twinning occurs but is rare. The absence of mul- 1968). Marine otters inhabit kelp beds off the Pacific
tiple-young pregnancies is typical of pinnipeds and ceta- coast of Peru and Chile, where their declining population
ceans, but atypical of the other lutrine carnivores (Estes is classified as endangered by the International Union for
1979). In addition, the sea otter's 4- to 6-month gestation the Conservation of Nature (IUCN) Red Data Book.
is relatively long compared with most other lutrines. Sea While marine otters usually forage at sea, they may also
otters are capable of delayed implantation, a trait which swim upstream into rivers in search of freshwater
1
also characterizes pinnipeds and other mustelids. Parturi- prawns (Hayes 1985*) . Their diet typically consists of
tion in the sea otter is apparently more often aquatic, molluscs, crustaceans, and fish (Brownell 1978 *; Ostfeld
although it can occur on land. Aquatic parturition is et al. 1989). Fish are carried to shore to be eaten, while
unknown for other carnivore species, and even the pinni- invertebrates may be consumed either on shore or on the
peds give birth on land. Like many marine mammals, the water's surface, with the otter assuming a belly-up posi-
period of maternal care in sea otters is relatively long, and tion, as sea otters do. Tool use has not been observed
milk fat content is high. Such intensive maternal invest- among marine otters. While diving, marine otters are able
ment helps prepare the young for survival in a harsh to remain submerged for an average of 30 sec (Ostfeld et
environment after weaning. al. 1989). Marine otters utilize inaccessible and remote
Socially, sea otters share a tendency with many other burrows for resting and protection. They tend to be soli-
marine mammals to form groups (Fig. 4); in contrast, tary or found in small groups of three to five individuals
grouping is rare or absent in other lutrine carnivores. The (Castilla 1981 ). Ostfeld et al. ( 1989) suggested that they are
significance of grouping in sea otters is unclear. They monogamous. While little is known of reproduction, litter
commonly rest in groups of widely varying size; however, size is usually two cubs, although four to five cubs per
they usually feed, copulate, and give birth away from litter have been reported in the Magellan area (Cabello
other conspecifics. Therefore, grouping does not seem to 1985 *).
facilitate foraging or reproduction. However, Garshelis et
al. (1984) observed that males in Prince William Sound
often forage together, and1 they speculated that social
facilitation of foraging (allowing individuals to locate 1
Asterisks' *J throughout text indicate unpublished material; the refer-
good feeding areas) promotes gregariousness among ences are found in the Unpublished References section following the
males in unfamiliar areas where food resources are References section.
8 BroLocrc.\L REPORT 90 ( 14)

Fig. 3. Left hindtlipper (ventral or plantar surt'aceJ of adult male sea otter. Note elongated outer or fifth digit. an adaptation
which enhances propulsion when the otter swims on its back \K. Kenyon).
 THE SEA OTTER: BEHAVIOR, EcoLOGY. AND NATURAL HISTORY 9

Fig. 4. Group of sea otters ir; California (L. Minden).

Differences in the morphology and life history of sea otters differentiating river otters from sea otters include the sea
and river otters (Lun·a canadensis) are listed in Table I. otter's more elongate body and larger, broadly flattened,
Sea otters are larger in size, roughly two to four times webbed hind feet (Fig. 5). In addition, the sea otter's tail
heavier than river otters. Other obvious characteristics is comparatively flat and of uniform width, whereas the

Table 1. Morphological and life histOI}' differences between the sea otter (Enhydra lutris) and the river otter (Lutra
canadensis). (Kenyon 1969; Nowak and Paradiso 1983; Chaninl985.)
Sea otter River otter Sea otter River otter
(Enhydra lutris) (Lun·a canadensis) (Enhydra lutris) I Lwra canadensis)

1. Larger sized I. Smaller sized IO.Lives exclusively in the 10. Primarily inhabits freshwater.
weight= 20-40 kg weight = 6-10 kg ocean but also enters the ocean
length= 120-140 em length= 102-118 em
11. Usually swims belly up II. Usually swims belly down on
2. More elongated body 2. Shorter body on surface, paddling with surface, with much of the
hindflippers; floats high in back submerged
3. Hindfeet modified to 3. Hindfeet webbed, but smaller water
flippers and webbed to and not flipperlike;
tips of toes; fifth or outer fifth digit not elongated 12. Comes ashore less often 12. Frequently on land, where
digit elongated in most areas: moves movement is agile and swift
awkwardly on land
4. Tail more flattened, of 4. Tail rounder in diameter,
uniform width, and shorter thicker at base and tapers to a 13. Usually rests in kelp 13. Usually rests on shore in dens
(< 1/3 of body length) point, and longer ( > 1/2 of beds or open water
body length)
14. Diet limited to marine 14. More diverse diet, including
5. Foreclaws short and 5. Foreclaws long and not macroinvertebrates and fish. frogs, crayfish. snails.
partially retractile retractile fish rodents, and birds
6. Fur longer and softer; 6. Fur shorter and coarser; under- 15. Food eaten in water 15. Food consumed on shore
underfur denser; guard fur not as dense; guard hair while floating on back
hair sparse covers fur completely
16. Produces single young at 16. Produces Iitter of up to
7. Longer baculum (6 inches) 7. Shorter baculum (4 inches) one time four young
8. Molars broad and flattened 8. Molars not flattened; 17. Young more precocial; 17. Young less precocial; eyes
for crushing hard-shelled carnassial cheek teeth eyes open at birth do not open until -I month
invertebrates; canines adapted for shearing flesh after birth
rounded and blunt
18. Social; usually found in 18. Usually found alone or in
9. Two mammae 9. Four mammae small to extremely large family groups
groups

7 £1. IAMW MUM£ @)£.#.

10 BIOLOGICAL REPORT 90 ( 14)

Fig. 5. A) Adult male river otter (Lun·a canadensis); weight=

10.5 kg; length= 122 em (V. B. Scheffer). B) Adult female
sea otter; weight = 18.1 kg; length = 127 em. White dots
indicate mammae and umbilicus (K. Kenyon).

tail of theo river otter is considerably longer, thicker at the (Wilson et aL 1990). ranging from the Aleutian Islands to
base, and tapers to a point (Fig. 6). Oregon; and E. I. nereis (Merriam 1904: 159), ranging
from northern California to approximately Punta
Abreojos, Baja California (Fig. 7). The taxon E. !. nereis
Subspecies ofSea Otters (southern sea otterl is controversial. and its validity, as
well as its northern range limit. was only recently re-
The genus En hydra (Fleming 1822: 187) has only one solved (Table 2).
species, E. lutris. Three subspecies are recognized: £. Several authors concluded that the northern range limit
lutris lutris (Linnaeus 1758:-1-5), occupying the Kuril Is- of£.!. nereis was the Strait of Juan de Fuca (e.g., Taylor
lands, the east coast of the Kamchatka Peninsula, and the and Shaw 1929: Barabash-Nikiforov 1947; Kenyon
Commander Islands: £. !un·is [unnamed subspecies] 1981), although recently it was suggested that if£. !.
 THE SEA OTTER: BEHAVIOR, ECOLOGY. AND NATURAL HISTORY 11

Fig. 6. River otters (Lum; anadensis) on San Juan Island. Washington (T. Ransom).

I
·I··
...

Aleutian Islands
CANADA
Sanak
Islands
1
Rat Delarof
Islands

Islands Islands

PACIFIC OCEAN

II IIIII Original Distribution (1740)

mlti Present Distribution (1984)

Remnant Colonies (1911)---..-

Surviving Translocated Populations * 11

.o c Hawaiian Islands
.I>

Fig. 7. North Pacific Ocean showing original and current distribution of sea otters and indicating remnant populations existing in
1911.
12 BIOLOGICAL REPORT 90 (14)

Table 2. Taxonomic classification of sea otters. Areas graphically distinct sea otter groups, including skulls
inhabited by subspecies in brackets. from areas between southwestern Alaska and California.
Class Mammalia Results supported his earlier interpretation that differ-
Order Carnivora ences in skull morphology represented a cline, and that
Family Mustelidae all sea otters from the Commander Islands to California
Tribe Aonychini should be included within the subspecies E. !. lutn·s.
Enhydra lutris (Fleming 1822: 187) Davis and Lidicker ( 1975) disagreed with Roest's con-
Enhydra lutris lun·is (Linnaeus 1758: 45) clusions and presented an alternative interpretation of his
[Kuril Islands/Kamchatka/ data. They proposed that a high degree of separability
Commander Islands] exists between the northern and southern populations,
Enhydra /un·is (unnamed subspecies;
and that otters from southwestern Alaska (the Alaska
Wilson eta!. 1990)
Peninsula, southern Alaska, and Prince William Sound)
[Oregon-Aleutian Islands]
Enhydra lutris nereis (Merriam 1904: 159) represent an area of intergradation between the two sub-
[California] species. Davis and Lidicker pointed out that, if the varia-
tion is regarded as clinal, there would be a pronounced
shift in the slope steepness of the indicated cline between
Prince William Sound and the Alaska Peninsula. They
concluded that E. l. nereis should continue to be recog-
nized as a valid subspecies, based on existing morpholog-
ical and behavioral differences between the populations
and the degree of geographic and genetic isolation char-
acterizing the sea otter population in California. Rice
nereis is a valid subspecies, it probably ranged northward (1977), Hall (1981), and Nowak and Paradiso (1983)
to Prince William Sound (e.g., Roest 1971 *; Davis and subsequently recognized E. l. nereis as a distinct subspe-
Lidicker 1975; Rice 1977). However, Wilson eta!. ( 1990) cies in their respective listings of marine mammals and
concluded that the northern limit of E. !. nereis was other mammalian species.
northern California or Oregon. Most recently, Wilson et a!. (1990) conducted univari-
In 1904, Merriam (1904: 159) recognized E.!. nereis on ate and multivariate analyses on 20 skull characters of304
the basis of a single skull from San Miguel Island, Cali- sea otters from throughout the species' geographic range
fornia, which he compared with several skulls from the (including 236 specimens from the Soviet Union) from
Bering Sea. Grinnell et a!. (1937) confirmed the validity which they concluded that three subspecies should be
of E. !. nereis after comparing the type specimen with recognized. The geographical distributions of these sub-
a single skull from Alaska. Scheffer and Wilke (1950), species are somewhat different from those previously
however, examined 56 skulls (8 from California, Oregon, recognized, resulting in several nomenclatural changes.
and Washington; 48 from Alaska) and found no signif- Wilson eta!. 's ( 1990) analysis indicates that the range of
icant differences in skull features. They concluded that the far western Pacific subspecies-previously desig-
E. l. nereis was not a valid subspecies and should there- nated E.!. gracilis (Bechstein 1800:408) and distributed
fore be synonymized with E. l. lutris. Kenyon (1969) from Kamchatka southwestward through the Kuril Is-
considered sea otters in California and Alaska to be the lands to the northern Japanese archipelago-should be
same subspecies, whereas Miller and Kellog (1955) and expanded to include the Commander Islands. Since the
Hall ( 1981) regarded the California population as a dis- type locality for E. lutris is Kamchatka, £. l. gracilis
tinct subspecies (E. !. nereis). becomes a junior synonym of the nominate form, E. l.
Roest (1971 *) examined 50 skulls from California and lutris. A second subspecies, previously designated E. /.
214 from Alaska and compiled total length and weight lutris (considered to range from the Commander Islands
measurements reflecting size differences between the two to about Prince William Sound) was named E. lutris
populations. He concluded that E.!. nereis was recogniz- (unnamed subspecies). Wilson et a!. 's ( 1990) analysis
ably different from E. !. lutris and constituted a valid indicates that E.lutris (unnamed subspecies) ranged from
subspecies. However, his subsequent, more detailed, the Near Islands (western Aleutian archipelago) eastward
analysis of more than 250 skulls from California and across the Pacific rim to Oregon. The third subspecies,
Alaska (Amchitka and Adak islands and southwestern which retains the name E./. nereis. ranged from northern
Alaska) led Roest (1973, 1976) to conclude that E. !. California to the central Pacific coast of Baja California,
nereis was not a distinct subspecies but rather a variation Mexico. Except for occasional extralimital wanderers,
of a northwest-southeast cline. the present range of E. /. nereis is restricted to central
Roest ( 1979 *) performed another analysis in which he California and San Nicolas Island in the southern Califor-
compared skulls representing nine (rather than four) geo- nia Bight.
 THESE.-\ OTTER: BEHA vroR. EcoLOGY ..·\' L"' :\ \ TLI<.·\L HrsToRY 13

Morphology and Physiology Woodhouse et al. ( 1977'1 reported similar average

weights of 29.5 kg for adult mab and 19.5 kg for adult
females. The large-,r male found dead in California
Bod)' Measurements weighed 41.7 kg and was 134 em long (Ames. personal
communication 1. At birth. pups\\ eigh 1.4-2.3 kg (Miller
Sea otters are moderately sexually dimorphic. Adult 1974: Fig. 9). Monnett and Ratterman ( 1988b. J found
males are 349c heavier and 89c longer than adult female,. that, in eastern Prince William Sound. male sea otter pups
and the male ·s head and neck are heavier and more grew at a higher rate (95 g/dayJ than did females
muscular than those of the female (Kenyon 1969: Estes (83 g/day). Based on these pattems. they concluded that
19EO 1. However. it is not possible to determine sex in the more parental resources were required to raise males than
field solely on the basis of size (Fig. 8). The presence of females from conception to weaning: more information
penial and testicular bulges-most visible when the fur is is needed before this conclusion can be verified.
wet-is the only reliable way of identifying an animal's According to Roest ( 1971 ''. I913. 1979\ Alaskan sea
sex . .\1easurements taken on dead California sea otters otters are generally somewhat larger than California sea
indicated that standard lengths of adult males and adult otters. However. size of Alaskan otters varies with geo-
females average 129.1 em (N =58) and 119.8 em (1\" = graphic location. and some Alaskan otters weigh less than
49: J. A. Ames. California Department of Fish and Game. California otters. Kenyon ( 19691 found that adult sea
Monterey, Calif.. unpublished datal: predicted average otters from heavily populated areas (e.g .. Amchitka Is-
weights for healthy sea otters of those sizes are 29.0 kg land) may weigh less than adults from sparse populations.
for males and 19.8 kg for females (Ames et a!. 1983 l. The mean weights and lengths of dead Amchitka adults

Fig. 8. :\dult male sea otter. note penile bulge as field idemiiication for determining sex rK. Kenyon.!
14 BIOLOGIC\L REPORT 90 ( 14)

:-

,_-

~~
·~ .::-
~,
~ "-:i
;>---r ~~

:t ...

.. -
9.

Fig. 9. Dorsal (A) and ventral (B l view of newborn female sea

otter pup at Amchitka Island. Alaska: weight= 1.95 kg;
length= 56 em. Note lighter. yellowish natal pelage on
head and neck (K. Kenyon).

were 28.3 kg and 135.0 em for males (N = 79) and Lifespan and Age Determination
21.1 kg and 125.2 em for females (N = 254). Sizes of
adults killed in sparsely populated areas (Shumagin
Islands. Unimak Island. and Adak Island) were 39.5 kg Alaskan females live an estimated 15-20 years, while
and 140.8 em for males (N = 5) and 25.2 kg and 129.8 em male lifespan appears to be about 10-15 years (Calkins and
for females (N = 4 ). The largest adult male killed in the Schneider 1984\ R. J. Jameson (U.S. Fish and Wildlife
Aleutians weighed 45 kg and was 148 em long, while the Service. San Simeon. Calif.. personal communication) esti-
largest female weighed 32.6 kg and was 140 em long. mates a minimum lifespan of 11-12 years for some Califor-
Newborn pups in Alaska measure about 61 em and weigh nia males. In the northern part of the range in California,
1.9 to 2.3 kg (Kenyon 1969). one tagged female \\as known to have lived for 15-16 years,
 THE SEA OTTER: BEHAVIOR. EcoLOGY. AND NATURAL HISTORY 15

and other known-age females 10-11 years old are currently "The claws are closely associated with. and move only with,
under observation. An adult male was at least 13 years old the terminal phalanx .... " This makes them in one sense
(probably 2 or more years older) when he disappeared nonretractable, but they can be extruded to a degree by
(M. L. Riedman, J. A. Estes, M. L. Staedler, Monterey Bay flexing the terminal digits. In some necropsied California
Aquarium, Monterey, Calif., unpublished data). Garshelis otters the claws are extensively worn and are mere nub-
( 1984) found that older otters tended to have lighter-colored b;ns. The hindfeet are flattened and flipperlike (Murie
fur on their necks and related age to pelage color patterns to 1959; Fig. 3). Each of the five hind digits is progressively
provide estimates of age categories in field observations longer. the outer digit being the longest-an adaptation
of living sea otters. Counts of the incremental lines in that enables the otter to more efficiently swim on its back
tooth cementum have been used to estimate ages of living at the surface (Kenyon 1969; Tarasoff 1972, 1974; Ta-
and salvaged sea otters in Alaska (Schneider 1972c *; rasoff et a!. 1972; Howard 1975). Surface swimming is
Garshelis 1984) and California (Pietz eta!. 1988\ Tooth accomplished by vertical, undulating motions of the tail
cementum counts typically have been made from the first and hindflippers (Howell 1930; Taras off eta!. 1972). The
premolar. In a sample of 580 salvaged carcasses in Califor- tail is horizontally flattened to enhance propulsion. A sea
nia, Pietz et a!. ( 1988 *) estimated maximum age, based otter floating on its back may move the tail in a sculling
on tooth cementum, to be 16 years for females and 15 years action to shift or maintain position (Kenyon 1969, 1981 ).
for males. Unfortunately, there are no teeth available from
older known-age sea otters to confirm the relation be-
tween cementum lines and age; such material will be- Swimming Speeds
come available, however, as sea otters recently marked
as juveniles eventually grow old and die. In captivity, a Observations in Alaska indicate that sea otters typically
male sea otter ("John," a yearling captured from Am- swim at a speed of 1-2.5 km/h on the surface, although
chitka in 1968) survived to about 20 years at the Vancou- speeds of 9 km/h may be attained for short distances
ver Public Aquarium (M. Butschler, Vancouver Public underwater (Kenyon 1969). Garshelis ( 1983) reported
Aquarium, Vancouver, British Columbia, personal com- that a male Alaskan sea otter traveled 11 km at an average
munication) and the Point Defiance Aquarium (T. Otten, rate of 5.5 km/h. In California, Jameson (personal com-
Point Defiance Aquarium, Tacoma, Washington, personal munication) calculated average speeds ranging from
communication). He sired a pup born at the Vancouver 0.6 km/h (distance of 52 km) to 3.3 km/h (distance of
Aquarium in April 1986 and died on 1 October 1987. 75 km) for two adult males that moved from male groups
to female areas. Observations made on captive female
California sea otters indicate that underwater swimming
Dentition velocities average 3.6 km/h (Williams 1984). Movement
on land is comparatively slow and awkward (Barabash-
Sea otters have bunodont molars, unlike the typically Nikiforov 1947; Tarasoff eta!. 1972), partly due to the
carnassial cheek teeth of most mammalian carnivores. elongated fifth hindflipper digits, which impede move-
The sea otter's dentition is adapted for crushing hard- ment. A sea otter walking on land raises one foot at a time
shelled macroinvertebrates: molars are broad and flat- and arches its back, moving with a rolling gait or swinging
tened, canines are rounded and blunt. The adult dental from side to side. When startled, an otter moves quickly
formula is i 3/2, c 1/1, pc 3/3, m 1/2, total 32 teeth by bounding or hopping with forelegs and hind feet
(i = incisor, c =canine, pc = postcanine, m = molar; Ken- together or by sliding across the ground on its belly while
yon 1969; Fig. 10). Extremely worn teeth indicate old age pulling with the forelimbs (Kenyon 1969).
in sea otters, and serious tooth wear may possibly contrib-
ute to mortality in older animals.
Sensory Organs

Forelimbs and Hindlimbs Little information is available about the sensory organs.
Chemoreceptive and tactile senses seem well developed.
The forelegs of the sea otter are used primarily for groom- Although olfaction in the sea otter is poorly known, the
ing and foraging, rather than for propulsion. The extremely existence of extensive nasal turbinates-as well as obser-
powerful forelegs and sensitive paws help it to locate, cap- vations of social interactions among individuals-sug-
ture, and break open hard-shelled prey (Fig. 11). A loose gests that olfaction is acute. On numerous occasions, sea
pouch of skin at the axilla of hch forelimb is used to otters have been observed actively sniffing the air, the
temporarily store and transport food (Kenyon 1969). Un- water's surface, or other otters. Adult males may possibly
like the hindclaws, the foreclaws can be extended (Ken- locate and identify estrous females by means of olfactory
yon 1969; Howard 1973). According to Howard (1973), cues (Deutsch, unpublished data; Riedman, unpublished
 16 BroLOGIC\LREPCJRT90(i-1-l

Fig. 10. Dentition and 'kull of older

juYenile or young subadult sea otter
found dead on Arnchitka Island (5
'v1arch 1962): Weight = I 0.9 kg:
length= 100.5 ern. Note broad. flat-
tened molars and blunt. rounded ca-
nine> 1 K. Kenyon).

~- . - ... ~---
I
I

l
!8 BIOUlCIC\LREPORT SJO ( !4)

Fig. ll. (A) Sea otter forepa\\: note absence of fur on inner ventral surface. !B l Dorsal view of sea otter forepaw
(K. Kenyon).
 THE SEA OTTER: BEHAVIOR. EcoLOGY. AND NATURAL HisTORY 19

Fig. 12. External ear of the sea

otter (K. Kenyon).

data). The paws and vibrissae are used to locate and habituated to the noise (within 2 h) and did not subse-
capture prey underwater (Radinsky 1968; Kenyon 1969; quently avoid the sound source.
Shimek 1977a,1977b; Hines and Loughlin 1980). Unlike Visual acuity in the sea otter seems to be good both
other mustelids, however, the sea otter lacks functional above and underwater. Murphy et a!. ( 1990) found that.
anal scent glands (Kenyon 1969). both above and below water, sea otters are approximately
Although their sense of hearing is not well known, emmetropic; that is, they are able to focus clearly on
Kenyon ( 1969) wrote that hearing seems to be "moder- targets both underwater and in air (although they
ately well developed." The ear pinna is moderately curled occasionally exhibit myopic reflexes in both environ-
and resembles that of otariid seals (Fig. 12). An otter's ear ments). Sea otters depend on accommodation of the eye-
is held erect above the surface but folds sharply down- ball to compensate for the loss of the eye's corneal refrac-
ward during dives (Pocock 1928; Kenyon 1969). Davis et tive power when underwater.
a!. ( 1988) examined the anatomy of the sea otter cochlea Sea otters have an exceptional accommodative range of
(inner ear) and Organ of Corti (which contains hair cells about 60 diopters (a unit of curvature and of the power of
within the cochlea) and found them to be indistinguish- lenses)-at least three times greater than that reported
able from that of other placental mammals. In addition, for any other terrestrial mammal (Sivak 1980). In
they concluded that sea otter hearing is most sensitive to comparison, diving marine birds, such as cormorants
high frequencies, which is also true of North American (Phalacrocorax spp.), have an accommodative ability of
river otters (Lutra canadensis). <40 diopters (Levy and Sivak 1980). Murphy eta!. ( 1990)
Results of a study conducted near Soberanes Point, found that the sea otter eye is characterized by extensively
California, indicated that sea otters were seemingly un- developed iris musculature, meridional ciliary muscle,
disturbed by experimentally projected waterborne indus- and comeoscleral venous plexus surrounding the entire
trial and seismic noise or by recordings of killer whale ciliary body region; all these may be associated with a
(Orcinus orca) vocalizations (Riedman 1984a* , 1984b * ). unique and well-developed lenticular accommodative mech-
Davis et al. (1988b *) tested the response of California and anism that is able to change the refractive power of the
Alaska sea otters to a variety of acoustic stimuli and found lens. In addition, they speculate that the well developed
that while California sea otters exhibited little reaction to anterior epithelium of the cornea may be an adaptation
killer whale vocalizations. Alaska sea otters showed a that helps the otter cope with salinity in its environment.
stronger response, possibly because killer whales are In comparison, Schusterman and Barrett (1973) found
more common in Alaska and may prey on sea otters there. that the visual acuity of the Asian small-clawed otter
Other acoustic noise. such as random playback of syn- (A onyx cinerea) was the same in air and water when tested
thetic sounds (air hom and warble tone), initially startled during daylight. In relation to pinnipeds, Gentry and
the otters. but like other marine mammals. they soon Peterson ( 1967) suggested that sea otters have slightly
 20 BIOLOGICAL REPORT 90 (14)

poorer underwater VISIOn than California sea lions Williams eta!. (in press) found that sea otter fur density
(Zalophus californianus) or harbor seals (Phoca vitulina) varied between bodv regions, with hair amounts rang-
and speculated that an otter's vision may be better in air than ing from 26,413/c~ 2 (!70,364/in. 2) on the foot ;o
2
underwater. Although recent studies have shown that sea 164,662/cm (I ,062,070/in. 2) on the foreleg. Previous
otters can see clearly in both environments, the orbits of sea estimates of average underfur hair densitv have been
7 2 -
otters are not enlarged, as they are in most pinniped species. reported at 100.800/cm- (650,160/in. : Kenyon 1969)
2 2
Orbital enlargement is thought to be an adaptation for and 131,000/cm (844,950/in. : Tarasoff 1974). In
increasing visual sensitivity in deep, dimly lit water. comparison, domestic cats (Felis si!vestris) have 16,000-
7
Sea otters appear to have a well-developed tapetum, as 32,000 hairs/em-, dogs (Canis fami!iaris) have 200-
2
do the pinnipeds and most nocturnal carnivores that need 9,000 hairs/cm , and humans average only about 100,000
to see well at night or in dimly lit waters. The specialized hairs on the entire head. The northern fur seal
layer behind the retina, the tapetum Iucidum (containing (Ca!lorhinus ursinus) has an estimated 40,000-60,000
2
many guanine crystals), enables the retina to reflect light. hairs/cm (Scheffer 1962). The sea otter has specialized
It gives a metallic appearance. By sending light passing glands that secrete oil and enhance the water-repellent
once through the retina back through the retina a second quality of the fur. In addition, the sea otter's lack of
time, the tapetum enhances the light-gathering capacity arrector pili muscles in the epidermis allows the hairs to lie
of the eye. close to the animal's skin when immersed (Kenyon 1969).
Molting takes place gradually throughout the year
(Ognev 1931; Kenyon 1969), although a peak period of
Internal Organs molting seems to take place in spring among captive
Alaska otters (Kenyon 1969). The number of fur fibers in
The lungs are large in relation to body size, nearly 2.5 each bundle may increase as an otter ages, indicating that
times that found in other mammals of similar size. Large some of the fibers are not shed later in the molt, but
lungs serve to regulate buoyancy and store oxygen (Lenf- instead remain attached within the bundle. Throughout
ant et a!. 1970; Kooyman 1973; Leith 1976: Costa and the year, individual fibers are probably in molt while
Kooyman 1982). The liver and kidneys are also large others are at rest (Kenyon 1969).
relative to body size. An enlarged liver probably helps An air layer is trapped within the fur fibers. providing
maintain the high metabolic rate (Kenyon 1969; insulation and buoyancy and enabling the skin to remain
Morejohn et al. 1975), while the large, lobulated kidneys dry when immersed (Kenyon 1969; Morrison et a!. 197 4;
allow the otter to produce large volumes of moderately Tarasoff 1974; Costa and Kooyman 1982). When contam-
concentrated urine (Kenyon I 969; Costa 1982 ). Costa inated with pollutants (such as oil), the fur loses its
( 1976 *, 1978b) demonstrated that sea otters drink sea insulative properties, and the otter subsequently dies of
water. Because California sea otters consume primarily hypothermia or pneumonia (Stulken and Kirkpatrick
invertebrates (which possess higher electrolyte concen- 1955; Kenyon 1969; Kooyman et a!. 1977*; Williams
trations than teleost fish), they must process large 1978; Kooyman and Costa 1979 *; Costa and Kooyman
amounts of electrolytes, nitrogen, and water; ingestion of 1979 *, 1980 * , 1982; Siniff et a!. 1982).
seawater may therefore promote urea elimination by in- Frequent grooming of the fur is essential to maintaining
creasing the urinary osmotic space without increasing the its insulative properties. In addition to trapping air within
electrolyte concentration in the urine (Costa 1982). Inter- the pelage, grooming essentially serves four purposes: ( 1)
estingly, captive sea otters at the Monterey Bay Aquarium to clean the fur, (2) to straighten and align the hair shafts
sometimes drink fresh water from a hose and from water so that the loft is maintained, (3) to stimulate the produc-
sprinklers cleaning the exhibit windows; in addition, the tion of natural oil and distribute the oil over the skin and
juvenile male and females in the exhibit ingest their own hair, and (4) to enhance blood circulation (Williams eta!.
urine at times (1. Hymer and B. Grey, Monterey Bay 1990). Vigorous grooming bouts generally occur before
Aquarium, Monterey, Calif., personal communication). and after feeding episodes and rest periods. Intermittent
grooming takes place at other times (often during and at
the end of rest periods), but this type of grooming is brief
Pelage and Grooming Behavior and languid (Kenyon 1969; Loughlin 1977).
Loughlin (1977) found that the intensive grooming
Unlike most other marine mammals, sea otters have bouts of longest duration (which generally occurred after
little subcutaneous fat, depending instead on their dense, feeding) involved a highly stereotyped sequence of four
water-resistant fur to provide insulation against cold. stages. Stage I is characterized by energetic somersault-
Underneath the outer flattened and protective guard hairs ing and lateral rolling, with vigorous rubbing of the entire
is an extremely fine and dense underfur. In fact. the sea body, especially the back, base of tail, and nape. Air is
otter's fur is more dense than that of any other mammal. blown or rubbed into the fur of the abdomen and chest. In

,,
~
'!;t , .. ~LS: LfC
 THE SEA OTTER: BEHAVIOR. EcoLoGY ...>.No \.o.TURAL HISTORY 21

Fig. 13. California sea otter in ·'stage -1." grooming. slowly rubbing face with forepaws (D. Buchich).

stage 2. vigorous grooming continues. but no rolling or as the hairs lose pigment. this is not always the case:
somersaulting occurs. as though the otter is trying to keep dark-headed older otters. as well as light-headed young.
its Yentral surface dry. The chest. face. and nape are are observed. Newborn pups are characterized by a light
rubbed with the paws. while the hindt1ippers are rubbed brown or yellowish. woolly. natal pelage (Fisher 1940),
together rapidly. An otter might roll laterally and entwine which is completely replaced by the adult pelage by 13
itself in kelp. Stage 3 is characterized by slow licking and weeks (Payne and Jameson 1984: Fig. 15).
rubbing of the tail and hindflippers. In stage 4. the animal
is nearly fully groomed. but slowly continues to lick its
paws and chest, rub its face and nape. and rub the Metabolism and Energetics
hindt1ippers together. The limbs are held high above the
water while the otter wraps itself in kelp (Fig. 13 ). Because of their small body size and lack of blubber,
Pelage color in adults varies in shades of brown. The which in other marine mammals provides insulation as
fur of some individuals may become progressively griz- well as a reserve of energy, sea otters compensate for the
zled and lighter in color on the head. neck. chest. and problem of thermal stress not only by means of their
forelimbs due to loss of pigmentation in the guard hairs insulative fur but also by maintaining a high level of
(Barabash-Nikiforov 1947: Jones 1951: Kenyon 1969: internal heat production (Iverson and Krog 1973: Morri-
Miller 1974: Estes 1980: Fig. 14). Garshelis (1984) sug- son eta!. 1974: Costa and Kooyman 1982). A sea otter's
gested that "light-headedness·· develops with age in both rate of heat production is 2.4-3.2 times that expected for
sexes but is most pronounced in old males whose heads a terrestrial mammal of similar size (Costa 1978a: Costa
may appear to be nearly white. He found that in Prince and Kooyman 1982. 1984 ). Sea otters are characterized
William Sound. males appeared to become "white- by an elevated standard metabolic rate (SMR) of about
3
headed" at 6 years. which is younger than the age most 2.5 met. or 0.67-0.7:?. cm per gram of body weight per
females became white-headed (8-9 years). While it may hour. which enables the maintenance of an average body
generally be true that the fur gradually lightens with age temperature of 38.1 ± 0.34° C under typical environmental
 22 BIOLOGICAL REPORT 90 (14)

Fig. 14. California sea otter with heavily grizzled head and chest (J. Mattison).

conditions (Morrison et al. 197 4 ). the outer limit of the kelp canopy, which generally corre-
Energetic requirements are high and critical for main- sponds to the 18-m depth contour. Occasionally. Califor-
tenance of the elevated SMR. Captive adults require nia sea otters are seen further offshore to the 36-m depth
189-253 kcal/kg body weight per day, equivalent to 20- curve (Odemar and Wilson l969a; Wild and Ames 1974;
25% of their total body weight (Kenyon 1969; Costa Loughlin 1977; Ribic 1982a; Ralls eta!. 1988a* . l988b * ;
1976 *). A 20-kg adult otter would therefore need between D. Croll, Moss Landing Marine Laboratories. Moss Land-
4,295 and 5,750 kcal/24 h. Costa (l978a. 1982, 1985 *) ing, Calif., personal communication), but they are rarely
estimated that free-ranging adults daily consume an found many miles out to sea. In some areas. especially
amount of food equivalent to 23-33% of their body portions of Alaska, water shallow enough for sea otter
weight. The sea otter's assimilation efficiency of 80-85% foraging may extend many miles offshore. and in such
is low compared to other mammals (Fausett 1976; Costa areas large numbers of otters may be distributed accord-
1982) and may result from the rapid rate of food passage ingly. Foraging activity in California is generally re-
(typically about 3 h) through the gastrointestinal tract stricted to water depths 25 m or less (Wild and Ames
(Stulken and Kirkpatrick 1955; Costa 1982). 1974; California Department of Fish and Game 1976*;
Estes 1980; U.S. Fish and Wildlife Service 1980*), al-
though California otters have been reported foraging in
Ecology waters up to 36m deep (R. A. Hardy. California Depart-
ment of Fish and Game, Morro Bay, Calif.. unpublished
data). The record dive depth occurred in the Aleutian
Habitat Characteristics Islands, where a sea otter drowned in a king crab
(Lithodes and Paralithodes) pot that was set in about
Sea otters inhabit shallow coastal waters and seldom lOOm of water (Newby 1975). In the deep tJords of north-
range more than l-2 km from shore. In areas with rocky eastern Prince William Sound, Garshelis (! 983) reported
substrates. they usually occur between the shoreline and that sea otters typically dive to depths of 28 rn when

~t,o ~

~~~~jc·· ~.,....-~...,._..,,.~--
 THE SE.t.. OTTER: BEHAVIOR. EcoLOGY. A '-D NATURAL HisTORY 23

Fig. 15. Small California sea otter pup showing natal pelage. which is replaced by adult fur by 3 monrhs of age (S. Webster).

feeding on Dungeness crab (Cancer magister). surface kelp canopy in rocky-bonom habitats is formed
Sea otters occur in areas with widely ranging exposure. entirely by the annual species Alariaflstulosa. Although
substrate types. and community composition. In Cali- sea otters in such areas typically associate with this sur-
fornia. they are usually found in rocky-bottom areas. face canopy in summer. the canopy is absent dunng much
although they also occur in soft-bottom habitats. Rocky- of the rest of the year. In California. sea otters may also
bottom habitats typically support diverse and productive inhabit areas devoid of canopy-forming kelps and rest in
communities. including prey frequently consumed by sea open water. However. the kelp canopy. used for foraging
otters (e.g., sea urchin. abalone. crab). Sea otter density and resting. is an important habitat component. and the
in California is probably related to substrate type. On density. areal extent. and species composition of kelp
average. rocky-bottom habitats in California support sea canopies are known to influence the distribution patterns
otter densities around 5 individuals/km, whereas sandy- as well as territorial and home range boundaries (Benech
bottom areas support average densities of 0.8 individu- 1981 ':Jameson 1989: G. R. VanBlaricom and R. J. Jame-
als/km (California Department ofFish and Game 1976\ son. U.S. Fish and Wildlife Sen ice. University of Cali-
The type and structure of rocky bottom also seems to fornia. Santa Cruz. Calif.. unpublished data). California
affect sea otter density. Areas with extensively fractured sea otters preferentially associate with giant kelp
or topographically heterogeneous substrates seem capa- (Macrocystis pwifera) as opposed to bull kelp (Nereo-
ble of supporting higher densities of sea otters than areas cysris !eutkeana). Specific kelp beds are used as habitual
with tlat and unbroken substrates. rafting sites for groups of otters as well as for individuals
Sea otters seem to prefer ~eas with surface kelp cano- (Loughlin 1977: Jameson 1989: Vandevere. personal
pies. although this is not an essential habitat requirement. communication: Riedman unpublished data). Territorial
Large numbers of sea otters are found in areas of Prince males may rest in the same kelp beds. at nearly the same
William Sound and southwestern Bristol Bay. where the specific location. for many years (Jameson 1989:
bottom is composed exclusively of soft sediments. In Deutsch. personal communication: VI. L. Riedman. J. A.
other areas. such as the western Aleutian Islands. the Estes. and M. Staedler. unpubli,hed data).

. $. )0¥$'-""'P
24 BIOLOGICAL REPORT 90 (14)

Fig. 16. Adult male sea otter hauled out on beach in Monterey, California (D. Buchich).

one occasion (Faurot et al. 1985), and 14 adults and 4 pups

were seen hauled out near Bird Rock at Point Lobos State
Reserve in May 1986 (Riedman and Vandevere, unpub-
lished data). In the northern part of the range, certain
Haul-out Behavior individuals haul out more frequently than other otters in
the same area (Riedman et al. 1988 * ; K. Lyons and
Sea otters in California have been observed hauled out E. Faurot, personal communication). In addition, females
on the shore at numerous sites throughout their range often tend to haul out during their estrus period (Riedman
(Vandevere 1971 * , 1973b *; Vandevere and Baldridge etal.1988\
1973 * ; Miller 1974; Faurot eta!. 1985; Riedman eta!. Although the frequency of haul-out behavior in Califor-
1988; Jameson, personal communication). Preferred nia is unknown, California otters do not come ashore as
haul-out sites are characterized by low-relief, algal- often or in groups as large as do sea otters in parts of
covered rocks that are exposed at low tide (Faurot 1985), Alaska (Kenyon 1969; Estes. personal observation; Fig.
although sand or cobble beaches are occasionally used as 17). For instance. up to several hundred otters were ob-
haul-out sites (Fig. 16). Sea otters and harbor seals (Phoca served hauled out in groups at Amchitka Island, particu-
vitulina) often haul out close to one another. While harbor larly in male areas, during winter (Estes, personal obser-
seals and otters usually ignore one another, a seal may vation). In one instance, a group of males had hauled out
occasionally behave aggressively towards an otter that inland several hundred meters from shore. This behavior
attempts to haul out too close to the seal (Riedman, is rarely seen elsewhere and probably relates to the ab-
unpublished data). The number of otters hauled out at a sence of terrestrial predators and human disturbance. Sea
particular site usually ranges from 1 to 6 (sometimes otters in the Aleutian Islands tend to haul out less often
including mother-pup pairs); however, up to 18 adults after they have been disturbed by people (Estes, personal
and 4 pups were observed hauled out at Cypress Point on observation).
 THE SEA OTTER: BEHAVIOR. ECOLOGY. A'\D NATURAL HISTORY 25

Fig. 17. Group of 39 male sea otters resting on shore at St. Makarius Point East, Amchitka Island, Alaska (K. Kenyon).

Role in Marine Communities populations of many species of benthic invertebrates. One

is that sea otters are abundant (especially in Alaska and
Pronounced and complex relations between sea otters. the Soviet Union) and, on an individual basis, have a high
a "keystone" (sensu Paine and Vadas 1969) or "founda- rate of food consumption. For example. an estimated
tion" (sensu Dayton 1972) species, and the nearshore 5,000-8.000 sea otters inhabit the roughly 150 km of
community have been documented in Alaska (Estes and shoreline surrounding Amchitka Island in the western
Palmisano 1974; Dayton 1975; Palmisano and Estes Aleutian archipelago (Estes 1977. 1990), and each daily
1977; Estes et al. 1978: Simenstad et al. 1978; Duggins consumes an estimated 25-30% of its 23-kg average body
1980: VanBlaricom and Estes 1988: Duggins et al. 1989; weight. In addition. their extreme mobility, highly devel-
Kvitek and Oliver, University of Washington. Seattle. oped forelimb sensory and motor functions (Radinsky
Wash., in preparation), British Columbia (Farrand Bun- 1968), crushing dentition, and proficient use of tools for
nell 1980; Breen et al. 1982), Washington State (Jameson breaking open the exoskeletons of invertebrate prey
et al. 1986; K vitek et al. 1989), and California (McLean render sea otters easily capable oflocating, capturing, and
1962; North 1965 *, 1974 * ; Ebert 1968a, 1968b; Lowry consuming invertebrates of nearly any size and shape.
and Pearse 1973; Wild and Ames 1974; Haaker and Indeed. the only apparent refuges or defense mechanisms
Wilson 1975; VanBlaricom 1984a. 1984b; Estes and from sea otters available to most invertebrates are very
VanBlaricom 1985; VanBlaricom and Estes 1988). deep water (Estes. unpublished data), deep holes and
crevices in rocky substrates (Lowry and Pearse 1973),
Direct Effects of Sea Otter J;lredation being small in size (Estes et a!. 1989. Estes and
The direct reduction of benthic invertebrate populations VanBlaricom 1988). or sequestering of PSP toxins as a
by sea otter predation is the most general and well docu- chemical defense (Kvitek et al.. in review *). Burrowing
mented part of these complex relations. Several factors deep into soft sediments (K vitek and Oliver 1988: K vitek.
lead to the strong limiting intluence sea otters have on personal communication) is also thought to be effective,
26 BIOLOGICAL REPORT 90 (14)

although Kvitek commented that he recently observed sea more than an occasional sea urchin within the sea otter's
otters eating geoducks (Panopea generosa) in southeast- range in British Columbia. Furthermore, she found that
em Alaska and found huge pits they had excavated to several sites surveyed by Breen et al. ( 1982)-which at
obtain them. the time of their studies were outside the otter's range and
Evidence that sea otters have such profound limiting supported abundant sea urchin populations-had been
influences on many of their invertebrate prey populations reinhabited by otters and lacked sea urchins at the time of
comes mainly from comparisons of areas with and with- her surveys in summer 1987. One of her sites, which
out otters, through either space or time. For example, in lacked otters and supported an abundant urchin popula-
central California large sea urchins (Strongylocentrotus tion when she first surveyed it, was reinhabited by otters
purpuratus) are almost never found outside of protective when she revisited it about a month later, at which time
substrate cracks and crevices within the sea otter's ran~e she found little more than broken urchin tests covering
(Lowry and Pearse 1973; Foster and VanBlaricom 1986 ). the sea floor. Similar results have been obtained by
Yet sea urchins are among the most abundant, conspicu- Duggins ( 1980) for an area near Glacier Bay in southeast-
ous, and important invertebrates on rocky reefs that occur em Alaska. Sea urchins were abundant in Torch Bay, a
beyond the sea otter's range in central California (Foster site lacking sea otters; however, he was unable to find
and Schiel 1985, 1988; Harrold and Pearse 1987). We are more than an occasional urchin in nearby Surge Bay,
aware of only a single case in which abundant sea urchins where otters were abundant. Sea otters reinhabited Torch
have been reported within the sea otter's range in central Bay around 1986, and in an extensive survey of this area
California, and that is the report of Watanabe and Harrold done in May 1988 (including all five of Duggins' study
(Monterey Bay Aquarium, Monterey, Calif., unpublished sites) only an occasional small urchin could be found
manuscript) from an area known as "the pinnacles," lo- (Estes et al. 1989; Estes and Duggins, unpublished data).
cated about 1 km off the shore of Carmel Bay. These Estes et al. ( 1978) reported similar differences between
urchin populations seem to have developed following a islands with and without sea otters in the western Aleutian
heavy settlement event around 1985. Although this obser- archipelago, with one rather striking exception. At Am-
vation poses an apparent paradox with our previously chitka Island, where sea otters not only were abundant but
stated contentions, the urchin population at the pinnacles also apparently at or near equilibrium density, high den-
developed in rather deep water (20-30 m), and the pre- sities of small sea urchins (<35 mm and most <25 mm test
viously well-developed kelp canopy in the area has also diameter) were found, especially at depths greater than
been lost. It is still unknown whether the urchins occur about 10-15 m. At Shemya and Attu islands, where sea
below a depth at which sea otters can profitably forage otters were absent, sea urchins typically reached 65-
(as occurs in the Aleutian Islands), or whether otters have 85 mm test diameter. We subsequently surveyed a large
foraged at all in that area in recent years. It could be that number of sites in the western and central Aleutian Islands
loss of the kelp canopy has made the urchin populations and found that these urchin population structures were
at the pinnacles difficult for sea otters to locate, although predictably associated with the presence or absence of sea
this is unlikely. otters. Our preliminary analyses (Estes et al. 1989; Estes
Most sea urchin population reductions that have oc- and Duggins, in preparation) indicated that high densities
curred through time following the reestablishment of sea of small sea urchins persist amidst abundant sea otters for
otters have been documented anecdotal!;' (McLean 1962; two reasons: ( 1) sea urchins recruit heavily each year
Ebert 1968a,l986b; Benech 1977, 1981 ), and in all cases throughout the central and western Aleutian Islands, and
the reported patterns were similar. Laur et al. (1988) (2) there is a lower size limit below which urchins gain
conducted one of the few studies in California designed refuge from otter predation.
to document the community level effects of the expanding Sea otters are known to effectively limit populations of
sea otter population: within a year of the arrival of sea various other benthic invertebrates, such as Pismo clams
otters on their two study reefs, red urchin (S. fran- (Tivela stultorum), abalone (Haliotis spp.), Dungeness
ciscanus) and purple urchin (S. purpuratus) densities crabs, and mussels (Mytilus californianus and M. edulis;
declined to zero. Ebert 1968a, 1968b; Lowry and Pearse 1973; Wild and
There is similar evidence that sea otters limit sea urchin Ames 1974; Miller et al. 1974, 1975; Gotshall et al.
populations in other geographical areas. For example, 1976 *; Stephenson 1977; Estes and VanBlaricom 1985;
Breen et al. (1982) reported that sea urchins were rarely Wendell et al. 1986; Garshelis et a!. 1986; Kvitek and
found within the range of the sea otter in British Colum- Oliver 1988; VanBlaricom 1988). The behavior and dis-
bia, whereas outside the otter's range, urchins were per- tribution of certain prey, such as sea urchins and abalone,
haps the most conspicuous and important herbivore. A are also affected by sea otter predation. For instance, in
more recent survey by J. Watson (University of Califor- central California, abalone are found almost entirely in
nia, Santa Cruz, Calif., personal communication) has crevice refuges that, among other things. provide shelter
confirmed these patterns. She also was unable to find from foraging sea otters and perhaps other predators
 THE SEA OTTER: BEHAVIOR. EcoLOGY. AND NATURAL HISTORY 27

(Ebert 1968a; Faro 1970; Lowry and Pearse 1973; Cooper (1987) suggested that mussels were sporadically con-
et a!. 1977; Hines and Pearse 1982). Hines and Pearse sumed in areas supporting large aggregations of males.
(1982) presented evidence showing that the abundance, When this occurred, the foraging sea otters caused the
size, and species composition of abalone remained stable virtual local elimination of the mussel populations.
from 1972 to 1981 at the Hopkins Marine Life Refuge in The foraging pattern of sea otters in mussel (M.
Monterey-an area that had been occupied by sea otters californianus) beds along the exposed coast of central
for nearly 20 years-although the overall density and California is considerably different from that observed in
average size of abalones were substantially reduced from Prince William Sound. VanBlaricom ( 1988) found that
that found in areas not occupied by otters. Garshelis eta!. sea otters only feed sporadically in these mussel beds,
(1986) similarly concluded that sea otter predation was creating gaps remarkably similar in size to those caused
responsible for the collapse of the Dungeness crab fishery by wave shear on the outer coast of Washington (Paine
in eastern Prince William Sound-shortly after foraging and Levin 1981 ). However, gaps formed by sea otter
sea otters moved into the area, crab populations declined, foraging are created in calm seas when the otters can
and the fishery had to be closed. It was known that the effectively forage over the intertidal zone at high tide,
otters fed extensively on crabs and very likely reduced whereas gaps generated by wave shear are created during
crab populations; however, this case was confounded rough, stormy conditions.
somewhat by the fact that bivalve populations, which are VanBlaricom ( 1988) also reported that whereas sea
prey for Dungeness crabs, had declined substantially due otters were nonselective in the removal of patches of
to coastal uplifting from the great Alaska earthquake of mussels from the intertidal zones. they consumed only
1964. This perhaps, in tum, caused an observed long-term those individuals longer than about 40 mm. In Prince
decline in the crab population (Estes and VanBlaricom William Sound, mussel populations subjected to intense
1985). sea otter predation mainly contained individuals <40 mm
Sea otters also feed at high tide in intertidal communi- in shell length, seemingly because of such size-selective
ties. Intertidal mussels have been reported in dietary predation. It is interesting to note that this size preference,
studies of sea otters from the Kuril Islands to central and the resulting influence of sea otter predation on the
California. VanBlaricom (1987, 1988) has studied the size distribution of prey, is similar to that reported by
interaction between sea otters and intertidal mussel pop- Estes eta!. (1978, 1989) for green sea urchins (Strongy-
ulations in central California and Prince William Sound. locentrotus polyacanthus) in the western Aleutian Is-
In Prince William Sound, mussels (Mytilis edulis) are one lands.
of the main sea otter foods (Estes et a!. 1981 ). Sea otter The recent findings of K vitek and Oliver ( 1988) and
predation was found to reduce the size and density of Kvitek eta!. (1988) are in contrast with the view that sea
mussels, although this effect varied among areas, depend- otter predation is the major controlling influence on some
ing on age and sex composition of the local sea otter of their prey populations. Their study of a soft-bottom
population. Through translocation and caging experi- habitat in lower Elkhorn Slough demonstrated that sea
ments, VanBlaricom (1987) was able to demonstrate that otters had little effect on either the density or size distri-
growth rate and maximum attainable size of mussels were bution of infaunal bivalves. K vitek et a!. ( 1988) argued
comparable or greater in populations depredated by sea that sea otters incurred large time and energy costs in
otters than in unexploited populations. digging the deep-burrowing bivalves (Tresus nuttallii and
In Prince William Sound, VanBlaricom (1987) found Saxidomus nuttallii) that inhabited their study site, thus
that mussels were consumed primarily by recently preventing the otters from substantially reducing their
weaned juveniles and females with dependent pups, prey populations. Although this pattern may be at least
whereas they were rarely eaten by adult males or single partially a result of seasonal and recent sea otter occu-
females. Since sea otters segregate spatially by age and pancy, it contrasts with the well-documented interaction
sex, the composition of the local sea otter population between sea otters and Pismo clams (Miller eta!. 1975;
influences the extent to which mussels are consumed in a Stephenson 1977; Wendell et al. 1986), which are com-
particular area. Because of the high mussel abundance paratively shallow burrowers, and which decline quickly
and calm sea conditions throughout most of Prince Wil- and substantially following the arrival of sea otters in
liam Sound, it is likely that mussels are more easily areas supporting dense clam populations. Compelling
captured than other prey, such as decapods and burrowing evidence for this interaction is provided by Wendell et al.
bivalves, perhaps explaining why I
they are so commonly ( 1986), who reported that recreational landings of Pismo
eaten by juveniles and females with large pups. However, clams at Pismo Beach, California. declined to near zero
Garshelis (1983) suggested that whereas mussels were shortly after sea otters dispersed into the area. The large
easily obtained, their nutritional value was relatively low, male group of otters that caused the clam decline has since
possibly explaining why they were less frequently eaten moved on; there has been a heavy recruitment of clams,
by the more experienced adults. In addition, VanBlaricom and it is possible that a recreational fishery may again be
28 BIOLOGICAL REPORT 90 ( 14)

Fig. 18. (A) Kelp forest at Amchitka

Island. Alaska (the kelp understol)'
nearthe diver was cleared). (B) Sea
urchin barrens at Shemya Island,
Alaska (J. Estes).

possible. at least for smaller-sized Pismo clams. Estes and Indirect Effects of Sea Otter Predation
VanBlaricom ( 1985) reviewed the evidence for the effect Sea otters limit herbivorous sea urchins in many areas
of sea otter predation on benthic invertebrate populations of the North Pacific Ocean, which in tum promotes the
and speculated on the potential for sea otter depredations growth of kelp and other macroalgae. This scenario pre-
on a wide range of marine invertebrates. which are of com- dicts that rocky reef communities are dominated by kelps
mercial and recreational value throughout the historical and other macroalgae when sea otters are present, but that
range t)f the ->ca otter in the northeastern Pacific Ocean. these communities become deforested by sea urchin graz-
 THE SEA OTTER: BEHA vroR. EcoLoGY. AND NA ruRAL HrsTORY 29

ing when sea otters are absent (Fig. 18). Evidence for this California. VanBlaricom ( 1984a) used maps, prepared by
effect, summarized by Estes and Harrold (1988), is of the U.S. Department of Agriculture in 1911 and 1912, to
three general kinds: (1) comparative observations, either demonstrate that the areal extent of the surface kelp
between nearby areas with and without sea otters or canopy had expanded considerably and that species com-
through time with the reestablishment and growth of sea position shifted from bull kelp (Nereocystis leutkeana) to
otters at specific locations (Estes and Palmisano 1974; giant kelp (Macrocystis pyrifera) following expansion of
Estes et a!. 1978; Duggins 1980; Breen et a!. 1982; Laur the sea otter's range into these areas (Fig. 19). Duggins
eta!. 1988); (2) historical information on kelp beds with ( 1980) removed sea urchins from subtidal plots in south-
sea otter population changes (VanBlaricom 1984a); and eastern Alaska and found significant increases in kelp
(3) small-scale experimental manipulations that mimic settlement and growth compared with unmanipulated
the influence of sea otter predation (Duggins 1980). control plots. Similar results have been obtained from
Comparative studies provide the most well-known, and numerous other areas of the North Pacific Ocean, as well
probably the most compelling, evidence of the influence as elsewhere in the world (Harrold and Pearse 1987).
of sea otter predation on kelp forest communities. Estes There are various problems with all the evidence of
and Palmisano (1974) reported that rocky reef habitats at indirect effects of sea otter predation. Comparative obser-
islands with abundant sea otter populations in the western vations suffer from possible confounding influences of
Aleutian archipelago were characterized by dense stands spatial or temporal variation unrelated to the influence of
of kelps and other fleshy macroalgae, whereas compara- sea otter predation. Because kelp forest communities are
ble habitats at nearby islands lacking sea otters were known to vary substantially in space and through time
largely deforested. Similar reports were subsequently (Foster and Schiel 1985; Estes and Harrold 1988), this
published by Duggins ( 1980) for southeast Alaska, Breen problem could be notable. Historical reconstructions suf-
et a!. (1982) for British Columbia, J arne son et a!. (1986) fer from problems of interpretation, which is to say that
for Washington State, and Laur et al. (1988) for central changes correlated with the sea otter's recovery, but caus-
ally unrelated to the influence of sea otter predation.
cannot be discounted when attempting to interpret the
otter's role in observed changes. Furthermore, the quality
of historical information is often suspect and always
11 Km
N
poorer than that obtained from contemporary studies.

1 When properly done, experimental studies are not con-

founded by community effects unrelated to sea otter pre-
dation, although such studies probably experience other
problems. For example, while experimental treatment
effects usually are absolute (i.e., sea urchins are undis-
turbed or they are removed entirely), the effects of sea
otter predation may not be. Additionally, small-scale ma-
Bixby Creek Bixby Creek nipulations may produce effects different from those that
occur when the same factors change on a larger scale,
particularly if larval or spore dispersal is narrowly con-
fined. Nonetheless, these studies collectively provide
strong evidence that kelp beds are enhanced by sea otter
predation, and that this effect occurs widely in the North
Pacific Ocean. The important questions now are: (1) How
general is this scenario? (2) How broad is the influence
of sea otter predation on other kelp forest species? and (3)
What is the time course of community changes with the
reestablishment and growth of sea otters? These difficult
questions are being investigated.
Estes and Duggins (unpublished data) addressed the
Point Sur Point Sur Point Sur
question of generality by sampling a large number of
randomly selected sites from islands in the western Aleu-
tian archipelago with and without sea otters. Depending
7917 7972 7987 on which community characteristics were measured,
Fig. 19. Density and distribution of kelp beds in central Cali- these data showed that the extent to which benthic com-
fornia before and after the recolonization of sea otters (from munities between such areas differed was predictable. In
VanBlaricom 1984b). general, sites at islands without sea otters were deforested,
 30 BIOLOGICAL REPORT 90 (14)

whereas those at islands where otters were abundant urchins; otherwise. these areas remained as deforested sea
were not. urchin barrens with high densities of small individuals
The most predictable character of these communities preventing settlement and growth of macroalgae. How-
was sea urchin size distribution. Urchins with test diam- ever, at one site where sea urchins apparently recruited
eters >30-35 mm were seldom found at the islands with unpredictably, a kelp forest became reestablished soon
otters, whereas all of the samples from otter-free islands after otters reinhabited (J. A. Estes, unpublished data).
contained sea urchins with test diameters of 60-80 mm. Laur et a!. ( 1988) documented the structure of two reef
Sea urchin biomass per unit area was predictably low at communities near Point San Luis in central California
islands with otters, whereas it was high but variable at before and after sea otters became established in that area.
otter-free islands. Similarly, kelp densities were predict- One was a shallow-water, high-relief site, which sup-
ably near zero at otter-free islands, whereas they were ported a kelp bed before the arrival of sea otters. The other
high but variable at islands with sea otters. Watson's was a deeper-water, low-relief site, which was exten-
(personal communication) Vancouver Island data, which sively deforested (by sea urchin grazing) before the ar-
were obtained similarly to those of Estes and Duggins, rival of sea otters. Sea urchin densities declined to near
show similar patterns, except that sea urchins were virtu- zero at both sites within several months following the
ally absent from Watson's sites occupied by sea otters. arrival of otters. A kelp bed developed within a year in the
Ongoing research throughout the Kodiak archipelago and area that previously had been deforested, and the abun-
southeastern Alaska (Kvitek and Oliver, unpublished dance of several fish species also increased. Although
data), on the outer coast of southeastern Alaska near similar data are lacking from other geographic locations
Glacier Bay (Estes and Duggins, unpublished data), and in the northeastern Pacific Ocean, anecdotal evidence
in Sitka Sound (J. Estes, G. VanBlaricom, and D. Carney, suggests that where deforested habitats occur, these are
unpublished data) indicate patterns resembling those ob- transformed rather quickly into kelp beds following the
served in British Columbia. arrival of sea otters.
Comparable data from randomly selected sites in areas There has been further speculation that the interaction
with and without sea otters are lacking for California. between sea otters, sea urchins, and macroalgae can have
Foster and Schiel (1988) sent questionnaires to workers far-reaching influences on coastal communities (Estes et
familiar with different regions of the California coast, and a!. 1978). For example, reduction in the intensity of
based on the responses, they argued that sea otters play a herbivory by sea otter predation may promote strong
relatively minor role in California kelp forests, contend- competitive interactions within algal assemblages (Day-
ing instead that both sea urchin populations and ton 1975; Duggins 1980; Reed and Foster 1984). The
macroalgal assemblages are limited by a range of physical presence of kelp may act on coastal ecosystems in many
and biological factors. Consistent with this view, Laur et important ways. such as by providing food and habitat for
a!. ( 1988) concluded that substrate relief influences the other organisms or by altering water flow (Gerard 1976;
extent to which, in the absence of sea otter predation, Mann 1982: Jackson 1984; Ebeling eta!. 1985; Duggins
rocky-bottom habitats in California have become defor- 1988). Evidence for these influences is mainly supposi-
ested by sea urchin grazing. However, Foster and tional, coming from studies in which sea otters were not
VanBlaricom ( 1986 *) surveyed 9 sites within the sea a factor in the design, and usually not even a point of
otter's central California range from Villa Creek to Gran- concern. For example, several studies have shown im-
ite Canyon. Whereas site selection was not random (sam- portant relations between kelp and a number of fish
pling was done only under Macrocystis canopies), no species (Quast 1968a; Ebeling and Laur 1985, 1988;
evidence of grazing disturbance by sea urchins or other Ebeling eta!. 1985; Bodkin 1986, 1988; Simenstad, Estes,
invertebrates was noted. These sites were generally char- and Cowen, unpublished data). Kelp may create or im-
acterized by understories "that graded from Laminaria prove fish habitat, for instance, by providing shelter from
setchellii (a kelp) and articulated coralline algae in shal- predators (especially to juvenile fishes); by increasing
low water (6 m) to Pterygophora californica and encrust- overall substrate area; and by expanding the food base and
ing coralline algae in deeper water (:S;l5 m). Foster and habitat for kelp forest organisms that in tum provide food
VanBlaricom ( 1986 *) reported that among the sites, plant for fishes (Davies 1968; Quast 1968a, 1968b; Haaker and
densities and the cover of sessile invertebrates and algal Wilson 1975; Leamon 1976, 1980; Wilson et al. 1977;
turf varied considerably. Bodkin 1986). In the Aleutian Islands, populations of
Temporal and spatial patterns of community change certain fish species, most notably the rock greenling
following reestablishment of sea otters are even less well (Hexagrammos lagocephalus), occur at higher densities
known. In several sites at Attu Island, Alaska, Estes and in kelp habitats than in sea urchin barrens (Simenstad et
Harrold ( 1988) reported that the only remarkable change a!. 1978; C. A. Simenstad, J. A. Estes, and R. K. Cowen,
in benthic community structure with reestablishment of unpublished data). That sea otters themselves may be
sea otters was a reduction in the maximum size of sea influenced' by algal-fish interactions is indicated by the

~$&.{.,8!Hii.
 Tt-!E SEA 0TrER: BEHA vroR. EcoLOGY. AND N.uuRAL HISTORY 31

fact that in parts of Alaska and the Soviet Union, fish urchin grazing on attached macroalgae. In southern Cal-
constitute an important element of the otter's diet (Estes ifornia, commercial harvest of urchins may also limit red
eta!. 198 I, 1982). Similarly, Trapp ( 1979) and Irons et al. urchin populations within established kelp forests. The
( 1986) found that where sea otters were absent, glaucous- sunflower star (Pycnopodia he/ianrhoides) preys on ur-
winged gulls (Larus glaucescens) in the western Aleutian chins and may impose an important structuring influence
Islands fed extensively on sea urchins and other intertidal on some urchin populations, with consequent effects on
invertebrates but consumed mainly fish where sea otters macroalgae (Duggins 1983). Locally abundant popula-
were abundant. tions of sunflower stars occur from the eastern Aleutian
In the western Aleutian Islands, the importance of kelp Islands to central California. In addition, severe storms,
as a source of organic carbon between communities with sediment scour, changing climatic conditions, disease,
and without sea otters was studied by Duggins et al. and recruitment failure may limit sea urchin populations
( 1989). Their study was based on the fact that sessile along the California coast in areas not subject to heavy
macroalgae and water column-borne phyto:flankton fix sea otter predation (Pearse et al.l970 ~; Miller and Geibel
12 1
the two stable isotopes of carbon ( C and C) in differ- 1973; Pearse et al. 1977; Yellin et al. 1977; Pearse and
ent relative amounts. The study demonstrated that, al- Hines 1979; Cowen et al. 1982; Ebeling et al. 1985; Ebert
though stable carbon isotope ratios within species vary and Russell 1988).
considerably among sites at any given island, highly
significant differences existed between islands with and
without sea otters.
Foraging Behavior and Diet
Other Influences on Kelp Forest Communities
Kelp forest communities are influenced by many phys-
ical and biological processes, such as unstable substrata, Feeding and Diving Behavior
chronic surge or wave action, climatic and hydrographic
conditions (such as those accompanying the El Nino Sea otters forage in rocky substrate and soft bottom
Southern Oscillation [ENSO or "El Nino"] of 1982-83), communities, along the bottom as well as within the kelp
intensity and quality of available light, water temperature, understory and canopy. Foraging activity takes place
nutrient conditions, severe storms, and predation by other most frequently in subtidal zones. although otters also
kelp herbivores (see Dayton 1985; Foster and Schiel forage intertidally to some extent (Vandevere 1969 *;
1985; Schiel and Foster 1986 for reviews). However, Estes 1980; Kovnat 1982; VanBlaricom 1988; Harrold
discussion of these variables is beyond the scope of this and Hardin 1986; Jameson, unpublished data; Riedman,
review. Staedler, and Estes, unpublished data). In California, ot-
The diets of several other species or groups of consum- ters usually forage at depths of< 25 m (Wild and Ames
ers in California and Alaska overlap with the diet of the 1974; California Department of Fish and Game 1976*;
sea otter, including several asteroid species, octopus (Oc- Estes 1980; U.S. Fish and Wildlife Service 1980 *), be-
topus spp.), crabs, birds (gulls and eiders), harbor seals, yond which the canopy-forming kelps and certain prey
and fishes such as cabezon (Scorpaenichthys items become scarce (Abbott and Hollenberg 1976).
marmoratus) and wolf-eels (Anarrhichthys ocellatus). However, along the northern Monterey peninsula, certain
However, the extent to which competition for food occurs territorial males sometimes forage offshore in depths of
among these species is unknown. 30-40 m (Riedman, unpublished data: Deutsch, personal
Other sea urchin predators in central and southern Cal- communication), and in the center of the range, juvenile
ifornia include invertebrates (e.g., asteroids; Landenber- males tend to forage deeper and further offshore (1-
ger 1967; Rosenthal and Chess 1972; Dayton et al. 2 km) than other age or sex classes of otters (Ralls et al.
1980 *), spiny lobsters (Panulirus interruptus; Tegner and 1988a* , 1988b*). In the Aleutian Islands, in contrast, sea
Levin 1983; Robles 1987), and octopus, as well as fishes otters commonly feed at depths of 40 m or more (Estes
such as cabezon, wolf-eels, and California sheephead 1980).
(Semicossyphus pulcher; Hobson and Chess 1976; From direct observations of foraging sea otters, Estes
Cowen 1983). Sheephead are found primarily in southern et al. ( 1981) reported that average dives lasted from about
California, beyond the present range of the sea otter, 50 to 60s and that dives exceeding 125 s were extremely
although sea otters recently were relocated to San Nicolas rare. However, Ralls et al. ( 1988b*), using radiotelemetry,
Island where sheephead occur. In particular, sheephead found that 5 of 31 otters in central California had mean
predation seems to limit sea urchins (Nelson and Vance dive times exceeding 125 s, 12 individuals had maximum
1979; Cowen 1983). Cowen (1983) speculated that be- dives exceeding 200 s, and the maximum dive time
cause sheephead limit red and purple urchin populations recorded was 246 s. These findings indicate that visual
in some areas at San Nicolas Island, they may prevent studies are biased against animals feeding in deep
32 BIOLOGJCALREPORT90 (14)

Fig. 20. California sea otter holding red

sea urchin (Ston[?ylocentrotus francis-
canus) underwater (R. Mattison).

water far from shore. Maximum dive times in all age or capture large prey items that are less accessible but more
sex classes studied by Ralls et a!. ( 1988b *) ranged to rewarding in terms of energetic value (such as abalone
about 4 min; however, average dive time was longest and Cancer crabs) than are necessary to obtain less valu-
for juvenile males and shortest for females with pups. able prey (such as turban snails; Loughlin 1977; Costa
This pattern ret1ects their finding that juvenile males 1978a, 1978b; Estes et a!. 1981; Ralls et a!. 1988b *). As
tend to feed far from shore in deep water, whereas adult might be expected, surface times were highly correlated
females with pups tend to feed close to shore in with prey size and type, and lasted longest for large prey
shallow water. Ralls eta!. ( 1988b *) found that the mean such as abalone, large crabs, and octopus, which fre-
dive time and surface interval between dives for all in- quently took an otter several minutes to consume (Ralls
strumented otters was 74 s and 65 s. Most individuals et al. 1988b*).
differed significantly between day and night in length of Sea otters capture prey with their forepaws, often stor-
dives, but the direction of this difference varied among ing food items within loose t1aps of skin beneath the axilla
individuals. The average foraging bout duration of radio- of each foreleg until the prey can be consumed at the
instrumented otters studied by Ralls et a!. (l988b •) in surface (Barabash-Nikiforov 1947; Kirkpatrick et a!.
central California was between 77 and 373 min. Juvenile 1955; Fig. 20). A sea otter may capture two or more prey
females tended to have longer feeding bouts than other items of the same or different species ina single dive. Prey
age or sex classes. The fact that juvenile females have such as clams are captured by rapid and repetitive digging
long feeding bouts may be related to their tendency to in soft substrates with the forepaws, and the otter often
forage on small-sized prey (Riedman, Staedler, and Estes, dives several times before it can excavate the clam
unpublished data). The average interval between feeding (Shimek 1977a; Hines and Loughlin 1980).
bouts was 188 min, from the range of 81-300 min for
individuals.
An average of 70-73% of all diurnal feeding dives in Food Stealing
California result in the successful capture of prey
(Loughlin 1977; Estes eta!. 1981), although a complex Sometimes one otter steals another otter's food at the
array of variables may affect the proportion of successful surface (Fisher 1939; Miller 1980). It is possible that food
dives, type of prey obtained, dive times, and foraging stealing also takes place underwater, since a feeding otter
strategies (Estes et a!. 1981 ). Adult otters make unsuc- may occasionally surface while interacting with another
cessful dives more often than juveniles, although adults otter after a foraging dive. Incidents of food stealing are
also obtain more rewarding but less easily captured prey. common among mother-pup pairs, with older dependent
Longer dives-and often several dives-are required to pups regularly taking food from their mothers during a

5
 THE SEA OTTER: BEHAVIOR. ECOLOGY, AND NATURAL HISTORY 33

foraging bout. The majority of other food-stealing inci- phins, and (occasionally) polar bears (Ursus maritimus)
dents involve territorial males, who often take prey from as well as sea otters (Alcock 1972; Beck 1980). Tool use
females and mother-pup pairs foraging in their territory appears to be more frequent among sea otters in Califor-
(Riedman et a!. 1988 ). Territorial males do not seem to nia than in the Aleutian Islands (Estes, unpublished
be selective when stealing prey; they usually take what- observation). The reason for this may be the increased
ever food the female has obtained. Such males steal prey occurrence of more heavily shelled forms at latitudes
in which they do not specialize, as well as prey they obtain closer to the tropics (Vermeij 1978). In addition, Aleutian
on their own (Riedman, Staedler. and Estes, unpublished Island sea otters feed heavily on fish in areas such as
data). Generally, a female's food is stolen by a territorial Amchitka Island. in which case tool use is unnecessary.
male at least once or at most several times during a In Prince William Sound, however. otters frequently
complete foraging bout. Females usually relinquish prey use tools to open bivalves (Calkins 1978; Garshelis
to males with little resistance. A territorial male who is 1983).
pair-bonded to a female may also frequently steal her Sea otters may use rocks or other objects underwater to
prey. In fact, pair-bonded males sometimes solicit or steal pry loose or break apart prey such as urchins or abalone
prey from their mates in the same manner as dependent that adhere tightly to rocks or are wedged in crevices.
pups; the female occasionally even offers prey to the male About 80% of the abalone shells examined by Ebert
as she would to her pup. Particular territorial males may ( 1968a) in California had breakage patterns suggesting
steal food from females more often than others. An inter- that they had been struck by tool-using otters. Sea otters
esting male strategy, termed hostage behavior, has also along the northern Monterey peninsula often carry a rock
been observed along the Monterey peninsula. This occurs or other tool with them while diving underwater, yet do
when a male approaches and grabs a dependent pup while not always use it to break open captured prey only at the
its mother is foraging underwater. The pup is relinquished surface. When brought to the surface, mollusks (e.g.,
to the mother only when she gives the male her prey in abalone or rock oysters [Pododesmus cepio]) often bear
apparent exchange for her offspring (Riedman. Staedler, a large hole near the center of the shell, which it seems
and Estes, unpublished data). the otter created underwater with its tool (Riedman, un-
Stealing of food occurs occasionally between adult published observation).
females, one or both of which may be accompanied by a Recent research has shown that California sea otters are
pup. Observations of such incidents suggest that prey may quite versatile in tool use techniques and foraging tactics,
be selectively stolen by females. For example, in one case indicating well-developed learning and cognitive abili-
only abalone was taken. Whether such food stealing inci- ties. The most common form of tool use occurs when an
dents among adult females are based on age or social otter places a rock on its chest while floating on its back
status is currently under investigation (Riedman et al. and pounds hard-shelled prey (e.g., snails, mussels,
1988 *). Juvenile females have also been observed at- clams) against the rock as an anvil to crack open the outer
tempting to steal food from each other as well as from shell. Numerous variations of this method may be em-
adults (Riedman, Staedler, and Estes, unpublished data). ployed, and sea otters are capable of learning new and
However, Ralls and Siniff (1988*) found that juvenile innovative tool use techniques and capture strategies to
females often had food stolen from them and speculate enhance foraging ability (Riedman, Staedler, and Estes,
that their tendency to feed at different times (through- unpublished data). Sometimes an otter may use the rock
out a 24-h period) than other otters may reduce the tool as a hammer, or it may use two rocks as hammer and
chances that food is stolen from them. Only large and anvil. At other times, pieces of the shell or crab carapace
valuable prey was stolen from the juvenile females, may be broken off and pounded against the prey itself. In
indicating that such stealing was selective. Victims of addition to rocks, which are the most frequently used tool,
food stealing may either temporarily stop foraging, move to otters may use empty shells, driftwood, empty glass or
another location, or simply continue foraging in the same plastic bottles, aluminum beverage cans, and other man-
area. made objects discarded by humans (Riedman et al.
1988*). Live clams may also be pounded against each
other to break the shells in Alaska (Kvitek, personal
Tool Use communication) and California (Riedman, Staedler. and
Estes, unpublished data).
The use of tools such as rocks to break open or dislodge Many otters vary their tool use behavior appropriately
hard-shelled macroinvertebrates 'is common among sea with the particular prey species obtained. For instance, a
otters (Fisher 1939; Limbaugh 1961; Hall and Schaller female who captures both turban snails and purple urchins
1964; Kenyon 1969; Houk and Geibel 1974; Miller 1974; may eat the urchins using her teeth, then dive specifically
Fig. 21 ). Tool use is uncommon among mammals and for the purpose of obtaining a tool to crack the hard-
has only been reported in humans, chimpanzees, dol- shelled snails. Other feeding methods include rolling

z )Q_Q)_c:q.• J~~JIIM .:. :;: ~ .

34 BIOLOGICAL REPORT 90 (14)

Fig. 21. California sea otter using rock tool to break open prey (D. Buchich).

urchins between the paws to break off the spines and using
the hindflippers to hold crabs on the abdomen while Individual Variation in Diet
eating another food. An otter may even immobilize a crab and Foraging Tactics
by wrapping it in kelp fronds draped over the otter's
abdomen while it eats another food item (Riedman et al. There is substantial variation among individual Califor-
1988*). nia sea otters with respect to diet and the amount of time
Observations on tagged sea otters along the Monterey allocated to diving and foraging on the surface (Estes et
peninsula have shown that individual variation exists in al. 1981: Lyons a~d Estes !98S~: Riedman et al. 1988*;
tool use methods, as it does in choice of prey, with certain Lyons 1989). Among animals foraging within an area,
otters consistently using the same type of tool and tool individual variation in diet has also been documented in
use technique. An otter may also keep a tool to use tropical marine snails (Thais emarginata: T. melones:
throughout a particular forage bout (Riedman eta!. 1988 *: West 1986a. 1986b). Cocos Island finches (Pinaro/oxia
K. Lyons, Institute of Marine Sciences, University of inornata; Werner and Sherry 1987), possibly among chim-
California. Santa Cruz, unpublished data). For instance. panzees (Pan trog/odvtes; Goodall 1986). and in some
one tagged female in Monterey consistently used an ex- pinnipeds (Riedman I 990). In all of these cases. individ-
tremely large flat rock or slab of concrete underwater, uals specialize in particular foods or foraging strategies
seemingly to dislodge abalone. Another female in Mon- regardless of age, sex. or body morphology. For sea otters.
terey Harbor used a glass bottle to pry rock oysters these individual dietary patterns seem to vary greatly in
from rocks beneath the surface. Studies on the cognitive their energetic profitability. For example, from estimates
aspects of tool use abilities in captive sea otters are of caloric content of prey (Costa 1978a) and prey-specific
currently under way at the Monterey Bay Aquarium search. pursuit and handling times (Estes et a!. I 98 I).
(J. Cur land, R. Gisiner and R. Schusterman. Moss Landing Estes eta!. (I 989) calculated that foraging times required
Marine Laboratories, Moss Landing, Calif.. personal to meet daily energy intake ranged from <4 to >21 h for
communication). the individual sea otters studied by Lyons (I 989) .

.. . . . ......,......_,,~z;g·---·
 THE SEA OTTER: BEHAVIOR. EcoLOGY. AND N.-'\TURAL HISTORY 35

Fig. 22. California sea otter consuming kelp crab. Pugettia, (D. Buchich).

Although diet of the sea otter population in a given area changes in dietary composition and foraging tactics as an
may be extremely diverse, individual otters tend to spe- animal matures. Observations of tagged weaned pups and
cialize on selected prey (usually l-3 species). In the juvenile offspring of tagged females indicate that juvenile
Monterey area, for instance, one female fed on mussels. females may in fact forage on the same types of prey, and
kelp crabs, and turban snails (Fig. 22); another female employ the same tool use method and use similar foraging
specialized in clams and fat innkeeper worms (Urechis strategies as their mothers (Riedman et al. 1988*: Ried-
caupo); and a territorial male ate turban snails (Tegula) man et al. 1989\
almost exclusively (Riedman. Staedler and Estes, unpub- Sea otters exhibit individual differences not only in
lished data). These individual patterns seem to persist for choice of prey, but also in choice of tool. method of tool
at least 2.5 years (Lyons 1989) to 5 years (Riedman eta!. use, area in which they tend to forage. water depth (e.g.,
1988~). However, Lyons (unpublished data) found that some otters consistently forage in the intertidal or shallow
the diet of tagged females changed predictably with birth water areas), and other foraging strategies. A few otters
and again with ~eaning of their pups. According to Ried- solicit food from humans, and one otter learned to reach
man eta!. (I 988 ·).the diet and foraging strategies of some into a bucket on the stem of a boat in Monterey Harbor
(but not all) tagged females vary with their reproductive to obtain squid (Loligo opalescens ). Another otter. a ju-
status (the presence of a pup. age of pup, and period in venile female raised in Monterey Harbor. regularly waits
which a female is in estrus). In Prince William Sound. the for hand-outs of bait fish such as anchovies (Engraulis
diet of females with pups was often of poor quality mordax) from tourists, occasionally threatening adult
because the mothers frequently foraged on prey items of male California sea lions for their anchovies. In another
low nutritive value that were ~asily captured by pups instance. a male otter learned to bite into aluminum bev-
(Garshelis 1983: VanBlaricom 1988). erage cans and extract small octopuses that had taken
Currently in progress in Monterey are investigations refuge inside (McC!eneghan and Ames 1976). Another
that focus on the acquisition of individual foraging strat- male otter (presumably one individual) learned to cap-
egies in otters. development of foraging skills in pups. and ture. kill. and eat large seabirds. as have other otters in the

; .• • • •ISIIUII
.•~Jt[(! "b," "-" '·"'"~·
36 BIOLOGICAL REPORT 90 (14)

northern part of the California range (Riedman and Estes established for long periods (e.g., Amchitka Island), fish
1988a). Using radio-instrumented sea otters, Ralls et al. constitute an important part of the diet (Fig. 23). The high
( 1988b*) reported individual differences in length of dive, proportion of fish in the diet of Amchitka Island sea otters
surface interval between dives, feeding bout length, inter- is apparently associated with an increased availability of
val between feeding bouts, and nocturnal versus diurnal nearshore fish and a corresponding scarcity of benthic
feeding patterns. invertebrates, such as sea urchins. As populations of
herbivorous invertebrates at Amchitka were reduced by
sea otter predation, the abundance of kelp beds and
Diet in Alaska and the Soviet Union nearshore fishes inhabiting kelp forest communities has
increased. In contrast, sea otters feed primarily on sea
Whereas the diet of California sea otters consists pri- urchins (Strongylocentrotus polyacanthus), as well as
marily of macroinvertebrates, sea otters in Alaska and various crustaceans and molluscs, in recently reoccupied
Russia feed on epibenthic fish as well as invertebrates in areas of the Aleutians (such as Attu Island), where otter
many areas where the otter populations are near equilib- populations exist below equilibrium densities. Fish are
rium density (Simenstad et al. 1977; Estes et al. I 978, rarely consumed in such areas (Estes et al. 1982).
I 982). Prey availability varies with location and the time These ecological relations may have profound influ-
an area has been occupied by sea otters; it also influences ences on the behavior and population biology of sea
diet (Table 3). otters. For example, Estes et al. (1982) showed that fish
In areas of Alaska where otter populations have been were captured by sea otters at Amchitka Island only near

Table 3. Prey reported to be consumed by sea otters (Enhydra lutris) throughout the range. (Principal sources:
California-U.S. Fish and Wildlife Service 1982 [and references therein], Lyons 1989, R. Kvitek, University of
Washington, personal communication, f. Vandevere, Pacific Grove, Calif., personal communication,
G. VanBlaricom, Fish and Wildlife Service, Santa Cruz, Calif., personal communication; Oreeon-Jameson 1975;
Washington-Bow/by 1988* ; Southeast Alaska-Rosenthal and Barilotti 1973* , Pitcher 1987¥, R. Kvitek, personal
communication; Aleutian Islands-Kenyon 1969, Estes et al. 1981, f. Estes, unpublished data; Commander
lslands---Barabash-Nikiforov 1947,A. Zorin, Soviet Ministry ofFisheries, Moscow, personal communication; Prince
William Sound-Calkins 1978, Estes et al. 1981, R. Kvitek, personal communication, G. VanBlaricom, personal
communication; Kodiak archipelago---R. Kvitek, personal communication; Shumagin lslands-R. Kvitek, per-
sonal communication.)
Prince
Southeast Aleutian Commander William Kodiak Shumagin
Prey California Oregon Alaska Islands Islands Sound archipelago Washington Islands

Echiura
Echiurus echiurus X
Urechis caupo X

Nemertea
Emplectonema sp. X

Annelida
Polychaeta
Arenicola sp. X
Eudistylia po(vmorpha X
Eudistylia sp. X X
Nereis sp. X
Nereis vexillosa X

Arthropoda
Crustacea
Cirripedia
Thoracica
Balanus cariosus X
Balanus nubilus X X

---- -~------~-------~-----~--~-~-------- -.-~--.

 THE SEA OTTER: B EHA VI OR. EcoLOGY. AND NATURAL HISTORY 37

Table 3. Continued.
Prince
Southeast Aleutian Commander William Kodiak Shumagin
Prey California Oregon Alaska Islands Islands Sound archipelago Washington Islands
Lepas anatifera X

Malacostraca
Isopoda
ldotea sp. X
Isopod (unidentified) X
Amphipoda
Amphipod (unidentified) X
Gammarus sp. X
Decapoda
Blepharipoda occidentalis X
Cancer antennarius X X
Cancer magister X X X X X
Cancer oregonensis X
Cancer productus X X
Cancer sp. X X
Chionecetes bairdi X
Chionecetes opillio X
Cryptolithodes sitchensis X
Dermaturus mandtii X
Emerita analoga X
Hapalogaster cavicauda X
Hapalogaster grebnit=kii X
Hemigrapsus sp. X
Hyas coarctatus X
Lopholithodesforaminatus X
Loxorhynchus crispatus X
Pachygrapsus crassipes X
Paguristes sp. X
Pagurus gilli X
Pagurus hirusutiusculus X X
Pagurus sp. X
Panulirus interruptus X
Placetron wosnessenski X
Pleuroncodes planipes X
Pugettia producta X X
Pugettia richii X
Pugettia sp. X
Sc/erocrangon boreas X
Te/messus cheiragonus X X X
Mollusca
Gastropoda
Astraea gibberosa X
Astraea undosa X
Alxobuccinium oregonensis X
Buccinium sp. X
Calliostoma sp. X
Crepidu/a adunca X
Haliotis cracherodii X
Haliotis kamtschatkana X
Haliotis rufescens X
Haliotis walal/ensil X
Haliotis sp. X
Lottia gigantea X
Lottia ochracea X
Megathura crenulata X
38 BroLOG!CALREPORT 90 (14)

Table 3. Continued.
Prince
Southeast Aleutian Corrunander William Kodiak Shumagin
Prey California Oregon Alaska Islands Islands Sound archipelago Washington Islands

N atica clausa X X
N otoacmaea persona X
Polinices lewisii X
Tectura spp. X
Tegula brunnea X
Tegula funebralis X
Tegula montereyi X
Tegula pulligo X
Tegula sp. X
Thais sp. X
Bivalvia
Clinocardium ciliatum X
C linocardium facanum X
Clinocardium nuttallii X X
Gari californica X
Hiatella arc·tica X
Hinnites giganteus X
Hinnites multirugosus X
Humilaria kenerlia X X X X
Liocyma viridis X
Macoma incongrua X
Macoma inquinata X X
Macomasp. X X
Modiolus modiolus X X X X
Musculus niger X
Musculus vernicosa X
Musculus sp. X
Mytilus californianus X X X
Mytilus edulis X X X X X
Mya arenaria X
Mya truncata X X X X
Panopea generosa X X
Pecten beringianus X
Pecten islandica X
Pododesmus cepio X
Pododesmus macroschisma X X
Protothaca staminea X X X
Protothaca sp. X X X
Sa.xidomus giganteus X X X X
Sa.xidomus nuttalli X X
Sa.xidomus sp. X
Serripes groenlandicus X X
Siliqua patula X X
Solen sicarius X
Spisula alascana X
Spisula hempellz.a X
Tage!us californianus X
Tivela stultorum X
Tresus capax X X
Tresus nuttallii X X
Venericardia paucicostatus X
Voluplopsius beringi X
Polyplacophora
Callistochiton aassicostatus X
C ryptochiton stelleri X X X X X X
Ischnochiton sp. X
 THE SEA OTTER: BEHAVIOR, ECOLOGY, AND NATURAL HISTORY 39

Table 3. Continued
Prince
Southeast Aleutian Commander William Kodiak Shumagin
Prey California Oregon Alaska Islands Islands Sound archipelago Washington Islands
Mopaliasp. X
Schizoplax hrandtii X
Tonicella marmorea X
Tonicella ruher X
Cephalopoda
Loligo opa/escens X
Octopus sp. X X X X X
Polypus sp. X

Echinodennata
Echinoidea
Dendraster excentricus X X
Strongylocentrotus
drohachiensis X X X
Strongylocentrotus
fi·anciscanus X X X X
Strongylocentrotus
po/yacanthus X
Strongylocentrotus
pwpuratus X X X
Asteroidea-
Asterina miniata X X
Ceramaster sp. X
Evasterias troschelii X
Henricia sp. X
Leptasterias sp. X
Pisaster hrevispinus X
Pisaster giganteus X
Pisaster ochraceus X X
Pycnopodia helianthoides X X

Ophiuroidea
Brittle star X
Gorgonocepahus eucnemis X
Holothurioidea
Cucumaria miniata X X
Cucumaria piperata X
Cucumaria sp. X X X
Parastichopus sp. X

Chordata
Ascidiacea
Stye/a montereyensis X
Tunicata X
Pisces
Ammodytes hexapterus X X
Anoplopoma fimbria X X
Aptocyclus ventricosus X
Cottidae X X
Cyclopterichthys glaber \ X
Embiotocidae X
Gadus morhua X X
Gymnocanthus pistilleger X
Hexagrammos superr:iliosus . X
Hemgrammos sp. X X
Hemilepidotus hemilepidotus . X
40 BIOLOGICAL REPORT 90 ( 14)

Table 3. Continued
Prince
Southeast Aleutian Commander William Kodiak Shumagin
Prey California Oregon Alaska Islands Islands Sound archipelago Washington Islands
Hem ifepidotus jordan i X
Lepidopsetta hilineata X
Mallotus J•i!losus X
Oncorhvnchus nerka X
Pleurogrammus
monoterygius X
Theragra cha!cograma X
Aves
Anatidae
Anas crecca X
M e/anitta perspici/lata X
Gavidae
Gaviaimmer X
Laridae
Larus sp. X
Phalacrocoracidae
Phalacrocorax sp. X
Podicipedidae
Aechmophoru.s occidentalis X

a Indirect evidence of foraging noted; actual feeding not observed.

Fig. 23. Sea otter eating fish at Adak Island. Alaska (1. Watson).
 THE SEA OTIER: BEHAVIOR, EcoLOGY. AND ~ATURAL HISTORY 41

dawn and dusk, and they speculated that die! variation in Shitikov 1970; Shitikov eta!. 1973).
the availability or vulnerability of fishes caused the dis- Dietary composition also changed seasonally among
tinct crepuscular peaks in foraging activity observed sea otters in the Kuril Islands. In winter, sea otters con-
there. Estes (1990a) speculated that the inclusion of fish in sumed mainly sea urchins and mollusks, while in summer.
the sea otter's diet resets the equilibrium population size the diet broadened to include fish. fish eggs, octopus, and
of otters well above that which is attainable on a diet of crab (Barabash-Nikifovov 1947: Shitikov 1971 ). In the
invertebrates alone, thus perhaps explaining the 3- to Aleutian Islands, rock greenling may be most vulnerable
5-fold differences in population size reported for Am- to otter predation in summer. when they spawn and must
chitka Island by Kenyon ( 1969; about 1,500 in 1965) and defend their eggs. Sea urchins attain maximum gonadal
Estes (1977, 1990a; 5,000 individuals in 1972 and 1986). development in winter, which is probably when they are
Estes et al. ( 1989) suggested that, for the sea otter, forag- of highest nutritional value to otters. A similar situation
ing on fish is a dietary innovation that may have been lost may exist at the Kuril Islands.
when the species was reduced to a few remnant colonies
at the end of the fur hunting era. We hypothesize that
benthic invertebrates were more common and nearshore Diet in California
fishes more rare when otters were near extinction, and that the
economics of prey choice may have excluded fish from In recently reoccupied habitats of central California. the
the otter's diet under those circumstances. Our studies of diet consists principally of abalones (Haliotis spp.), rock
prey selection in California have shown highly individu- crabs (Cancer spp.), and large red sea ~rchins (S.
alized diets (Lyons and Estes 1985 *; Riedman et a!. franciscanus; Ebert 1968a; Vandevere 1969 ; Wild and
1988 *), which may possibly be inherited matrilineally Ames 1974; Wade 1975; Stephenson 1977; Benech
(from mother to pup; Riedman et al. 1989*). If similarly 1981 *; Estes et a!. 1981 ). These food items are higher in
individualized diets occur in Alaska-and if foraging on caloric value and therefore more rewarding than other
fish requires search and capture skills substantially differ- prey species (Costa 1978a, 1978b ). In time, populations
ent from those required for feeding on benthic inverte- of preferred prey are reduced by sea otter predation, and
brates-then the innovation of foraging on fish by individ- diet at the population level diversifies to include large
uals in a population that had lost this behavior may occur numbers of food items: kelp crabs (Pugettia spp.), clams
only rarely. However, under the ecological conditions (various spp.), turban snails, mussels (Mytilus spp.), oc-
where this behavior is cost-effective (i.e., when otter popu- topus (Octopus spp.), barnacles (Balanus spp.), scallops
lations are food-limited, benthic invertebrates are rare, (Hinnites spp.), fat innkeeper worms, sea stars (Pisaster
and fish are common), once the innovation occurred it spp.), and chitons (Cryptochiton spp.; Boolootian 1961;
would be expected to grant an advantage to the individu- Limbaugh 1961; Ebert 1968a; Hennessey 1972; Wild and
als who adopted it, and might thus be expected to spread Ames 1974; Estes 1980; Benech 1981 *; Estes et al. 1981;
rapidly through the population by way ofleaming. Although Ostfeld 1982; U.S. Fish and Wildlife Service 1982; J ame-
largely speculative, these processes would explain the tim- son, unpublished data). Predation on fish in California is
ing of the population change seen at Amchitka Island extremely rare (Hall and Schaller 1964; Miller 1974;
(Estes 1981 ), as well as the comparatively small sea otter Estes et al. 1981; U.S. Fish and Wildlife Service 1982).
population at Medny Island in the Commander Islands (i.e., Surprisingly, while wild otters are rarely observed eating
about 1,000 at an island similar in size to Amchitka), which kelp, the captive sea otters at the Monterey Bay Aquarium
appears to be food-limited but where individuals nonethe- frequently consume giant kelp. The four exhibit otters
less do not feed on fish (A. Zorin, Soviet Ministry of share one large piece of kelp once or twice each week,
Fisheries, Moscow, U.S.S.R., personal communication). when available. They appear to prefer the stipes and
In the Kuril Islands of the Soviet Union, a similar relation bulbous gas floats; they eat these parts first when given
exists among diet, long-term and seasonal changes in prey an unlimited supply of kelp. However, the exhibit otters
availability, and the length of time a given area has been seem to eat kelp so readily because of its novelty, rather
occupied by sea otters (Fig. 24). At Simushir Island, than using it as a food source (Hymer, personal commu-
where the sea otter population was below equilibrium nication). Table 4 provides a complete list of prey items
density in the late 1960's, sea urchins were large and consumed by otters in California. Some of these species
abundant, and otters consumed them almost exclusively are consumed frequently, while others are eaten only
(Shitikov 1973). However, a4 Urup and Paramushir is- rarely.
lands, where sea otter populations had been established Dietary composition in California is also influenced by
for many years, sea otters consumed a substantial amount habitat type and time of year. Bivalve molluscs are heav-
offish, in addition to various bivalve molluscs (Modiolus ily consumed in soft-sediment communities. For exam-
difficilis, Mytilus edulis, and Tellina spp.) and sea urchins, ple, Pismo clams make up a significant proportion of the
which were small and relatively scarce (Maminov and diet of sea otters foraging along the sandy shores of
 .j::..
N

to
6
§
~
~~
200km ~
,__.
~ ~

00 Bering Sea
~ Unimak I.
~~~
"
A ~...i-.t )?. . ~

Beriog I. 'II. "% <1-/· · / .<?!~

.
)1
~·-
-
' /' C::l'
Medny I. C::I·.·C::I· N
<(O'V( .
~j~·

l~·N
,~,-c.~o~o'~,i,~~
/
1\!e
.
~
<lr t
oS'f.:l.
I?O's
~0\) ·9
;~
I
. ,~,'().~
0~

A!lul.~... 7 180° w ,r.o\ \';,\ar.os .t!l

G
<(Oi-

Aat Islands

. ~y~-~~··-~~
p..r.o(e"' 0

Shemya I. ~ ·~o e
. ... .. '41 c:

~
Amchitka I.
o" .

Kanaga I.
Adak 1.

Pacific Ocean
Fig. 24. Aleutian and Commander islands, indicating areas referred to in text.
 THE SEA 0ITER: BEHAVIOR. ECOLOGY, AND NATURAL HISTORY 43

Table 4. Scientific and comon names of prey items of the California sea otter (Enhydra lutris). Some of these species
are commonly eaten, while others are rarely consumed. a
Phaeophyta Pododesmus cepio (rock oyster or abalone jingle)
Prothothaca staminea (littleneck clam)
Kelp (Macrocystis pyrifera)
Saxidomus nuttallii (Washington clam)
Echiurida
Siliqua patula (northern razor clam)
Urechis caupo (fat innkeeper)
Solen sicarius (razor clam)
Annelida
Spisula hempellz.a
Polychaeta
Tagelus californianus Gacknife clam)
Eudistyla polymorpha (sabellid worm)
Tivela stultorum (Pismo clam)
Nereis vexillosa (clam worm)
Tresus nuttallii (gaper clam)
Arthropoda
Amphineura
Crustacea
Polyplacophora
Cirripedia
Cryptochiton stel/eri (gumboot chiton)
Thoracica
Ischnochiton sp. (chiton) .
Balanus nubilis (barnacle)
Callistochiton crassicostatus (chiton)
Malacostraca
Cephalopoda
Decapoda
Loligo opalescens (market squid)
Blepharipoda occidentalis (spiny sand crab)
(also squid egg case)
Cancer antennarius (rock crab)
Octopus spp. (octopus)
Cancer magister (Dungeness crab)
Cancer productus (red crab) Echinodermata
Cryptolithoides sitchensis (umbrella crab) Echinoidea
Emerita analoga (sand crab) Dendraster excentricus
Hapalogaster cavicauda (furry crab) Strongylocentrotus franciscanus (red sea urchin)
Hemigrapsus spp. (purple shore crab) Strongylocentrotus purpuratus (purple sea urchin)
Lopholithodes foraminatus (stone crab) Asteroida
Loxorhynchus crispatus (decorator crab) Asterina miniata (bat star)
Pachygrapsus crassipes (green shore crab) Pisaster brevispinus (short-spined sea star)
Paguristes sp. (hermit crab) Pisaster giganteus (sea star)
Panulirus interruptus (California spiny lobster) Pisaster ochraceus (common sea star)
Pleuroncodes planipes (pelagic red crab) Pycnopodia helianthoides (sunflower star)
Pugettia producta (kelp crab) Ophiuroidea
Pugettia richii (kelp crab) Gorgonocepha/us eucnemis (basket star)
Mollusca Holothurioidea
Gastropoda Cucumaria miniata (orange sea cucumber)
Astrea gibberosa (brick-red top snail) Cucumaria piperata (black-speckled white sea cucumber)
Astrea undosa (wavy turban snail) Parastichopus (sea cucumber)
Calliostoma sp. (top snail) Chordata
Crepidula adunca (hooked slipper shell) Ascidiacea Stye/a montereyensis (stalked tunicate)
Ha/iotis cracherodii (black abalone) Pisces
Ha/iotis rufescens (red abalone) Scorpaeniformes
H aliotis walallensis (flat abalone )b Cottidae (sculpins)
Lottia gigantia (owl limpet) Hexagrammidae
M egathura crenulata (giant key hold limpet) Hexagrammos sp. (greenling)
Polinices lewisii (giant or Lewis' moon snail) Perciformes
Tegula brunnea (brown turban snail) Embiotocidae (surfperches)
Tegulafunebra/is (turban snail) Aves
Tegula montereyi (turban snail) Anatidae
Tegula pulligo (turban snail) Melanitta perspicillata (surf scoter)
Bivalvia Gavidae
Clinocardiumfacanum (cockle) Gavia immer (common loon)
Clinocardium nuttallii (basket cockle) Laridae
Gari californica (sunset clam) Larus sp. (gull)
Hinnites giganteus (rock scallop) Phalacrocoracidae
Modiolus(= Volsella) modiolus (giant horse mussel) Phalacrocorax sp. (cormorant)
Mytilus californianus (California sea mussel) Podicipedidae
Mytilus edulis (bay musscl) Aechmophorus occidentalis (western grebe)

• Sources: U.S. Fish and Wildlife Service 1982; Reidman and Estes 1988b*; Riedman, Staedler, and Estes, unpublished data; R. Kvitek, personal
communication; G. VanBlaricom, personal communication.
b Indirect evidence of foraging noted; actual feeding not observed.

··········-!!J!!Illt!IJI!£!11'l_"~J!l"lf". . . "',.*. ,. +"'~. . _-,. ,_ ~-~-.A">'l'!JI " - '! I!W -.

......
, -~.r.~•-"'•~-·~--
ti4!H'...,...,.....,
PII'I!@"'J!O!iO""ZII!MA_.,._ _ _ _ _ _ _.. ...
44 BIOLOGICAL REPORT 90 ( 14)

Fig. 25. (A) California sea otter stalking male

surf seater in Monterey. (B) Same otter as
in (A) holding surf seater on abdomen
(G. Cathers).

Monterey Bay and Atascadero State Beach near Morro unpublished data). Large-scale, unusual oceanographic
Bay (Miller et a!. 1975: Wade 1975; Shimek 1977b; conditions, such as the "El Nifio" event of the early
Stephenson 1977; Hines and Loughlin 1980). In the Elk 1980's, can supply additional food resources such as the
hom Slough estuary of Monterey Bay, sea otters primarily pelagic red crab (Pleuroncodes planipes; K: J. Lyons,
consume the deep-burrowing bivalves Tresus mma/!ii unpublished data; Riedman, Staedler, and Estes, unpub-
and Saxidomus nuttallii (K vitek eta!. 1985, 1988; Kvitek lished data), which otherwise occurs farther south.
and Oliver 1988). In Prince William Sound. the diet of
otters feeding in soft-sediment areas of Montague Strait
consists principally of clams (particularly Saxidomus Predation on Seabirds
giganteus), which represent the most abundant food
resource (Calkins 1978) ..-\t Green Island and Sheep Bay Sea otter predation on seabirds occasionally occurs in
in Prince William Sound. otters consume primarily mus- California (VanWagenen et a!. 1981; Riedman and Estes
sels and clams (Estes et a!. 1981). 1988a), as well as in Alaska (Kenyon 1969; Fig. 25).
Squid spawning takes place during fall and spring in Riedman and Estes (1988a) described recent incidents of
Monterey Bay. At this time. squid constitute a substantial predation on seabirds and reviewed previous observa-
portion of the diet of some individuals. as foraging tactics tions of such predation in California and Alaska. Their
shift to take advantage of this seasonally abundant foo,? findings are summarized in the next paragraph. At Am-
source (California Department of Fish and Game 1976 ·; chitka Island, three cases have been reported, involving
Ames. unpublished data: Riedman, Staedler. and Estes, either a shearwater (Puffinus sp.) or fulmar (Fulmarus
 THE SEA 0ITER: BEHAVIOR, ECOLOGY, AND NATURAL HISTORY 45

glacialis) in one case, a pelagic cormorant (Phala- Islands (Sidorov 1987) and at Kodiak Island, Alaska, may
crocorax pelagicus; Kenyon 1969), and a green-winged have been caused by PSPT, because butter clams constitute
teal (Anas crecca; P. Holden, Utah State University, a major food resource there (DeGange and Vacca 1989).
Logan, unpublished data). In 20 cases in California, Kvitek et al. (in review *) investigated the little known
seabirds consumed included western grebes (Aech- but potentially significant effects of PSPT on sea otters
mophorous occidentalis), surf seaters (Melanitta per- by observing the behavior of five captive Alaskan sea
spicillata), cormorants (Phalacrocorax spp.), common otters that were fed butter clams containing various levels
loons (Cavia immer), and gulls (Larus spp.). Western of STX. They found that the otters either significantly
grebes were most frequently captured. The amount of reduced their feeding rates when given only high toxicity
nourishment derived from seabirds is unknown,.although prey or discarded clam siphons and kidneys, which con-
Kirkpatrick et al. (1955) and Kenyon (1969) presented tain most of the toxins. Most of the otters changed their
evidence that the flesh of cormorants and emperor geese feeding behavior rapidly after being given toxic clams.
(Chen canagica; fed to a captive otter) passed largely One female, who consumed the highest amount of STX,
undigested through the gastrointestinal tract. cracked the toxic clams and held them to her mouth, but
Most recorded incidents of sea otter predation on sea- then emitted screams and discarded them. She was the
birds in California have taken place in the northern part only otter to exhibit any obvious PSPT symptoms, such
of the range in three areas: Point Lobos, Stillwater Cove, as lack of coordination, sluggishness, and paralysis
and Monterey Harbor. (Several additional incidents of (Quayle 1969; Kvitek and Beitler 1988, 1989).
predation on birds between Santa Cruz and Granite Canyon These results suggest that sea otters, while not immune
near Soberanes Point have been reported since the Ried- to PSPT, are able to detect and avoid consumption of
man and Estes [ 1988a] review; Riedman, unpublished lethal levels of this toxic prey, and so are probably not at
data). Sea otters often initially capture the bird by diving mortal risk from PSPT. Kvitek et al. (in review *) sug-
and grabbing it from underwater while the bird floats on gested that sea otters may have not dispersed into other-
the surface, similar to the capture methods used by coastal wise suitable food-rich habitat because they are avoiding
river otters to obtain seabirds. If one compares mink, river PSPT-contaminated prey, especially in areas of southeast
otters, and sea otters, a graded reduction in the tendency Alaska known for the occurrence of PSPT and where
to consume birds seems to have taken place in the more butter clams are the primary prey of sea otters (K vitek and
aquatic mustelids, so that the relative importance of birds Oliver, unpublished data). The lack of overlap between
is greatest in mink (Mustela vison) and least in sea otters. the present (and historic) range of sea otters and the broad
Riedman and Estes (1988a) also point out some possi- geographic areas in southeastern Alaska known to contain
ble trends with respect to the incidents of sea otters highly toxic prey further supports this contention. Such
foraging on seabirds: (1) Particular individuals may re- potential exclusion of the sea otter from otherwise suit-
peatedly prey on seabirds, with six birds at Point Lobos able habitat has significant influences on the nearshore
killed by what appeared to be the same otter; (2) otters in marine communities and shellfisheries in these areas.
a particular area may learn new foraging strategies by
observing other feeders; and (3) male sea otters seem to
be involved in the majority of seabird-eating cases (al- Activity Patterns and Time Budgets
though the otter's sex was not determined in all incidents).
This tendency for males to feed on warm-blooded prey
coincides with a similar trend among other mammals that Many complex variables influence activity patterns and
sometimes feed on birds and mammals, such as chimpan- the amount of time allocated to various activities in sea
zees (Goodalll986) and some pinnipeds (Riedman 1990). otters, and they seem to be related to factors in the
environment and in the individual. Diurnal activity cycles
of sea otters tend to be characterized by crepuscular peaks
Effects of Paralytic Shellfish Poisoning (PSP) in foraging activity and a midday (late morning to late
afternoon) period of rest in California (Fisher 1939; Hall
Sea otters prey on numerous bivalve species that accu- and Schaller 1964; Sandegren et al. 1973; Miller et al.
mulate paralytic shellfish poisoning toxins (PSPT) during 1975; Loughlin 1977; Shimek and Monk 1977; Benech
blooms of toxic dinoflagellates (Protogonyaulax spp.; 1981 *; Ribic 1982b; Estes et al. 1986; Ralls and Siniff
Quayle 1969; Kvitek and Oliver 1988). Specifically, 1988 *), in the Aleutian Islands (Lensink 1962; Kenyon
Alaskan sea otters prey heavily'On the butter clam, which 1969; Estes 1977; Estes et al. 1982), and in some areas of
sequesters the most-lethal PSPT, saxitoxin (STX), and Prince William Sound (Garshelis 1983; Fig. 27).
which may retain the toxin for a year or more after being In California, Loughlin (1977, 1979) made observations
exposed to a toxic bloom (Chambers et al. 1955 *; Boyer using radiotelemetry over a 24-h period and found that
et al. 1986). Mortalities of sea otters in the Commander nocturnal activities were similar in nature to diurnal ac-
46 BIOLOGICAL REPORT 90 (14)

Prince
William
Sound

Gulf of
Alaska

t-20km--l

Fig. 26. Prince William Sound, Alaska, indicating areas referred to in text.

tivities and that foraging occurred throughout the night. spent foraging by as much as 15-20%. Most of this
Subsequent information collected by Ribic (1982b) and difference is accounted for when the activity-specific
Ralls and Siniff (1988 *)-also using radiotelemetry- probabilities of sighting (Estes and Jameson 1988) are
confirmed that nocturnal feeding occurred. Observations used to correct scan sampling estimates of the percentage
made by Shrmek. and Monk ( 1977), Benech ( 1981 *), of time spent foraging.
Ribic ( 1982b), and Payne and Jameson ( 1984) suggested Throughout a 24-h period, California sea otters seem to
that a third peak in foraging activity may take place be active about half of the time. Loughlin (1977) found ·
between 2300 and 0200 h. In the central and southern that individual telemetered otters in the Monterey area
portions of the range, information on radio-instrumented spent an average of 34% of their time foraging, 54%
otters collected by Ralls and Siniff (1988 *) indicates that resting, and 12% engaged in other activities. These esti-
another peak in foraging activity occurs between mid- mates were generally similar to those obtained from a
night and dawn among· all age or sex classes except larger sample and more extensive study in the central and
juvenile females. southern part of the sea otter's range (Ralls and Siniff
Observations of sea otters (using visual scan samples) 1988 *). Loughlin found that about 45% of feeding activ-
along the California coast from Point Piedras Blancas to ity took place at night, although there was substantial
Santa Cruz show that the average amount of time allo- individual variation in the proportion of nocturnal forag-
cated to various activities during daylight hours falls ing (22-73%). Juvenile otters tended to engage in more
within the following ranges: foraging, 21-28%; resting, nonfeeding activities (e.g., playful interaction) than
51-63%; grooming, 5-16%; swimming, 2-9%; and inter- adults (Loughlin 1977, 1979).
acting, 0-8% (King 1976; Harris 1977; Shimek and Monk An extensive study of activity in telemetered sea otters
1977; Yellin et a!. 1977*; Estes et al. 1986). Telemetry was completed recently by Ralls and Siniff ( 1988\ They
data obtained by Ralls and Siniff (1988 ), however, found that, except for juvenile females, there is a general
strongly suggest that scan sampling underestimates time increase in feeding activity early and late in the day, as
 THE SEA 0TIER: BEHAVIOR. ECOLOGY. AND NATURAL HISTORY 47

reported by Shimek and Monk (1977) and Estes et al. for resting (Miller 197 4; Shimek and Monk 1977; Ried-
(1986) on the basis of scan sampling. Ralls and Siniff man 1984a*. 1984b*; Estes et al. 1986). Preliminary obser-
(1988 *) also reported a third peak in foraging between vations in California suggest that inclement weather and s~a
midnight and dawn. Juvenile females, in contrast, tended conditions (in the form of high winds, choppy seas, and
to feed more during midday and to rest more at night. heavy rain) may promote an increase in activity, inhibit
Ralls and Siniff ( 1988 *) found that all age or sex classes the formation of resting groups in habitual rafting spots.
except juvenile females spent 36-37% of the time feed- and disrupt resting otters (Sandegren et al. 1973; Estes et
ing; juvenile females spent 48% of the time feeding. a!. 1986; Riedman, unpublished data). During windy or
Although these results indicate that juvenile females rainy conditions in Alaska, otters are more active, and raft
spend more time feeding than the others, individual vari- size diminishes significantly (Garshe1is 1983).
ation within all age and sex classes was large, and analy- Diurnal peaks in foraging and resting activity have been
ses have not been done to determine if there are statisti- attributed to several factors. including food availability.
cally significant differences among age or sex classes. energy conservation, and the disruptive influence of wind
Each major activity (foraging, resting, grooming) takes or inclement weather. Estes et al. ( 1982) argued that
place over a relatively long time. According to Loughlin crepuscular peaks in foraging by sea otters at Amchitka
( 1977), the average duration of a foraging bout was 2.5 h, Island were related to their piscivorous behavior and the
and at least three foraging bouts occurred within a 24-h likely situation that fish are more available or vulnerable
period on the Monterey peninsula. In the San Simeon to predation near dawn and dusk. This conclusion was
area, Ribic (1982b) showed that, on average, an otter was based on ( 1) the finding that in 584 foraging dives ob-
active three or four times a day (each activity period lasting served by Estes et a!. ( 1982), all 60 fish that were seen to
about 3 h), followed by an inactive period of about 4 h. be eaten were captured during the crepuscular foraging
A considerable amount of individual variation in 24-h peaks, and (2) the conclusion by Munz and McFarland
activity rhythms and the amount of time allocated to ( 1973) that fishes are highly vulnerable to their predators
foraging and resting appears to exist. Activity patterns near dawn and dusk because of visual impairment asso-
may vary with the sex, age, and reproductive status ciated with shifts between photopic and scotopic vision.
(whether or not a female has a pup) of an otter, as well as This conclusion was further supported by the fact that
its location in both California (Loughlin 1977, 1979; crepuscular foraging peaks were not observed at Attu
Ribic 1982b; Ralls and Siniff 1988*) and Alaska (Gar- Island or in Oregon waters, where fish were not eaten by
shelis 1983). In the central and southern parts of the range otters. Garshelis et a!. ( 1986) also reported that activity
in California, a greater degree of synchrony exists among peaks varied among different parts of Prince William
resting otters, while individuals seem to vary the times Sound in relation to differences in prey availability. At
and lengths of their foraging bouts from day to day. In the Green Island, where the otters fed mainly on mussels and
northern part of the range, females with older pups seem infaunal bivalves, foraging activity peaked in day-light,
to spend as many or more daylight hours feeding than whereas in northeastern Prince William Sound, where the
other animals, while females with very young pups may otters fed extensively on the nocturnally active Dunge-
spend less time feeding during the day than other otters ness crabs, foraging activity peaked at night.
(Sandegren et al. 1973; K. J. Lyons personal communica- Estes et a!. ( 1986) suggested that the typically elevated
tion; Riedman, Staedler, and Estes, unpublished data). In afternoon peak in foraging that occurred in central Cali-
Prince William Sound, females with pups spend more fornia was related to di urn a I patterns in wind intensity that
time feeding than independent adults, probably because occurred there; they also suggested that foraging peaks in
they must obtain additional food for their pups (differ- California might be related to changes in food availabil-
ences in a mother's activity patterns in relation to the age ity. Garshelis ( 1983) also reported that wind and inclem-
of her pup were not discussed). Recently weaned pups in ent weather disrupted resting otters, which became more
Prince William Sound also spend more time feeding than active and tended to spend more time foraging. Ralls and
solitary adults or older juveniles, apparently because they Siniff ( 1988 *) suggested that the tendency of sea otters to
are less adept at obtaining prey (Garshelis 1983). rest at midday. when the intensity of solar radiation is
Several aspects of activity cycles and time budgets may greatest, should minimize heat production needed for
be influenced by such environmental variables as daily thermoregulation and thus represents an energy conser-
fluctuations in prey availability, geographical location, vation strategy. Ralls and Siniff ( 1988 *) contended that
time of year, weather, and sea conditions in California and the tendency for juvenile females to rest at night and feed
Alaska. Within a given stretch of coastline in California, during the day was consistent with this explanation. They
specific segments (of perhaps l-2 km) are characterized believed that juvenile females were at a competitive dis-
by variation in the amount of utilization by otters for advantage with adults for food, making it necessary to
different activities. Foraging is most common in some feed when the adults were resting.
areas. for instance, while other areas are used primarily The activity patterns of groups of otters in Alaska and
48 B IOLOGJCAL REPORT 90 (14)

the individual activity patterns of California otters may Point Piedras Blancas to Santa Cruz) were characterized
also vary with respect to location of the otters. In Morro by a high degree of similarity with respect to general
Bay, the 24-h activity pattern of males (N = 4) was geographic region and time of year. Data presented by
bimodal, with one main feeding time in earl)' morning and Estes et al. (1986) indicate no relation between the per-
one in late afternoon (Ralls and Siniff 1988 ·).San Simeon cent of time allocated to foraging and the length of time
females (N = 7) seemed to feed primarily in the morning, a particular area had been occupied by sea otters. How-
with no distinct peaks throughout the day and night (Ribic ever, variation in the amount of food resources between
1982b). Females in the Big Sur area (N = 12) had foraging male areas (in the newly occupied range peripheries) and
peaks in midmorning, evening, and after midnight (Ralls female areas (in the center of the range) may not be as
et al. 1985 *). In Alaska, Garshehs . (1983) found that pronounced as the variation in food resources between
general activity patterns differed in two locations: Nelson newly occupied male areas and long-established female
Bay, an area recently occupied by male sea otters, and areas in Alaska.
Green Island, an area otters had inhabited for over 25
years, which was occupied primarily by females and
seasonally breeding males. Sea otters in one area of Social Organization and Behavior
Nelson Bay rested during the day and foraged at night,
while Green Island otters rested at night and fed during
the day. At Green Island, males and females had similar Social Structure and Behavior
average activity patterns, although females with older
pups spent significantly more time feeding. The extensive California sea otters generally rest singly or in small
nocturnal foraging in one area of Nelson Bay seemed to groups (called rafts) of two or more individuals, although
be related to the fact that Nelson Bay otters fed heavily larger rafts of twenty or more animals are not uncommon,
on Dungeness crabs, which are nocturnal. In another area especially among males (Miller 1974, 1980; Jameson,
of Nelson Bay where otters fed primarily on clams, the unpublished data). For instance, large groups of 40-50
activity cycle was crepuscular. The activity pattern of otters were observed off Soberanes Point and offshore of
males that traveled between each area shifted to corre- Point Joe in the northern part of the range in the mid-
spond to the general activity cycle characteristic of a I 980's (Riedman, unpublished data). In a survey of six
particular area (e.g., diurnal versus nocturnal feeding). sites within the sea otter's range in California (excluding
Male otters in Nelson Bay allocated 23% less of their male groups at the range ends), groups of up to 12 were
time to foraging but obtained an estimated 38% more sighted (Estes and Jameson I988). The frequency distri-
calories per day than otters at Green Island, where food butions of group size varied substantially among activity
resources were apparently less abundant. In one male area categories. Ninety-eight percent of foraging otters were
in Nelson Bay, large Dungeness crabs provided 70% of alone (or with only their pups); the few other feeders were
the caloric intake of some otters, yet were captured on in groups of two. About 20% of those resting.were alone;
only 9% of the foraging dives. others were nearly evenly distributed among groups num-
In Prince William Sound, seasonal changes in activity bering 2 to I 2. About 70% of all "other" otters (i.e., those
were most pronounced in the female area at Green Island classified as swimming, interacting, or grooming) were
and seem to be related to changes in weather and length alone, with the rest occurring in twos or threes.
of daylight. The spring crepuscular activity peaks were In Alaska, females also generally rest in small rafts,
displaced towards midday during the fall period of dimin- although males frequently rest in very large groups (Fig. 26).
ishing daylight, and eventually merged into an extended In Prince William Sound, the average maximum group size
diurnal activity period during winter. Stormy weather for females was about five animals in spring and two animals
conditions in fall and winter-besides causing an increase in fall (Garshelis et al. I984). In contrast, Kenyon (I 969)
in activity-often caused otters to haul out and rest on and Garshelis et al. (I 984) observed male groups of up to
land. Rest periods in autumn and winter occurred noctur- 440 and 330 otters, respectively. Estes ( 1980) reported that
nally in female areas, since solitary females generally K. B. Schneider observed a resting congregation of about
hauled out when it was dark. In some male areas, the 2,000 animals in an area devoid of kelp beds in Bristol Bay.
diurnal rest period was maintained throughout winter, At times, females with pups seem to form "nursery groups,"
which seemed to be related to the tendency of males to in which most of the otters consist of resting mothers and pups
haul out together in large numbers during daylight. In one in California (Riedman, Staedler, and Estes, unpublished
area, periods of rest and hauling out were synchronized data) and in Alaska (Ralls eta!. 1985\ In Prince William
with winter tidal conditions, since otters usually hauled Sound, Ralls et a!. ( 1985 *) observed one large group of
out on mudbars exposed by low tide (Garshelis 1983). I50 females in May, of which nearly two-thirds had pups.
Estes et al. ( 1986) reported that diurnal activity time Although otters commonly rest in tightly to loosely
budgets throughout much of the California range (from structured groups, foraging activity generally takes place
 THE SEA OTTER: BEHA vroR. EcoLoGY. AND NATURAL HISTORY 49

Fig. 27. Large aggregations of sea otters:

(A) Western Bristol Bay (K. B.
Schneider); (B) Prince William Sound
(C. Monnett).

individually. often away from resting areas. Parturition and (Sancfegren eta!. I 973; Jameson, personal communication).
mating also tend to occur away from others. Mothers with Sometimes territorial males tend to rest a short distance from
newborn pups are frequently solitary and may rest apart the main female raft, while at other times they rest within
from other animals for a short rime following parturition the raft (C. Deutsch, unpublished data; Riedman, Staedler,
 50 BIOLOGICAL REPORT 90 (14)

and Estes, unpublished data). In California, large white- are entering, leaving, or simply swimming past a raft, an
headed males often seem to rest apart from male groups individual, or a mother and pup pair typically approach
(Bolin 1938; Siniff and Ralls, unpublished data) and in and make contact (usually nosing the other otter) with
Prince William Sound (Garshelis et al. 1984 ). some or all of the otters within the group. Often the
Many otters prefer particular rafting sites, and some interacting otter performs a ritualized head movement
return frequently to specific foraging areas as well termed the ''head jerk" by Loughlin ( 1977). The head jerk
(Loughlin 1977). Several individual males have been involves a rapid, repeated lateral jerking of the head from
observed habitually resting in the same kelp bed in their midline to the side, as the otter nuzzles the recipient's
respective territories over a period of years in California head, chest, abdomen, or anogenital area. An adult male
(Jameson 1989) and in Prince William Sound, Alaska approaching a female will often direct the nuzzling at her
(Garshelis et al. 1984 ). It is not known if otters recognize genital area. possibly to determine if she is in estrus. A
and preferentially associate or rest with the same individ- resting otter that is approached and contacted frequently
uals over time, although this aspect of social behavior is remains relatively passive but may become alert, sniff the
currently under investigation in the northern range of other otter, or briefly roll and rock in the kelp. Less
California (Riedman, Staedler, and Estes, unpublished common reactions on the part of the disturbed animal
data). In Prince William Sound, large male groups are include tail block of the anogenital area and lunging and
characterized by a high degree of fluidity, with single snapping at the intruder (Riedman, Staedler, and Estes,
otters or small groups often breaking off from one raft and unpublished data).
joining another or forming a new raft. Interactions in male Loughlin ( 1977) suggested that the head jerk behavior
groups in California and Alaska include frequent mock (or any type of relatively brief investigatory interaction)
fights and mock copulations (e.g., Garshelis et al. 1984). probably serves to communicate a variety of information.
Occasionally, apparently altruistic behavior among otters In this respect. an interacting or head-jerking otter might
in Prince William Sound and California has been ob- "greet" others. convey information about social status or
served during capture operations. Otters may accumulate intent, identify individuals, or determine sex and repro-
around the netted animals, vocalizing, exhibiting distress, ductive status. The nature of head-jerking interactions
and sometimes attempting to free the captive otters, and other nonvocal forms of communication involving
which increases the risk of being caught themselves (Gar- scent or behavioral cues are not well understood. Investi-
shelis et al. 1984; J. A. Ames, C. Deutsch, and M. Ried- gations focusing on nonvocal communicatory interac-
man, unpublished data). In California, mothers whose tions among individually identifiable otters are currently
pups have been captured always remain near the boat and in progress in the Monterey area (Riedman et al. 1988 *).
repeatedly vocalize. One mother actually climbed into a Sea otters are generally not considered to be very vocal
skiff to retrieve her pup as researchers were tagging it animals. but many of the adult vocalizations are soft and
(Riedman and Ames, unpublished data). low in volume and therefore difficult to hear in the field.
Packard and Ribic ( 1982) compiled an ethogram for sea The loudest and most frequently heard vocalizations are
otters, classifying the behavior of otters observed in Cal- produced by dependent pups. Pups often emit a high-
ifornia and Alaska into 43 discrete action patterns. Each pitched squealing call (sounding similar to the cry of a sea
action pattern was associated with a number of broad gull) when separated from their mothers. For instance,
functional activity categories, including resting, feeding, while the mother is underwater foraging or surfaces a
grooming, locomotion, and interactions. Some of the distance away from the pup, the pup may vocalize
behavioral patterns occurred in the context of several repeatedly until making contact with its mother again.
activities. They concluded that, while the general activity Mothers also vocalize quite loudly in response to the
categories of feeding and resting were distinctive enough pup's cries but less frequently than pups do. There seems
to allow reliable identification by observers, the catego- to be considerable individual variation in the acoustic
ries of grooming, locomotion, and interaction showed characteristics of the vocalizations of individually iden-
considerably more overlap. Table 5 summarizes and tifiable mother and pup pairs (Staedler, Riedman, Mc-
briefly defines the various action patterns occurring Shane, and Williams, unpublished data). Individually dis-
within each general activity category as presented by tinctive vocalizations would facilitate recognition and
Packard and Ribic ( 1982). help maintain contact between a female and her pup.
Qualitative descriptions of sea otter vocalizations are
provided by Fisher ( 1939), Kenyon ( 1969), and San-
Communication and Vocalization degren et al. ( 1973 ). Kenyon ( 1969) described eight types
of vocalizations: baby cry. scream, whistle or whine. coo.
The common and investigatory nosing between otters grunt, snarl or growl, hiss. and bark. The baby cry, which
probably involves some form of scent recognition or other is produced by dependent pups. has been previously de-
chemoreceptive means of communication. Sea otters that scribed. A scream is emitted by a mother separated from

\.
lbas
 THE SEA OTTER: BEHAVIOR, EcoLOGY, AND NATURAL HISTORY 5I

Table 5. Sea Otter (Enhydra lutris) hehavioral action patterns occurring within general activity categories (from
Packard and Rihic 1982).
Behavior General description Behavior General description
Locomotion at a short distance not in line with previous
direction of movement
Diving From a belly-down position, the otter sub-
merges head then feet (this dive usually used Grooming and Resting
while feeding)
Low intensity: arching of the back is minimal Dunking While floating on the back, the otter briefly dips
High intensity: otter leaps out of water with the head in and out of the water; the chin is
arched torso clearly visible pushed forward, and the back of the head
moves dorsally
Folding dive From a belly-up position, the rear feet and
shoulders move toward the center of the body Floating Otter floats on the surface, belly up, rear feet up,
and the otter sinks backward into the water no sculling, feeding, or grooming movements
Low intensity: body motionless
Porpoising As the otter swims just below the surface, the High intensity: slight movement of paws, head,
arched back repeatedly appears on the sur- or feet
face; general movement is in the forward
direction (contrasted with a feeding dive) Hanging Belly down with both rear and head submerged;
Low intensity: back just breaks the water sur- the arched back remains visible at the surface
face but motionless for a few seconds as the otter
High intensity: the otter repeatedly leaps out of apparently grooms its belly
the water with back arched in an inverted U
Logrolling From a belly-up position, the otter rotates to the
Rowing Floating belly up, otter folds ventrally in a V side like a rolling log; differs from rocking in
shape then straightens; may be repeated; otter that feet and paws are submerged
does not submerge
Looking Belly up or on its side, the otter turns its head
Sculling Belly up, the otter moves along the surface in various directions
propelled by movement of the tail and (or) Low intensity: slow, occasional head turns
feet High intensity: rapid agitated movements of
head from side to side
Sidestroking The otter moves along the surface on its side;
one foot may be waved above surface and Nibbling or Mouth contact is made with some part of the
head may be oriented toward an object licking otter's own body, in a nibbling or licking
movement; commonly directed toward paws,
Swimming Belly down; the head and back are visible mov- belly, feet, tail
c,·,~ 7"" ing along the surface
Rocking From a belly-up position, the otter does a side
Underwater Body is totally submerged; the otter reappears roll with torso arched such that the feet and
swimming at a distance at a location in line with previous paws remain out of the water
direction of movement Low intensity: otterrocks 180° from side to side
High intensity: otter rolls 360°
Feeding
Rubbing Rear feet rub some area of otter's own body
Eating While floating on the back, the forepaws are Low intensity: both rear feet are rubbed slowly
brought repeatedly to the mouth; object may against each other in a "hand-washing"
be shoved into the mouth or pieces bitten off movement
High intensity: rapid scratching movement of
Periscoping Only the shoulders and head are visible above
one foot directed toward back, neck, or side
the water as the otter takes a few seconds to
of body
look around; usually precedes a high-inten-
sity dive Shaking The head is rotated rapidly from side to side in
a typical shaking movement; water flies; the
Pounding Rapid pounding movements are made onto the
muzzle may be outstretched
chest with or witho~t an object held between
the forepaws; a hard object may be balanced Somersaul ring Full 360° forward roll with the head tucked
on the chest as the otter floats on its back; close to the belly; often only the curved back
observer can often hear pounding is visible until the head reappears at the end
of the roll
Submerging Body is totally submerged; the otter reappears
52 BIOLOGICAL REPORT 90 (14)

Table 5. Continued
Behavior General description Behavior General description
Stroking Front paws repeatedly stroke some area of the Lunging Sudden forward body movement toward an-
otter's own body; may vary in intensity (ra- other otter
pidity of strokes); commonly directed toward Low intensitv: no contact
chest, head, rear feet, belly, tail. flank, back High intensity: lunge and nip, mouth contact

Tuckrolling Head is brought toward chest but bent over to Mutual Porpoising as described under Locomotion.
side while otter does a 360° side roll; inter- porpoising synchronously or in close sequence with a
mediate between a somersault and a logroll partner moving in same direction

Interaction Nosing Muzzle contact made with another otter: diffi-

cult to distinguish between nibbling and
Begging Otter remains near the side or head of a feeding sniffing as the two movements are often inter-
otter; head is oriented toward the feeding mixed
otter; paws may or may not make contact
Pawing With one forepaw, the otter reaches out to con-
Biting Otter closes jaw briefly on body of opponent; tact its partner: may be a shoving or patting
more intense and not as prolonged as grasp- movement
ing; may be repeated
Riding The otter places its body on the belly of another
Chasing Rapid swimming with one otter behind another otter by swimming up slowly or by rolling
sideways onto its partner: the other otter may
Chinning The otter swims slowly toward another and
move away or remain stationary
places chin on chest, belly, or near the head
Low intensity: front half of body covers head
of the other otter
and front half of partner's body
Clasping Female uses front arms to hold pup to her chest; High intensity: full body contact
the pup is usually clasped around the chest,
Shoving Otter forcefully pushes another otter away with
neck or head, and becomes limp
forepaws
Gaping Otter holds the mouth open, usually oriented
Splashing Belly up, otter moves partly submerged front
toward partner's head
paws away from body towards another ani-
Low intensity: brief duration, quality of a threat;
mal. making water splash
may lunge without making contact
High intensity: prolonged interaction, each otter Suckling Pup has mouth in area of female's nipples
parrying lunges made by the other Low intensity: suckling interrupted
High intensity: continuous contact with nipples
Giving Holding food or another object, otter moves
paws toward another otter; the object is relin- Tumbling Two otters roll over and over each other; the
quished when the other otter takes it arched backs are usually visible, with an oc-
casional glimpse of feet, tails, or heads. The
Grabbing Jaws are closed on the body of another otter,
body contact is highly variable: sometimes it
maintaining prolonged contact
appears they are wrestling, at other times
Female grabs pup by neck
making jaw contact
Male grabs female by nose
Wrestling In a vertical position, two otters actively grasp
Interfering Otter attempts to move body between two other
each other with forearms around the head and
interacting otters
shoulders, then twist to break the hold

her pup or by an adult in extreme distress. Whistling or California sea otters, recorded by California Department
whining sounds seem to be produced when the otter is of Fish and Game biologists while the animals were being
mildly distressed or frustrated. For instance, older pups temporarily held together in an outdoor pen, frequently
may whine when not allowed to suckle from their mothers emitted extremely loud and unusual whines and high-
(Riedman, personal observation). In another case, an pitched whistles, sounding somewhat like the abovewater
adult male was heard to whine when he could not reach whistling produced by dolphins.
an estrous female who was hatlled out on an offshore rock Adults appear to make cooing sounds when "satisfied
(Deutsch, personal communication). A group of 10 male or content," according to Kenyon (1969), although these
 THE SEA 0TIER: BEHAVIOR. ECOLOGY, AND NATURAL HISTORY 53

sounds could also be used in other situations. Cooing Sex and Age Composition in California
appears to be generated in the throat, and the mouth is
generally closed when the sounds are emitted. Cooing is Sex and age composition of the California popula-
heard among pair-bonded adults, as well as females tion varies throughout the range in relation to general
grooming their pups. Kenyon (1969) also noted that geographic location and time of year. The center of the
females may coo "while eating food that is particularly range between Cayucos and Monterey is occupied pri-
pleasing." Soft grunting sounds also seem to convey marily by females (all ages) and pups as well as territorial
satisfaction, according to Kenyon (1969), and may be adult males (that move into female areas in summer and
produced when the otter is eating. Kenyon believed fall) and recently weaned juvenile males, some of which
that grunting in the male is equivalent to cooing in the remain in female areas until they are 2-3 years old. The
female. Growling or snarling sounds may be produced southern and northern peripheries of the range (south of
when a wild otter has been captured. Adults and depen- Cayucos and north of Monterey) are inhabited mainly by
dent pups may hiss at humans when frightened after being nonreproductive, immature males throughout the year,
captured. Barking is an uncommon vocalization. Kenyon and adult males that move out df the center of the range
(1969) heard a captive yearling male produce a high- during the winter-spring non~reeding season (Benech
pitched bark that trailed off into a whistle in apparent 1981; Estes and Jameson 1983a ; Jameson 1989). In some
frustration when trapped in an empty pool. A study of the male groups at the southern end of the range in winter and
acoustic repertoire of wild California sea otters is in spring, Jameson ( 1989) resighted 76% of the adult males
progress (Staedler, Riedman, McShane, and Williams, that had occupied breeding areas near Point Piedras Blan-
unpublished data). cas during the summer-fall period.
Solitary adult males-at least those from the Piedras
Blancas area-return to the center of the range in spring
Sexual Segregation and remain there throughout the summer and fall
breeding season, when pup density is low and the number
Sea otters exhibit a high degree of sexual segregation of estrous females is presumably high (Benech 1981 *;
in California and in Alaska, which varies seasonally to Estes and Jameson 1983a* ; Jameson 1989). Seasonal
some extent. Females and males generally rest in separate fluctuations in the sizes of peripheral male groups
areas (often called female and male areas), with the reflect these movements (Benech 1979 * , 1981 * ; Estes,
exception of solitary, adult males that maintain territo- unpublished data). Peak male densities occur in female
ries within female areas in California (Peterson and areas during late summer to early fall, when ratios of
Odemar 1969; Wild and Ames 1974; Loughlin 1977, one male per six independent otters are found. Al-
1979; Jameson, unpublished data) and in Alaska though the breeding season peaks from July to October
(Lensink 1962; Kenyon 1969; Schneider 1978 *; Gar- in the Piedras Blancas area, adult males may be found
shelis et al. 1984). in the center of the range from April to December. Along
In Alaska, male groups are usually situated in areas with the northern Monterey peninsula, adult males occupy
more abundant food resources but that are less protected territories in female areas throughout the year (Loughlin
from stormy weather than female areas (Schneider 1978 *; 1977, 1980; Deutsch, unpublished data; Riedman,
Garshelis et al. 1984). In California, differences in the Staedler, and Estes, unpublished data; Lyons, personal
degree of exposure to rough sea conditions and avail- communication).
ability of food resources characterizing established male While sexual segregation is well defined, distinct fe-
and female areas are less pronounced than they are in male and male areas both locally and throughout major
Alaska. However, groups of juvenile males may occur portions of the range are not absolute. A nonterritorial
well offshore in exposed areas in California (Ralls et al. male, for instance, may enter a female raft and interact
1988a \ In California (Peterson and Odemar 1969; Wild with all females present (Loughlin 1977; Benech 1981 * ).
and Ames 1974; Benech 1981 *; Estes and Jameson Jameson (1989) found that some juvenile and subadult
1983a*) and in Alaska (Garshelis et al. 1984), male males may occupy female areas in the center of the range
otters are the first animals to colonize unoccupied habitat; throughout the year, although they do not usually associ-
therefore, male areas generally occur at the edges of the ate with adult females. Correspondingly, a few adult
range where expansion is taking place. The longest dis- females may be found at either end of the range. Groups
tance between male areas is about 150 km in Prince containing females and pups are located between Point
William Sound and about 120 km in California-where Buchon and Point San Luis to the south (Benech 1981 * )
the populations are expanding-and 15 km or less at and near Santa Cruz and Sandhill Bluff to the north
Amchitka Island-where the population is at equilibrium (Bonnell et al. 1983 *; Estes and Riedman, unpublished
density. data; Ames and Hardy, personal communication). Locally
54 BIOLOGICAL REPORT 90 (14)

established distinct male and female rafting sites may be Home Range and Movements
separated by a minimum distance of 1-4 km or more, as
they were in the late 1970's near Monterey (Loughlin California
1977) and Point Buchon (Benech 1981 "'). Home range has been defined as the area traveled by an
animal during its routine activities (Jewell 1966). How-
ever, when considering home range and movements of
Sex and Age Composition in Alaska sea otters, it is important to note that the dimensions of
the home range may vary in space and time-that is, the
Spatial segregation of the sexes also occurs throughout home range sizes recorded in various studies can change
the range in Alaska. At Amchitka Island, at least four (and according to the duration of the study and time of year.
probably seven) geographically distinct male areas exist The importance of this point was emphasized by studies
throughout the year (Estes, unpublished data). In the in Alaska (Garshelis and Garshelis 1984; Monnett and
female areas, an estimated 95% of the animals caught in Ratterman 1988a *) and California (Ralls et al. l988a *),
nets were females, while about 98% of the otters caught both of which showed that sea otter home ranges con-
in male areas were males (Kenyon 1969). Sexual segre- sisted of several heavily used areas connected by travel
gation also occurs in the U.S.S.R.'s Commander Islands corridors. In addition, sizes of home range and distance
(Marakov 1965). of movements depend on the portion of the range in which
Garshelis (1983) and Garshelis et a!. (1984) investi- the animals were marked and subsequently observed. For
gated social organization of sea otters in Prince William example, distances of yearly movements by adult males
Sound and found that predominantly male areas were tagged in the center of the range would probably be longer
located at the front of the expanding population, while than those recorded for males tagged closer to the periph-
females inhabited areas that had been occupied for longer eral groups located near either end of t~e range. A general
periods. Animals captured in the male areas from May to pattern observed by Ralls et al. (1988a ) in California for
August indicated a sex ratio of 97% males. Censuses all age or sex classes was that individuals tended to
conducted in female areas (at Gibbon Anchorage on remain in one area for extended periods, with occasional
Green Island) varied seasonally from a high of33% males sudden long-distance movements. These movements oc-
during the breeding season in July and August to <1% curred at all times of the year.
males in January and February. Males. The size of an adult male sea otter's home range
Unoccupied habitat in Prince William Sound was seems to vary seasonally in California. Most of the time
initially colonized by large, solitary, and usually white- males remain in the same area; however, Ralls et a!.
headed males. After months or even years, groups of ( 1988a*) found that both territorial and nonterritorial
younger males suddenly began to occupy the new males occasionally make long-distance trips throughout
areas. Garshelis et al. (1984) believed that older males the year. Short-period (18-36 h) movements of radio-
routinely explored new potential breeding territories, tagged otters in the central and southern parts of the range
often returning to established areas. The newly occu- averaged about 1 km for adult males and 2.3 km for
pied areas were therefore eventually occupied by large juvenile males, and although the longest movement dur-
groups of males, followed by females and pups after a ing this time was 47.5 km by an adult male, movements
period of years. Subsequent initial occupation of male of> 10 km were rare (Ralls et a!. 1988a* ). The area used
areas by females may proceed slowly due to harass- by an individual in one day ranged from 10 ha to more
ment of the few females by males in the form of food than 1,000 ha. In the summer-fall period, which encom-
stealing and sexual interactions (Garshelis et al. 1984). passes the breeding season in California, resident adult
As the proportion of sexually available females within male sea otters (territorial and nonterritorial) have smaller
the male areas gradmilly expands, the establishment of home ranges than resident adult females (Loughlin 1977,
territories by dominant males, along with diminishing 1980; Ribic 1982a; Jameson 1983a, 1989). The most
food resources, may collectively encourage most males comprehensive long-term study of male home range and
to abandon the area and move into adjacent unoccupied movements was conducted by Jameson ( 1989), who vis-
habitat again (Garshelis eta!. 1984 ). ually monitored home range sizes and movements of 19
According to Garshelis et al. (1984), it is to the female's males tagged near Point Piedras Blanc as over 6 years. He
advantage to limit her movements and remain in a found that territorial adult males occupied a mean home
sheltered area to raise her pup. Conversely, males not range of 40.3 ha (N = 10; SE = 3.97) in the summer-fall
constrained by the burden of parental care are able to period (at which time home range was considered equiv-
travel long distances to locate new habitat with abundant alent to territory size), with a mean coastline length of
food resources but that is often highly exposed to rough 1.1 km (N = 13; SE =0.44). The winter-spring ( 1 Decem-
seas. ber to 30 May) mean home range size of territorial adult
 THE SEA OTTER: BEHAVIOR. ECOLOGY. AND NATURAL HISTORY 55

males that remained in female areas was larger at 78.0 ha occasionally made long-distance trips. The nonterritorial
(N = 5; SE = 7.24), with a mean coastline length of males in Morro Bay remained with the male group in this
2.16 km (SE = 0.21). area most of the time, although they periodically moved
The annual home range and life range sizes of adult, a distance of roughly 40 km (to the San Simeon area) or
subadult, and juvenile males are substantially larger than about 10 km (to the Cayucos area where another male
those of adult and subadult females. The larger yearly group was located).
male home ranges apparently reflect the long-distance Five territorial males near Point Sur spent most of their
male movements of 60-100 krn or more to either end of time within a small area of less than a few kilometers.
the range that occur seasonally (U.S. Fish and Wildlife although two males made long-distance trips (>20 km)
Service 1980*; Estes and Jameson 1983a *; Jameson away from their territories. One otter traveled from Point
1983a; Jameson 1989). Jameson (1989) reported that Sur to Moss Landing (a distance of about 60 km); how-
80.1 krn (N = 13; SE = 4.17) was the mean seasonal ever, he was shot and found dead near the mouth of the
distance traveled south from female areas in the vicinity Salinas River. The other male, which maintained a terri-
of Point Piedras Blancas to peripheral male groups lo- tory near Pfeiffer Point, made one trip to an area just south
cated near Point San Luis, although possible movements of Grimes Point (8 km) and returned the following day.
of up to 150 km were recorded for one adult male. The His second trip was to the Santa Cruz area, where he
mean distance of 80.1 km was considered equivalent to remained for about two weeks before returning to his
life range, which was calculated as the number of kilome- territory. This 72 kilometers was the maximum distance
ters of coastline known to have been used within the entire traveled by a territorial male. Juvenile males tended to
study area (Jameson 1989). As mentioned previously, range farther from shore than did adult males.
however, the distance traveled seasonally by marked Females. Less information is available concerning fe-
males is dependent on the current population distribution male home range size and movement patterns, although
and the geographic location of the female area where each preliminary data indicate that compared to males, most
male was tagged and subsequently monitored. adult females are sedentary. Near San Simeon, females
Loughlin (1977, 1980) determined home range sizes may use an average of 18 km (N = 22) of coastline
along the Monterey peninsula, using radiotelemetry and throughout their life (Jameson, personal communication).
visual observations conducted at intervals throughout the As mentioned previously, females seem to have smaller
year. He found that territorial and non territorial males had annual or lifetime home ranges than males; however,
a mean home range size of 35 ha (N = 4, SE = 8.8) and 44 female home ranges are about 1.5-2 times larger than
ha (N = 7, SE = 13.4), respective! y, while the mean home those of resident adult males during the breeding season.
range size of adult females was substantially larger at 80 Ralls et al. (1988a *) found that adult females tended to
ha. A considerable amount of individual variation with make less extreme movements than males, and they trav-
respect to home range size was evident. eled average distances that were intermediate in length
Using radiotelemetry, Ribic (1982a) assessed home compared with those traveled by males, since males either
range sizes of sea otters near San Simeon in fall 1978 and remained within a limited area or made long-distance
1979. She categorized males as residents or nonresidents. movements. In California, 7 of 13 adult females, and 6 of 9
Her results indicated that the home range sizes of resident juvenile females moved maximum distances of>20 krn.
males averaged 460 ha (N = 5, SD = 0.8), while the Female otters are capable of traveling long distances,
average home range size of resident females was 680 ha however, and three tagged females in California are
(N = 4, SD = 2.3). The comparatively larger home range known to have moved between the southern and northern
sizes of resident adult males reported by Ribic seems due parts of the range. One adult female tagged near San
to differences in methods of calculating home range area Simeon traveled a distance of 110 krn north to Point
and in the timing of Ribic's study period (early fall to Lobos (Jameson, personal communication), and a young
early winter), both of which may have contributed to an female tagged near Cayucos moved a distance of ~160
overestimation of range. Both Ribic ( 1982a) and Jameson km to the northern Monterey peninsula (Riedman,
( 1989) concluded that adult male California sea otters use Staedler, and Estes, unpublished data). The third adult
two distinct home ranges (in the center of the range within female, who was originally tagged in Monterey, moved
female areas and at the end of the range within male to San Simeon and returned to Monterey, a round-trip
groups), connected by a migration corridor that can be distance of about 280 km. The female was last sighted in
traveled in a brief time. Monterey in May 1976 after losing her 2-month-old pup
Ralls et al. ( 1988a*) implanted
' radio transmitters in in April. She was observed about 1 year later near San
seven adult males and five juvenile males in central Simeon with a second pup of about l-3 months, which
California; four of these animals were associated with a seemed to have been weaned successfully. She was
male group in Morro Bay. All these males were relatively sighted about 7 months later in Monterey with a 1.5-
sedentary or moved only a short distance each day but month-old pup (Loughlin et al. 1981 ). Riedman et al.
56 BIOLOGICAL REPORT 90 (14)

(1988 *) found that three tagged adult females routinely a 5-km length of coastline for at least 2 years (Jameson.
traveled across Monterey Bay between Monterey and unpublished data). In Monterey. several tagged juvenile
Santa Cruz (a distance of 40-50 km, depending on the females remained in the vicinity of their natal area for at
route taken) for over 4 years. These females tended to least 3-4 years (Riedman, Staedler. and Estes, unpub-
spend several months in each area, and often returned to lished data). In fact, since the late 1970's, many adult
Monterey to give birth and raise their pups. Reasons are females weaned near Monterey still occupy the same area
unclear for long-distance travel by female sea otters in as their mothers, and some of these females have given
California, although Ralls et al. ( 1988a*) suggested that birth to their own pups. Some degree of matrilineal kin
both adult and juvenile females travel long distances in relationships therefore seems to exist in this area. Ried-
search of areas where they can become residents. Some man, Staedler, and Estes (unpublished data) observed
females may also move moderately long distances when several cases in which juvenile and adult offspring in the
weaning their pups (Riedman, Staedler, and Estes, unpub- Monterey area interacted with their mothers in some way.
lished data). Daily Movements. Localized, daily movement patterns
Dispersal of Juveniles. Dispersal and movement pat- vary in relation to territorial status of males and whether
terns of juvenile sea otters and newly weaned pups of both or not females have a pup. Most movements away from
sexes are currently under investigation in the southern habitual rafting sites are associated with foraging activity.
.
(Jameson, unpublished data), central (Ralls eta!. 1985 *), Females without pups and males typically leave their
and northern (Riedman, Staedler, and Estes, unpublished resting areas, feed individually, and subsequently return
data) ranges in California. Juvenile males seem to dis- to the resting areas. Territorial males generally forage
perse greater distances from their natal areas than juvenile within their territories or well offshore. Before territorial
females, although there are exceptions to this pattern. males return to their resting sites after feeding, they often
Juvenile males in the San Simeon area seem to leave the patrol the boundaries of their territories and travel to
natal area (which contains a high number of females and female rafting areas, where they may investigate each
pups) from about 6 months to 2.5 years after weaning to female in the raft (Loughlin 1977, 1980).
join male groups at either end of the range (Jameson. Many females with pups, however, do not always return
unpublished data). Most juvenile males in the Monterey to their previous resting sites after foraging, but instead
area leave the natal area immediately after weaning may continue to rest and feed, gradually returning to their
(Riedman, Staedler, and Estes, unpublished data). Jame- original resting sites within 12-48 h (Loughlin 1977,
son ( 1983b, and unpublished data) resighted two juvenile 1980; Jameson, unpublished data; Riedman, Staedler. and
males 64-80 km south of their natal area within 2 weeks Estes, unpublished data). Sandegren et al. (I 973) found
of weaning. At least 30% of the juvenile males tagged in that the location of resting groups of females with pups
the center of the range have been subsequently resighted changed daily. However, some females with pups in Mon-
in male groups (Jameson 1989). Seven juvenile males terey move short distances and rest in different sites from
moved an average distance of77 km (SE = 8.86) south of day to day, whereas others consistently rest and some-
the natal area near Piedras Blancas to male groups. An- times forage in the same areas, traveling very little CRied-
other juvenile male, which weighed 12.3 kg at the time of man, Staedler, and Estes, unpublished data).
capture, moved 187 km north from Piedras Blancas to join
a male group near Soquel Point near Santa Cruz. Nearly Alaska
2 years elapsed between sightings of this male at Piedras Movements and home range sizes of Alaskan sea otters
Blancas and Soquel Point. Subsequent observations sug- were first investigated in the Aleutian Islands by Lensink
gest that the male has remained in the Soquel Point area (1962) and Kenyon (1969), who tentatively concluded
(Jameson, personal communication). that a female's home range included 8-16 km of coastline
Ralls et al. ( 1985 *) reported that the only newly inde- and that males may have larger home ranges than females.
pendent juvenile implanted with a radio transmitter, a Lens ink ( 1962) reported that movements in the Aleutian
male, traveled more widely than any other adult sea otter Islands were related ttl season and weather conditions. In
monitored. The juvenile male was captured near Torre the Commander Islands of the Soviet Union, movements
Canyon in mid-March. One month later he traveled of otters were also related to weather, season, time of day,
slowly north, nearly to Yankee Point, after which he and human-caused disturbance (Barabash-Nikiforov
moved south to Pacific Valley. He then moved north again 1947; Barabash-Nikiforov et al. 1968). As in California,
to Moss Landing (about 120 km from Pacific Valley), and movement patterns and home range sizes of Alaskan
soon moved south again. At latest report, the young male otters reported in various studies probably depended on
had not moved into a predominantly male area. the location of the study area, time of year, and duration
In contrast, recently weaned females often tend to re- of the study.
main near the area in which they were born. In the San Males. Studies conducted by Garshelis (1983), Gar-
Simeon area, one newly weaned female remained along she lis and Garshelis (1984 ), and Ralls et al. (1985 * )
 THE SEA 0TIER: BEHAVIOR. EcoLOGY. AND ~ATURAL HisTORY 57

provided detailed information on movement patterns of females with large pups began moving into Gibbon An-
sea otters in Prince William Sound (Fig. 27). Comparable chorage in early fall, apparently because shallow-water
information is not available from other areas of Alaska. feeding areas in Gibbon Anchorage facilitated indepen-
Seasonal male movements seemed to vary in relation to dent foraging by pups. Before August, females with small
the time each study area was occupied by otters. In a new pups too young to forage successfully remained in deeper
area where food resources were relatively abundant, ter- water with more abundant or higher quality food. In fall
ritorial males were fairly sedentary and traveled only and winter, stormy weather also apparently caused inde-
.
short distances-generally <25 km (Ralls eta!. 1985 *). In pendent females and mothers with small pups to move
contrast, Garshelis et a!. ( 1984) recorded long-distance into protected areas such as Gibbon Anchorage (Garshelis
movements of >100 km for five adult territorial males and Garshelis 1984).
that left Gibbon Anchorage at Green Is.land, presumably Accordingly, the size of females' home ranges at Green
an area with reduced food resources that had been occu- Island appeared to vary as a function of reproductive
pied by otters for a long time. The males traveled to male status and age of pup (Garshelis and Garshelis 1984).
areas in northeastern Prince William Sound, where food Females without pups and those with pups 3 months old
was more abundant. These differences may simply occur had larger average home range sizes (x = 4.8 km; SE =
because newer habitats were closer to peripheral male 0.9; N = 7 and x = 4.5 km; SE = 1.8: N = 2, respectively)
groups than areas that were occupied longer. As in Cali- than females with pups older than 3 months (x = 1.0 km;
fornia, some males moved between male and female areas SE = 0.2; N = 6). Garshelis and Garshelis (1984) specu-
throughout the year. lated that the more sedentary behavior of females with
Males in northeastern Prince William Sound also large pups allowed the pups to become familiar with
moved to and from male areas relative to season, weather specific feeding areas. Such feeding areas were often
conditions, and boat traffic associated with commercial located within male territories, so that constant attempts
fisheries (Garshelis and Garshelis 1984). For instance, by the male to prevent the pair from leaving also may have
male groups were present in Orca Inlet only in winter. influenced the female's sedentary behavior. Independent
Throughout much of the remaining year, heavy boat traf- females and those with small pups were not restricted to
fic in Orca Inlet apparently disrupted the otters and caused shallow feeding areas. Garshelis and Garshelis (1984)
them to move. Males were also attracted to Orca Inlet believed that some females moved more extensively in
mudbars, where they frequently hauled out during stormy other areas, so that life ranges were larger than those
winter months. Unlike females, males often traveled in recorded in their study area.
groups between areas (Garshelis and Garshelis 1984). Through the use of radiotelemetry, .\1onnett and Rotter-
As in California, the home ranges of male otters in man (1988a *) found that adult female sea otters in Prince
Prince William Sound consisted of peripheral male areas William Sound moved distances of 30-80 km, traversing
and breeding territories within female areas, connected expanses of deep water and moving between major bays
by travel routes or migration corridors. Seasonal home and fjords. In contrast with central California, where adult
range sizes in male areas seem to vary in habitat charac- females tend to remain fairly sedentary (except for occa-
teristics. For example, Garshelis and Garshelis (1984) sional long-range movements), the adult females in
reported that males in Nelson Bay had significantly larger Prince William Sound undertake extensive seasonal
home ranges (x= ll.Okm; SE=0.7;N= 13) than Simpson movements. These females bear their pups and nurse
Bay males (x = 4.6 km; SE = 0.5; N = 4). They attributed them in the central part of the sound, wean their pups and
this to the fact that Nelson Bay is larger than Simpson copulate in the deep fjords of the north-central part of the
Bay, and provides more available habitat with greater sound, and then move far to the east to spend winter.
distances between feeding and resting areas. These complex patterns, compared with those docu-
Garshelis and Garshelis ( 1984) suggested that annual mented in central California by Ralls eta!. (1988a *), are
and lifetime home ranges of males may be larger than correlated with-and possibly caused by-differences in
those of females and may include most of Prince William habitat complexity between the two areas; Prince William
Sound. The seasonal and sexual variation in home range Sound may present a more variable large-scale mosaic of
size may be similar between Prince William Sound and habitats to sea otters, and the otters may benefit by mov-
California in that males have larger annual or lifetime ing among the mosaic patches to meet specific needs.
home ranges-but smaller seasonal home ranges (con- Dispersal of Juveniles. As in California, juvenile male
sisting of defensible territories)-than females. sea otters in Prince William Sound tend to disperse greater
Females. Female movement patterns in Prince William distances than juvenile females. Monnett and Ratterman
Sound seem to vary in relation to such interrelated factors ( 1988a*) found that juveniles tended to move away from
as duration of occupation (by otters), weather conditions, the natal area immediately after weaning, although, on
season, reproductive status, and age of pup. At Green average, males moved farther than females; the greatest
Island, where the population has been long established, distance traveled by a juvenile male from his natalloca-
58 BIOLOGICAL REPORT 90 (14)

tion in Prince William Sound was about 120 km; the birth. In central California and Prince William Sound.
greatest distance moved by a female was 38 km. Move- male areas tend to occur at the peripheries of the ranges.
ment patterns of recently weaned females were similar to This is also true of growing populations in the western
those of older independent females, although the average Aleutian Islands (Estes, unpublished data). These male
home range sizes of juvenile females Cx = 7.6 km; SE = groups are spatially labile, moving gradually outward as
1.6; N =3) were larger than those of solitary adult females adult females expand their range. The distance separating
(x = 4.8; SE = 0.9; N = 7; Garshelis and Garshelis 1984). male groups gradually becomes greater, requiring in-
Garshelis et al. ( 1984) found that male dispersal from creasingly longer distance dispersal by juvenile males
female areas often took place shortly after weaning; how- weaned near the center of the range. However, these
ever, some males may have delayed dispersal until2 years peripheral groups are juxtaposed with areas in which food
of age or made interim stops on the way to male areas. resources are comparatively abundant because they have
Despite its unfamiliarity with northeastern Prince Wil- not been heavily exploited by foraging sea otters. There-
liam Sound, one juvenile male born near Green Island fore, we conjecture that juvenile males experience higher
traveled 100 km to a male area. Newly independent males travel costs than do juvenile females; however, males also
may follow older males to distant male areas and remain benefit from foraging on more abundant food resources.
there at least until breeding age (Garshelis et al. 1984). Sex-specific differences in activity budgets and probabil-
Daily Movements. As in California, otters in Prince ities of survival seem to be related to these movement
William Sound and the Aleutian Islands use different patterns. Compared with juvenile males, females spend
areas for resting and feeding (Lensink 1962; Garshelis more time foraging and suffer hi*gher rates of mortality
and Garshelis 1984). Daily home ranges of males in (Monnett and Ratterman 1988b ; Ralls et al. 1988a ;
northeastern Prince William Sound were clustered within Siniff and Ralls 1988\
five separate bays or coves. Although males moved These patterns, implicitly assumed to be species char-
among these areas, they tended to remain in the same area acteristics, have been variously interpreted. Ralls et al.
on any given day (Garshelis and Garshelis 1984). Daily ( 1988a* ) suggested that sex-related differences between
home ranges offemales near Green Island were clustered juvenile males and females may serve to benefit male
within six areas delineated by distinct topographical reproductive opportunities and female feeding opportuni-
boundaries. Females accompanied by pups remained in ties-that is, the extensive movements of juvenile males
these areas longer than solitary females. Females moved may allow them to search for and assess available territo-
among areas somewhat more frequently than the males, ries, whereas the more limited movements of juvenile
probably because male areas were larger and separated by females may result in a detailed familiarity with food
greater distances than female areas. The movement of resources within the smaller, natal area. Monnett and
both sexes between areas tended to occur irregularly Ratterman ( 1988b *) speculated that these differences
. are
(Garshelis and Garshelis 1984). the consequence of higher parental investment in males
than females, as predicted by Trivers and Willard ( 1973).
Summary of Movement Patterns Garshelis et al. ( 1984) suggested that young males aggre-
In conclusion, information from studies of sea otters in gate in male areas because of social benefits derived from
Alaska and California suggested that complex relations gregariousness. Each of these explanations presumes sex-
exist between activity budgets, movement patterns, hab- related social benefits to the observed patterns, which
itat characteristics, and the probability of survival, and may be true. However, none of the explanations recog-
that these may differ fundamentally between juvenile nizes that (as we suggest) the patterns are derived from
male otters and juvenile female otters. Postweaning dis- adult male aggression, a fundamental outcome of the sea
persal tends to be greater in juvenile males than females. otter's polygynous mating system and not unlike the
Although the reason for this difference is not known, it juvenile dispersion patterns observed in numerous spe-
probably results from the sea otter's polygynous mating cies of polygynous mammals.
system and the fact that adult males maintain territories Limited data on sex-specific distribution and mortality
in most areas inhabited by adult females. Whether the patterns from Amchitka Island suggest to us that whereas
territorial males compete for food, females, or both is not behavioral processes related to the sea otter's polygynous
known, although it seems likely that males compete for mating system may be fundamental to all or most sea otter
access to mates. However, aggressive behavior by terri- populations, some of the behavioral and demographic
torial males seems to drive juvenile and subordinate consequences of these processes may vary, depending on
males away from the female areas. The result seems to be whether the population is at or near carrying capacity or
that juvenile males are forced into areas not inhabited by has access to unoccupied habitat into which it can grow.
territorial males, whereas juvenile females are not. These Unfortunately, we have no data on activity budgets or
juvenile males ultimately join male groups, whereas ju- movement patterns for different age or sex categories at
venile females tend to remain nearer the area of their Amchitka Island. However, results from Kenyon's ( 1969)
 THE SEA 0TIER: BEHAVIOR. EcoLOGY, AND NATURAL HISTORY 59

long-term studies at Amchitka indicate two intriguing dence of pup mortality would occur during winter, when
differences from the patterns reported from central Cali- small pups are most numerous and storm activity is great-
fornia and Prince William Sound. One difference is that est. Furthermore, females tend to come into estrus soon
male groups are interspersed within female areas (there after losing their pups (Riedman, Staedler, and Estes
are no range peripheries where they could form), and unpublished data); if females successfully mate shortly
these male areas tend to be separated by fairly short thereafter, they would give birth in early fall, after a
distances (11-19 km; Kenyon 1969; Estes, unpublished gestation of about 6 months (Wendell et a!. 1984 ).
data). All male areas that are presently known at Am- The proportion of females that lose their young pups
chitka Island occur near exposed points with extensive seems highest in winters with severe storms or prolonged
shallow habitat extending offshore. We presume that, inclement weather and sea conditions. The late summer
compared with central California and Prince William to early fall secondary pupping peak may therefore be
Sound, dispersing juvenile males are required to travel more pronounced during years when winter storms are
shorter average distances before encountering a male especially severe. For exampie, due to anomalies associ-
group, and these male groups are not juxtaposed with rich ated with the 1982-83 "El Nino .. event, winter 1983 was
food resources. The costs of male dispersal may therefore atypically severe in the high frequency and severity of
be less than they are in expanding populations, but juve- storms, large swells, and the resultant reduction in the
nile males derive no foraging benefits by occupying these kelp canopy from late January to April (Dayton and
areas. Indeed, male groups may be constrained to form in Tegner 1984). The number of pups counted throughout
habitats unsuitable for adult females. The second differ- the range in spring 1983 was low (9 .6% of the total
ence is that the juvenile mortality rate is higher in males population), compared with spring 1982 (16.5%) and
than females, based on Kenyon's (1969) analysis of 1985 ( 17.4% ), suggesting that pup loss was high in winter
beached carcasses. As Kenyon pointed out, this could be 1983 (California Department of Fish and Game and U.S.
due to biases in sex determination. However. a slightly Fish and Wildlife Service, unpublished data). In addition,
male-biased sex ratio persists even when all the indeter- there appeared to be a sudden and pronounced increase in
minate juveniles from Kenyon's sample are assumed to mating activity during April and May of 1983 in the
be females. Although more data from Amchitka Island Soberanes Point area, as would be expected if a high
are needed to substantiate these patterns, we expect to proportion of females lost their pups during the preceding
find fundamental sex-related differences in juvenile ac- winter (Riedman, unpublished data). In spring 1984, the
tivity, movement, and survival between sea otter popula- proportion of pups in the population was still low (9 .4% ),
tions that are still growing and those that are at or near indicating that the suggested shift in reproductive events
equilibrium. persisted for 2 years in the population.
Indirect evidence suggests that the mating season peaks
from July to October in the southern part of the range near
Reproduction San Simeon, although moderate densities of adult males
occur within female areas from April through December
there (Jameson 1989). In the Monterey area, the fre-
Seasonal Phases of Breeding quency of mating activity among territorial males gener-
ally appears to increase from September through Novem-
California ber (Deutsch, unpublished data; Riedman, Staedler, and
Although mating and pupping among sea otters take Estes, unpublished data). The general yearly reproductive
place throughout the year in California, a peak period of pattern in California therefore consists of a winter pup-
pupping tends to occur from January to March (Fisher ping season and summer-fall breeding season.
1940; Vandevere 1970* , 1972* , 1979* ; Sandegren et a!.
1973; Estes and Jameson 1983a; * SiniffandRalls 1988; * Alaska
Ames, unpublished data; Jameson, unpublished data). A Mating and pupping also occur throughout the year in
secondary but equally pronounced pupping peak appears Alaska. However, the breeding and pupping seasons peak
to occur in late summer to early fall (Siniff and Ralls about 2-3 months later in Alaska than in California. In
1988* ; Jameson, unpublished data; Riedman, Staedler, addition, reproductive events seem to be temporally syn-
and Estes, unpublished data; Vandevere, personal com- chronized to a greater degree in Alaska than in California.
munication). This second pup'ping peak may stem from The mating season in Prince William Sound peaks during
elevated pup mortality during the winter pupping peak. September and October (Garshelis eta!. 1984). In Prince
The rationale for this suggestion is as follows: Because William Sound, most pups are born in May; the peak of
the probability of mortality declines with increasing age weaning is about mid-November and, in contrast with
of the pup (Jameson, personal communication; Riedman, central California, few births occur in late fall and winter.
Staedler, and Estes, unpublished data), the greatest inci- There are no sex differences in the seasonal distributions
 THE SEA OTTER: BEH.A vro~<. EcoLOGY. "'D \/An RAL HrsTORY 61

they would not be ~exually r~ceptive. Possibly the fe- bling. and otherwise highly synchronous activity. During
males were experiencing an incomplete estrus cycle (one a typical copulation. the male clasps the female from
that would not result in pregnancy). such as that described behind and grasps her face or nose with his teeth, after
by Schneider ( l9n! in Alaska. :V1ales often engage in which the pair alternately rem and vigorously spins
nuzzling. biting. tumbling. and rough play with the fe- around their longitudinal axis ( 1\.~nvon 1969: Vandevere
male and her pup. Frequently during such interactions. 1969 . 1970\ Copulations comm;nly last 15-30 min.
pups seem to exhibit distress. \ ocalizing repeatedly and although duration is variable. In Prince William Sound.
trying to climb onto their mother or to pull her away from Garshelis et al. ( 1984) observed copulations lasting from
the male. Occasionally. pups seem to interact in a playful 15 s to 38 min. Kenyon reports that copulation may last
manner with the male. The mothers generally attempt to up to 35 min: in California. moq copulations have been
swim away from the attending male. As in Alaska. copu- reported to last 20-30 min. although briefer copulations
lations are occasionally attempted but are not successful have occurred (Estes. Staedler. and Riedman. unpublished
(Riedman. Staedler. and Estes. unpublished data: data Duetsch. personal communication: Jameson, per-
Deutsch, personal communication). sonal communication). There ar~ no reliable cues to en-
Copulation occurs exclusively in the water and is usu- able a field observer to determine rf and when ejaculation
ally initiated by the male. although females have been occurs. Interestingly. the briefer copulations frequently
observed to initiate copulatory activity on occasion (Ken- take place with young females (Garshelis et al. 1984).
yon 1969: Deutsch. personal communication). Coitus is A female's bloody nose indicat~s recent mating activity
preceded and followed by mutual nuzzling, pawing. tum- (Brosseau et al. 1975). and the resultant scars may aid in

Fig . .2S. Female California sea otter with distinctive nose scar ac4uired during mating activity (F. Bavendam 1.
 62 BIOLOGICAL REPORT 90 (14)

individual identification of adult females (Foott 1971; times, throughout the year (Loughlin 1977, 1980; Ried-
Fig. 28). Nose scars also indicate that a female is sexually man et al. 1988 *; Deutsch, personal communication).
mature, although some multiparous females have very Territorial maintenance is probably associated with the
little or no scarring. Interestingly, certain territorial males availability of good habitat (e.g., food, protected resting
in the Monterey area tended to be consistently rougher on sites) and an adequate number of estrous females, both of
females' noses than other males were during mating. which vary seasonally.
These females often sustained extremely serious nose and The best territories in California include canopy-form-
facial lacerations. In two cases, most of the nose was ing kelp (especially Macrocystis pyrifera), sheltered
removed (Ames, Riedman, and Staedler, unpublished areas for resting, and adequate food resources. The den-
data). Ames et al. (unpublished manuscript) reported that sity, distribution, and configuration of the kelp canopy, as
complications stemming from severe nose or facial inju- well as topographical features of the coastline, may play
ries inflicted during copulation may cause death in some a role in delineating territorial boundaries. In the southern
females, and they speculated that some of the youngest part of the range, the seasonal kelp canopy reduction that
and oldest females may be drowned during vigorous occurs in winter and spring may diminish the potential
mating bouts. Garshelis et al. ( 1984) observed one female number of male territories in preferred locations and
that died shortly after a forced copulation in Prince Wil- intensify competition for the remaining available sites.
liam Sound. On two separate occasions, one tagged male James on ( 1989) found that the kelp canopy in an area near
who held a territory along the northern Monterey penin- Point Piedras Blancas diminished from 150 ha in late
sula was observed copulating with a tagged dead female. summer to 8.3 ha during the following winter, with most
In the first case, he appeared to have accidentally killed winter kelp concentrated in one-fifth the area of the
her during an attempted copulation, at which time she was summer kelp distribution.
accompanied by a large pup approaching weaning age. In The number of potentially sexually receptive females
the second case, it was not known whether the male killed varies seasonally, as does the density and distribution of
the female, but she had a pup that was much too young to reproductively active males that maintain territories
be weaned (Riedman, Staedler, and Estes, in preparation). within female areas. Observations from the southern part
Jameson (personal communication) also observed a male ofthe range (Jameson 1983b) showed that throughout the
holding and guarding a female carcass. summer-fall breeding season, when the number of es-
trous females was potentially high, males held territories
within female areas. Jameson (1989) found that the num-
Reproduction in the Male ber of territorial males in female areas peaked in late
summer, with a mean arrival date of 28 May and a mean
Reproductive Physiology
departure date of 21 December. During the winter-spring
Although limited in scope, studies of male reproductive
pupping season, most adult males leave female areas to
physiologr have taken place primarily in Alaska. Schnei-
join male groups at the southern end of the range, evi-
der ( 1978 ) concluded that Alaskan males did not reach
dently because of increased competition for suitable ter-
sexual maturity for 5-6 years, and became active breeders
ritories, as well as the presence of fewer estrous females
several years later. Males 2-6 years old were rarely found
at this time of year.
in female areas during the breeding season (Schneider
In contrast, Loughlin ( 1977, 1980) found that territorial
1972b *). Garshelis (1983) found that no males aged <6
males remained in female areas throughout the year in the
years bred successfully. According to Johnson (cited in
northern part of the range near Monterey. He identified
·~ Ralls et al. 1983), Alaskan males did not hold territories
seven territorial males and reported that at least two of
until 8-10 years of age. The onset of sexual maturity and
these maintained territories continuously for 1 year or
the age that males become reproductively active in Cali-
longer. Recent observations of territorial males along the
fornia has not been established. Green (1978) suggested
northern Monterey peninsula confirmed Loughlin's fmd-
that California males reach sexual maturity at about 5
ings that territories are maintained throughout the year in
years but probably do not establish territories or actively
this area; many of these males have remained in their
breed for 2-3 or more years after reaching puberty. Sper-
territory for several years (Riedman et al. 1988 * ; Deutsch,
matogenesis in the Alaskan population occurs throughout
personal communication).
the year, although individuals probably produce sperm on
In summary, whether or not territories are maintained
an intermittent basis (Lensink 1962). Old males shown no
on a year-round or seasonal basis in female areas may be
signs of diminished sperm production (Kenyon 1969).
related to the following variables: topography, exposure
Territoriality to storms, abundance and distribution of kelp beds, abun-
California. In California, adult males establish and dance of food resources, number of sexually receptive
maintain territories in areas of high female density, sea- females, and distance from peripheral male groups. The
sonally (Vandevere 1970* ; Jameson 1989) and, some- length of time throughout the year that territories are

.; .
 THE SEA OTTER: BEHAVIOR. ECOLOGY. AND NATURAL HISTORY 63

maintained may vary depending on reproductive benefits which is similar to the overall average weight of 29 kg
or mating opportunities compared with costs of territorial reported for adult males in California (Woodhouse et al.
maintenance. There may be more opportunities for males 1977*; Ames, unpublished data). The average weight of
to mate throughout the year in Monterey. As Jameson transient males in Jameson's study was about 29 kg (N =
( 1989) pointed out, the northern side of the Monterey 12), although it was possible that some of the transient
peninsula is more sheltered from storms than his study males were actually territorial males moving to or from
area near Point Piedras Blancas, and the seasonal kelp their territories at the time they were captured.
canopy reduction in Monterey seems to be not as pro- Alaska. In Alaska, territories are also maintained sea-
nounced. In addition, the kelp beds off northern Monterey sonally (Schneider 1972b *, 1978 *: Garshelis 1983; Gar-
do not extend as far offshore as they do in the Piedras shelis et a!. 1984) and, to a lesser extent. throughout the
Blancas area, and onshore-Dffshore "layering" of territo- year (Lensink I 962; Sinha eta!. 1966: Antrim and Cornell
ries does not occur in Monterey Bay. 1980). However, with the exception of Garshelis's work.
Individual adult males show long-term site fidelity, less information is available on male territories in Alaska.
returning each year to the same territory (Loughlin 1977; Kenyon ( 1969) did not observe obvious male territorial
Jameson 1989). Several males near Point Piedras Blancas behavior on Amchitka Island, although lone adult male
held the same territory each breeding season for up to 6 otters were repeatedly seen in the same locations in a
years, and each territorial male habitually rested within female area, and numerous instances of pair-bonding
several meters of the same site after returning to his were observed. He surmised that males traveled from
territory (Jameson 1983b, 1989). Along the northern male to female areas when actively searching for estrous
Monterey peninsula, two males held the same territories females, without necessarily maintaining distinct territo-
for at least 7 and 8 years before their deaths, and another ries in the female areas. However, Kenyon did not observe
male occupied a territory he has held for at least 9 years individually marked males, and it is likely that territories
(Deutsch, unpublished data; Riedman, Staedler, and are maintained at Amchitka.
Estes, unpublished data). Garshelis (1983) and Garshelis et a!. (1984), who
Territorial males near Monterey seem to rest exclu- workei.i in Prince William Sound. presented the most
sively within their territories, although they sometimes recent and comprehensive study of male territoriality in
leave their territories to feed or search for estrous females, Alaskan sea otters. They identified four criteria for char-
occasionally trespassing through another male's territory. acterizing territory quality: availablity of food resources,
For instance, territorial males are sometimes observed territory size, degree of enclosure (protected versus open
feeding beyond the edge of the kelp bed up to several area), and accessibility or defensibility of territory en-
hundred meters offshore of their territories (Deutsch, trances. The presence of abundant food resources may
unpublished data; Riedman, Staedler, and Estes, unpub- attract females to particular territories, although this is
lished data). Territorial males have also been observed in difficult to measure due to the patchy distribution of prey.
another male's territory attempting to drag a female back Females with pups preferred territories with shallow-
to the first male's territory; two males seem to employ this water areas and mussel (M. edulis) beds where pups could
mating strategy more often than other otters (Deutsch, forage easily. Females also seemed attracted to well-
unpublished data; Riedman, Staedler, and Estes, unpub- enclosed and protected territories. Female-pup pairs
lished data). Females and dependent pups are allowed to often entered sheltered territories to rest during stormy
rest within the territorial boundaries while other males weather, which occurred frequently during the fall breed-
generally are not. Resting females, however, are some- ing season. In addition, territories with narrower entrance-
times disturbed by a resident male attempting to steal food ways-if they were not obstructed by other territories-
or initiate mating activity. Transient males are usually could be more easily guarded to prevent other males from
permitted to pass through or feed within a territory. entering or females from leaving. Simply by virtue of
Males often patrol the boundaries of their territories, their size. larger territories were more likely than smaller
sometimes seeming to advertising their presence with territories to contain adequate food resources and pro-
pronounced displays of splashing and grooming. Fights tected resting areas.
involving one or more territorial males are seen infre- Garshelis et a!. ( 1984) found that the average territory
quently; they typically involve lunging, pushing, and size at mid tide was 23 ha (N = I 2), ranging from 4 to 50
shoving motions directed toward the opponent's chest, ha, which was somewhat smaller than the 35-40 ha mean
face, and neck (Fisher 1939; Vandevere 1970*; Loughlin reported in California (Loughlin 1980: Jameson 1989).
1977, 1980). Calkins and Lent (1975) reported territory sizes for two
The elements of mating success in California males males in Prince William Sound to be 75 ha and 125 ha.
(i.e., correlations with size, age, and territory quality) Mating success of individual males in Prince William
have not been determined. Jameson ( 1989) found that the Sound varied with territory quality, duration of territory
weights of territorial males averaged 30 kg (N = 10), occupation, age, and size of the male (Garshelis et al.
 64 BIOLOGICALREPORT90 (14)

1984). Territory quality (ranked by the four qualities Although the breeding season in Prince William Sound
mentioned) was significantly correlated with the number peaks in fall, some males established territories as early
of copulations and pair-bonds formed with the different as April or May. However, before August, territories were
females observed within each territory. Mating success not rigorously maintained, and the territory holders often
was also correlated with the length of time a male occu- left their territories for up to 2 weeks in spring and early
pied his territory. Only males that spent >2 months in their summer to feed in areas where food resources were ap-
territories mated more than once and formed multiple parently more abundant. By September, territories were
pair-bonds. Conversely, mating success was low for well defined; most territories were vacated by December.
males that occupied their territory for< 1 month (although In winter, several territorial males occasionally returned
mating success was not determined for males when they to female areas, evidently in search of estrous females that
were not in their territories). Males that remained < 1 became receptive after the main fall breeding season
month occupied the poorest quality territories. (Garshelis et al. 1984 ).
Large males held higher quality territories than did
smaller (and presumably younger) males in Prince Wil-
liam Sound. Territorial males ranged in age from 6 years Reproduction in the Female
to > 12 years (N = 7). Males weighing less than 34 kg
occupied the poorest quality territories, while the best Reproductive Physiology
territories were occupied by the heavier, older males. In Alaska, most females reach reproductive maturity
Gars he lis et al. ( 1984) suggested that females may choose (enter their first estrus) between 4 and 5 years of age,
a mate not only on the basis of territory quality but size although some females enter their first estrus as early as
and age of the male. Indirect evidence suggests that males 3 years (Kenyon 1969; Schneider 1972a* , 1973a*; Gar-
typically develop a white-headed appearance at about 6 shelis 1983; Garshelis et al. 1984; Calkins and Schneider
years, while females do so at 8-9 years (Garshelis 1984). 1984* ; Jameson and Johnson, unpublished manuscript).
Garshelis et al. ( 1984) speculated that earlier develop- Although comparatively little information is available
ment of white-headedness in males may have evolved concerning the onset of sexual maturity in female Cali-
with the attraction of females to older-looking males. fornia sea otters, preliminary observations indicated a
Individual males in Prince William Sound exhibited site similarity with Alaska (Wendell et al. 1984; Jameson and
fidelity to their territory, as occurs among California Johnson, unpublished manuscript). Wendell et al. (1984)
males. Several males in Prince William Sound returned reported that one female gave birth for the first time at 4
to the same territories for 2-9 years. However, one male years. Jameson and Johnson (unpublished manuscript)
switched to the highest-rated territory after its occupant found that 67% (6 of 9) of the California females they
died (Garshelis eta!. 1984). No displacement of territory observed mated for the first time after reaching 4 years of
holders by other males occurred. All cases of territorial age. Of nine females, two pupped for the first time in their
desertion were evidently voluntary. third year of life, one in the fourth year, four in the fifth
Territorial and agonistic behavior of sea otters in Prince year, one in the sixth year, and one in her seventh year.
William Sound appears to be similar to that observed in Two females in Monterey mated for the first time at about
California. Territorial males often patrolled the bound- 2 years of age, and one of these females gave birth at 2.5
aries of their territories with vigorous and highly visible years, although her pup died soon after birth (Riedman et
grooming, kicking, and splashing (Calkins and Lent a!. 1988 *). Jameson and Johnson (unpublished manu-
1975; Garshelis et a!. 1984 ). Most territorial males left script) found that 50% (N = 6) of females with first pups
their territories for brief feeding excursions (generally lost their offspring before weaning.
lasting <10 h, but up· to 2 days), during which time Primiparous and multiparous females seem to come
territorial encroachment by other males was most com- into estrus and mate < 1 day to a few weeks after weaning
mon. Territory holders frequently rested in the main en- their pups in Alaska (Schneider 1978 *) and in California
tranceway of their territories at dusk, when transient (Jameson and Johnson, unpublished data; Riedman eta!.
males often entered the study area (Garshelis et al. 1984). 1988 *). Preliminary observations in the Monterey area
Actual fighting between males as well as territorial tres- suggested that a female often comes into estrus im-
passing by transient or other territorial males was infre- mediately after weaning her pup, at which time she cop-
quently observed. Territory holders usually repulsed tres- ulates or forms a pair-bond (Riedman et al. 1988*;
passers without actual contact or by brief aggressive Deutsch, unpublished data). Jameson and Johnson (un-
interactions (lasting <5 s), although one vigorous fight published manuscript) found that the mean interval be-
lasted 9 min (Garshelis et a!. 1984). Calkins and Lent tween separation from pup and copulation was 2.7 days
.. ( 1975) observed two brief fights (in defense of territory) for six Prince William Sound females (<1 day for four of
•.
:: i in addition to numerous chases of the intruding male from these females). Females in the Monterey Bay area that
the trespassed territory. have lost their pups (usually <2 weeks after parturition)
l
 THE SEA OTTER: BEHAVIOR. ECOLOGY. AND ~ATURAL HISTORY 65

came into estrus again and copulated about l-4 weeks multiple ovulations. Of these, five resulted in twin fetuses
after the pup ·s death (Riedman et a!. 1988 *). When cap- and one in triplet fetuses; most of the fetuses were rela-
tive Alaska females at the Tacoma Aquarium lost their tively large-sized and appeared to have developed nor-
pups before weaning, each female came into estrus within mally. These data indicate that more than one ovulation
a month after her pup died (Brosseau eta!. 1975). took place in 4.2% of the estrus cycles. and about half of
Observations from Alaska and California suggested these resulted in the development of more than one fetus.
that the average period of female sexual receptivity (du- In the Commander Islands, Barabash-Nikiforov (1947)
ration of estrus) seems to be 3-4 days (Garshelis et a!. found twin embryos in utero, and cited two similar cases
1984; Riedman eta!. 1988 * ; Jameson, unpublished data; reported by Japanese traders.
Deutsch, personal communication). Yet several Califor- It is highly unlikely that a mother could successfully
nia females, especially older individuals, seemed to come raise two newborn pups at once. However. a number of
into estrus 2-3 or more times within 2-3 months or observations of females accompanied by two pups of
possibly remained in estrus throughout this period until different as well as similar ages have been made in the
they were successfully impregnated, suggesting that aged Commander Islands (Barabash-Nikiforov I 94 7;
females possibly experienced problems in successfully Barabash-Nikiforov et al. 1968) and in Alaska (Snow
conceiving or maintaining early pregnancy (Riedman et 1910; Lensink 1962; Kenyon 1969: Garshelis 1983). It is
a!. 1988\ According to Brosseau eta!. (1975), captive unclear whether one of the pups was an orphan or the
Alaska females seemed to be in estrus for about 5 days; female ·s pup from a current or previous birth.
if conception did not occur, females seemed to come into Sea otters undergo a period of delayed implantation
estrus again within 5 weeks. It is not known for certain (Sinha et a!. 1966). The unimplanted gestation period in
whether a female would remain in estrus if she did not Alaska has been estimated to last from a minimum of
copulate, if the duration of estrus is variable as to when 3.5-4.5 months (Schneider 1972a ~.l973a*, 1978*)to 7-8
and how often the female copulates, or what factors or months (Kenyon I 969). There is more recent evidence
mechanisms stimulate ovulation and the onset of estrus. indicating that the length of preimplanted pregnancy may
Ovulation is induced by mating activity in other mustelids, be variable (Kenyon 198 I) and, in some instances, brief
yet the cessation oflactation stimulates ovulation in many (less than I-2 months), especially in California (Loughlin
other mammals (Cowie 1972) and may do so in sea otters. eta!. I 981 ). Detailed gross and microanatomical descrip-
However. Schneider ( 1978 *) found that a fairly high tions of the female reproductive tract are provided by
proportion of females with pups in Alaska began estrus, Sinha et a!. (I 966) and Kenyon (I 969).
although most failed to produce a successful pregnancy. The composition of sea otter milk is similar to that of
In California and Alaska, observations of mother and pup other marine and aquatic mammal species in its high fat
pairs indicated that females rarely copulate while still and low lactose content (Estes I 989). Fat and protein
accompanied by a pup (Kenyon 1969; Calkins and Lent content of four milk samples taken in California ranged
1975; Garshelis eta!. 1984; Riedman, Staedler, and Estes, from about 21-26% and 9-12%, respectively (Jenness et
unpublished data; Deutsch, personal communication). a!. I 981 ). The fat content of sea otter milk is considerably
Like all marine mammal species, sea otters give birth higher than that of other mustelids, such as badgers
to a single pup (Estes 1979). Twinning is rare, but it has (Taxi de a taxus; Jenness, unpublished data) and ferrets
been reported occasionally. No case has been documented (Mustela putorius: Jenness and Sloan I 970), in which
in which a female raised both pups successfully. Williams milk fat content has been reported to be 9.5 and 8%.
et al. ( 1980) found an adult female that evidently died However. many phocid seals and cetaceans have higher
while giving birth to twin fetuses (same incident de- average concentrations of milk fat than sea otters, exceed-
scribed in Wild and Ames 1974). Jameson and Bodkin ing 50% in some stages of lactation (Riedman I 990). The
( 1986) observed a female that probably had recently high proportion of fat and protein in the milk provides a
given birth to live twins. Although initially she nursed and high-energy diet and promotes rapid tissue growth in the
cared for both pups, one (a 1.1-kg female) was abandoned pup, which is important for survival in the marine envi-
about 24 h following birth and was taken to the Monterey ronment.
Bay Aquarium, where she is currently (October 1990) a It is unknown if changes in milk composition occur
healthy 6-year-old juvenile. throughout lactation in sea otters. In other mammals that
In the Aleutian Islands, Kenyon ( 1969) found no twin feed throughout lactation, fat and protein content tend to
fetuses in 178 female reproduotive tracts. Sinha et a!. remain constant during the nursing period (e.g., northern
( 1966) also found no evidence of twinning in 83 pregnant fur seal; Ashworth et al. 1966) or increase slightly (e.g.,
females. Both Kenyon ( 1969) and Sinha et al. (1966) black-tailed deer, Odocoileus hemionus; Mueller and
found reproductive tracts containing two corpora lutea Sad1eir 1977). Therefore, pronounced increases in milk
although only one fetus was present. Schneider (1972a *) fat composition over time probably do not occur in sea
examined 565 reproductive tracts and found 24 cases of otters as they do in fasting and lactating marine mammals,
66 BIOLOGICAL REPORT 90 (14)

such as northern elephant seals (M irounga angustirostris; 1981) and 6 months (Estes and Jameson 1983a* ; Jameson
Riedman and Ortiz 1979). and Johnson, unpublished manuscript). Assuming that
copulation occurred soon after weaning, Jameson and
Temporal Parameters Characterizing Johnson (unpublished manuscript) estimated maximum
the Reproductive Cycle gestation periods for 22 pups (born to 13 females) and
There seems to be a potential for considerable individ- found a range of 5.0-7.8 months, with a mean of 6.0
ual as well as geographical variation and plasticity in the months. They suggested that the 6-month gestation period
temporal phases of the female sea otter's reproductive consists of an implanted phase of 4 months and an un-
cycle. Evidence from California indicated that most adult implanted phase of2-3 months. Among California otters,
females give birth to one pup each year, with the repro- variation seems to occur in gestation length over time
ductive cycle ranging from 11 to 14 months (Vandevere between successive reproductive cycles. The length of
1978 * , 1979 *;JamesonandJohnson 1979;Loughlinetal. gestation periods may generally vary at the population
1981; Estes and Jameson 1983a; * Wendell et al. 1984; level in California, Prince William Sound, and the Aleu-
Siniff and Ralls 1988 * ; Jameson and Johnson, unpub- tian Islands; however, with the limited information and
lished manuscript). Jameson and Johnson (unpublished rough estimates of gestation lengths from early studies in
manuscript) calculated a reproductive cycle or mean pup- Alaska, and because of the different methodologies em-
ping interval of 12.4 months (N = 11; SE = 0.20). The ployed in Alaska and California, it is difficult to establish
natality rate among California females is estimated to be that such differences exist.
85-90% (Jameson and Johnson, unpublished manu- In Alaska, estimates of gestation length were derived
script). Siniff and Ralls (1988 *) radio-tagged adult fe- from examination of ovaries and conceptuses of repro-
males in California and found them to produce 0.87-0.90 ductive tracts rather than by observation of marked indi-
pups per year. These and other data (Loughlin et al. 1981; viduals. In the Aleutian Islands, Kenyon (1969) and
Wendell et al. 1984; Riedman, Staedler, and Estes, unpub- Chapman (in Kenyon 1969) estimated gestation to be
lished data) indicate that adult female California sea 10-12 months, with the implanted period lasting 4.5-5.5
otters most frequently give birth annually. months; however, these estimates were based on assump-
Lensink (1962) believed that females at Amchitka tions that the fetal growth rate during the implanted
Island gave birth every 2 years, while Kanaga Island pregnancy was similar to that of river otters, and that the
females gave birth each year. He suggested that geograph- timing of the peak mating and pupping seasons was
ical differences in reproductive cycles might account for representative of all of the reproductive tracts sampled.
the higher proportion of pups in the Kanaga Island popu- They note that the estimates of gestation period may be
lation. On the basis of histological and gross morpholog- high due to sampling errors. Schneider (1973a * ) esti-
ical examination of female urogenital tracts, Chapman (in mated that females in the Aleutian Islands had a gestation
Kenyon 1969), Kenyon (1969), and Schne1der . (1971 *) of 7.5 months with an implanted period of about 3.8
estimated that the reproductive cycle of females in the months. He also based his estimate on another estimate
Aleutian Islands was about 2 years. Kenyon (1982) sug- of peak breeding and pupping periods derived by analyz-
gested that females in Alaska gave birth every 2 years in ing reproductive tracts. Barabash-Nikiforov (1947) as-
areas of high population density. sumed that the gestation in Commander Island sea otters
Most females observed by Garshelis (1983) in Prince was about 8-9 months, based on the timing of mating and
William Sound (seven of eight) gave birth every 2 years, pupping seasons, stage of development of the pup at birth,
whereas one female pupped annually. Yet Garshelis esti- and one captive female that mated and gave birth 8
mated that pup dependency lasted only 5-6 months. He months later.
concluded that, although females are capable of reproduc- According to Wendell et al. (1984), pup dependency
ing annually, they rarely do so under food-stressed con- periods in California were 5-8 months, although most
ditions. Garshelis et al. ( 1984) speculated that poor phys- pups seemed to be weaned at around 6 months. Riedman
ical condition may lengthen reproductive cycles in some et al. ( 1988 *) found that pup dependency varied from
females by causing delayed estrus, delayed implantation, 4.5-9.5 months. Jameson and Johnson (unpublished
or resorption of the embryo. Jameson and Johnson (un- manuscript) followed 23 females in the southern part of
published manuscript) found that 77% ( 17 of 22) of the the range near Point Piedras Blancas and found that pup
females in Prince William Sound pupped annually, but the dependency lasted 5.0-7.5 months, averaging 6.1
remaining 5 females may have had longer reproductive months. Estes and Jameson (1983a *) estimated that pup
cycles. dependency periods were about 6 months. Payne and
The most accurate estimates of gestation length in sea Jameson (1984) also calculated a mean pup dependency
otters have been derived from observations of marked of 6 months; they presented ontogenetic information on
individual females in California. The gestation period pup development showing that 6-month-old pups are
there has been estimated at 4-6 months (Loughlin et al. self-sufficient in all activities and seem capable of surviv-
 THESE.~ OTTER BEH.-'. v1oR. EcoLoGY ..-'.\D \" ~ n R.~L HisTORY 67

ing on their own. It seems likely that pups abandoned or N = 23). ~o sex differences were detected in the duration
otherwise orphaned at <4.0-4.5 months do not survive on of pup dependency (Monnett and Ratterman 1988b * ).
their own in California, although in, Prince William Garshelis eta!. ( 1984) similarly found that pup dependency
Sound. Monnett and Ratterman ( 1988b ·) found that pups periods of 5---D months seemed to be common in Prince
survived when weaned only an estimated 2.5 months after William Sound. although he thought mo~t females gave birth
birth. Loughlin et al. ( 1981) reported pup dependency only every 2 years. In the Commander Islands. pup de-
periods of 8.0-8.5 months for three female and pup pairs pendency seemed to be 6-7 months 1B arabash-N ikiforov
and 3.5-6.0 months for two others. et al. 1968).
In Alaska. the duration of pup dependency often seems It is unclear why pup dependency periods are so vari-
longer than that observed in California. Kenyon ( 1969) able amone: females in the same area. although Monnett
believed that Aleutian Island females cared for their and Rotter~an ( 1988b *) suggested that variables such as
pups for a least I year-possibly longer in some cases. the abundance of food and a female ·s age and health may
Schneider ( 1971 ~) suggested that pup dependency peri- intluence the duration of dependenc;. periods. Observa-
ods in the Aleutian Islands were also about I year. In tions in the Monterey area suggest that a female's weight
Prince William Sound. Jameson and Johnson ( 1979*) may be related to the length of time she cares for her pup,
estimated that the duration of pup dependency was 6 and long-term research in the Monterey area may be able
months or longer. From radio-tagged adult females in to show how a female's age. diet. and foraging behavior
Prince William Sound. the average duration of pup depen- untimately intluence the length of her pup dependency
dency was estimated to be 169 days (5.6 months). al- periods and reproductive success (RJedman. Estes, and
though this varied from 76 to 333 days (2.7-12.0 months: Staedler. unpublished data).

Fig. 29. California sea otter mother nursing small pup about I month of age (D. Buchich).
68 BIOLOGICAL REPORT 90 ( 14)

Maternal Care and Pup Development resting, and substantially less time feeding (2%) than
Parental care is provided exclusively by the female. females with larger pups (26%; Sandegren eta!. 1973).
Maternal behavior in California sea otters has been Studies in Monterey also suggested that females with very
described by Fisher ( 1940), Limbaugh ( 1961 ), and Davis young pups spent more time resting and less time feeding
( 1979), but various aspects of pup development and ma- during the day than other animals (Riedman, Staedler, and
ternal care have been quantified or studied in greater Estes, unpublished data; Lyons, personal communica-
detail (Vandevere 1972~; Sandegren et al. 1973; Payne tion). It is possible that females with young pups spend
~ *
and Jameson 1984: Staedler 1987; Riedman et al. 1988 ; proportionally more time feeding at night than indepen-
Faurot, unpublished data). Kenyon ( 1969) provides a dent otters or females with large pups. Mothers with large
detailed description of maternal and filial behavior pups, however, appear to spend an equivalent or greater
among Alaskan sea otters. amount of time feeding during the day than independent
Observations from California indicate that parturition otters in the northern part of the California range
occurs both in the water (Sandegren et al. 1973; Riedman, (Sandegren et al. 1973; Lyons, unpublished data: Ried-
unpublished data) and on land (Woodward 1981 b; Jame- man, Staedler, and Estes, unpublished data) and in Alaska
son 1983a). Jameson ( 1983a) suggested that females may (Garshelis 1983). In addition, females with large pups
give birth on land in areas where kelp beds are sparse. obtain food not only for themselves but also capture much
Barabash-Nikiforov (1947) believed that birth occurred of the food eaten by their pup as well (Riedman, Staedler.
on land in the Commander Islands. He observed one and Estes, unpublished data). However, Ralls and Siniff
female that gave birth on land, and he found placentas on ( 1988 *) found that females with small pups fed slightly
the shore on two other occasions. Intensive postpartum more than females with large pups over a 24-h period in
grooming of the pup by its mother begins immediatell the central and southern parts of the range, although this
after birth (Sandegren et al. 1973; Woodward 1981a; difference was not significant. Mothers with small pups
Jameson 1983a). spent 40.6% of their time resting, 42.71% feeding, and
Mothers with newborns often tend to avoid other otters 16.5% engaged in other activities; mothers with large
(Fig. 29). Within several days of parturition, however, pups spent 48.45% of their time resting, 36% feeding, and
females will associate and rest with otters in rafts contain- 15.5% engaged in other activities. Sandegren et al. ( 1973)
ing other female and pup pairs (Sandegren et al. 1973; found that the diurnal activity cycle of females with pups
Jameson, unpublished data). Sandegren et al. (1973) was similar to that of independent otters, with activity
found that during the peak winter pupping season, fe- peaks at dawn and dusk, although observations in Mon-
males with pups behaved aggressively toward other indi- terey indicated that many females with large pups are
viduals, particularly during winter storms when sheltered active in the middle of the day (Riedman, Staedler, and
resting sites were scarce and kelp beds were sparse. Estes, unpublished data). Over a 24-h period, Ralls and
Apparently, competition for such favored resting sites Siniff ( 1988*) observed early morning and early evening
was intensified at this time. During brief periods of in- peaks in feeding activity among mothers with pups.
clement weather, mothers with young pups often repeat- While pups are young, females remain with their pups
edly swam in a large circular pattern, slowly traveling constantly unless the mother is diving for food. In some
downwind and then rapidly swimming upwind. areas of Alaska, bald eagles prey on small pups. appar-
Sandegren et al. (1973) suggested that females may swim ently capturing them as lone pups float on the surface
in such a pattern in response to their pup's apparent while their mothers are underwater (Sherrod et al. 1975).
distress during rough sea conditions as waves wash over Although sightings of pup capture were rare, numerous
them-a smooth downwind ride allows the pup to suckle remains of sea otter pups were discovered at eagle nest
and rest. sites at Amchitka Island in late spring and early summer.
A female invests considerable resources in caring for which corresponds with the seasonal peak in sea otter
her pup, which is dependent on her for nourishment, births and the period just before fledging of eagle chicks.
grooming, and protection, especially when young. Ac- Although some of the otter pups may have been obtained
cording to Sandegren et al. (1973), mothers nurse their by scavenging dead individuals, material examined from
pups an average of six times per day (during daylight), some of the nests showed hematomas around talon punc-
with each nursing bout averaging 9 min. Females with ture wounds and other evidence of live procurement.
pups at Point Lobos, California, spent 41% of their day- Eagles may cue in on the distinct, piercing vocalization
light hours resting, 16% feeding, 20% grooming their typical of pups separated from their mothers. The extent
pup, 10% grooming themselves, 13% swimming, and 8% to which nesting pairs of eagles exploit sea otter pups
nursing their pup (which was always done in conjunction varies substantially. The remains of one or more pups was
with resting, swimming, or grooming of the pup). During found repeatedly in some nests while never occurring in
daylight hours, females with smaller pups spent slightly others. At one nest site. nine pups were found over the
more time nursing and grooming their pups, more time breeding season.
 THE SEA OTTER: BEHAVIOR, EcoLOGY. AND NATURAL HISTORY 69

In 1972 at Amchitka Island, a minimum of 56 pup mined approximately by appearance and behavior. For
carcasses were retrieved from 34 nests examined. At that instance, the natal pelage was completely replaced by
time, there were 71 known active nest sites on the island, adult pelage by age 13 weeks. Nourishment was derived
and about 35-40% percent of the eagle population was primarily from the mother's milk during the first month;
composed of nonbreeding individuals. Thus, pup loss to by 4 months, the pup subsisted mainly on solid food
eagle predation may have affected the dynamics of the sea obtained by the mother. The pup's proficiency in other
otter population, even though it contained at least several activities, such as swimming, grooming, and the ability
thousand individuals (Estes 1977). The extent to which to use tools, also increased gradually with age. By 14
similar interactions occur in other areas containing both weeks, most pups were able to swim independently, dive
otters and bald eagles is unknown. It may be that eagle proficiently, and groom themselves without help from
predation on otter pups is restricted to areas where both their mothers. Pups captured and broke open hard-shelled
species are at resource-limited population abundances. In prey, using a rock tool, by 20-24 weeks (Payne and
Prince William Sound, coyotes apparently killed several Jameson 1984; Fig. 30). Despite these general correla-
recently weaned pups (Monnett and Ratterman 1988b \ tions between age and the development of various skills,
On numerous occasions. mothers have been observed pups of similar ages may show striking differences in
carrying and sometimes grooming their dead pups for up behaviors and proficiency in grooming, diving, and for-
to several days in Alaska (Kenyon 1969) and in California aging skills (Faurot 1987 *; Riedman et a!. 1988 *).
(Ames, Deutsch, Jameson. Lyons, Riedman, Staedler, In California (Payne and Jameson 1984) and in Alaska
unpublished data; Vandevere, personal communication). (Kenyon 1969; Schneider 1973a*) females continue to
Most of these pups are either newborns or less than one lactate until weaning, at which time-following an aver-
month old. In some cases, the pup had been dead for age pup dependency period of 6 months-California pups
several days, and patches of fur and skin were sloughing weigh about 12 kg (Jameson, unpublished data), and
from the carcass. One adult female (of unknown repro- Aleutian Island pups weigh 12-14 kg (Kenyon 1969;
ductive status) was seen carrying and manipulating a dead Schneider 1973a *). However, Schneider (1973a) * re-
red phalarope (Phalaropus fulicarius) as if it were a pup ported that one male pup reached 17 kg before weaning
(Vandevere, personal communication); another female took place. Preliminary information from California sug-
that had recently lost her newborn pup held and manipu- gests that the pup's weight may be positively correlated
lated an empty beer bottle like a pup (Riedman, Staedler, with its mother's weight-that is, small females may
and Estes, unpublished data). produce pups that are smaller than average in size at a
Payne and Jameson (1984) provided a detailed analysis given age (Riedman, Staedler, Estes, and Ames, unpub-
of the ontogeny of pup growth and behavioral develop- lished data).
ment (N = 14 wild California pups, 1 wild Oregon pup, As pups grow older and approach weaning age, inter-
and 3 captive pups); they found that age could be deter- actions between the mother and pup pair seem to change:

Fig. 30. California sea otter mother interacting with large pup, which is attempting to nurse; pup is approaching weaning age.
which is 5-8 months (D. Buchich).
70 BIOLOGICALREPORT90(14)

for instance, the mother may not offer her pup food as vicinity for several years. Riedman et al. (1988 * ) ob-
readily and may avoid her pup when it solicits prey served cases in which juvenile or adult female offspring
(Staedler 1987; Riedman et al. 1988 *). Preliminary obser- (up to 6 years old) interacted briefly with their mothers,
vations suggest that a mother may shift locations just as well as two instances in which pups reunited with their
before, during, or immediately after her pup is weaned in mothers after being separated or weaned. In one of these
California (Wendell et al. 1984; Jameson, unpublished cases, the mother cared for her pup an additional2 months
data; Riedman, Staedler, and Estes unpublished data) and after weaning it for about 1 week. In another instance, a
in Prince William Sound, Alaska (Monnett and Ratterman 14-kg female, who was not accompanied by a mother
1988a * ). In Prince William Sound, Garshelis eta!. ( 1984) when captured in Monterey (and released several kilome-
reported three cases in which pups (both male and female) ters from the capture site), was observed a few days later
traveled away from their mothers at the time of weaning. being nursed and groomed by her apparent mother back
Garshelis et al. ( 1984) suggested that sexual precopula- at the capture site. In another case a 2-year-old juvenile
tory interactions between the mother and a male may female was sighted in the same cove with her mother near
instigate female and pup separation and play a role in the Point Pinos (along the Monterey peninsula), but the pair
weaning process. was not observed to interact during the observation period
Observations of eight female and pup pairs in Prince (Lyons, personal communication). Studies focusing on
William Sound indicate that a mother in poor health may the existence and nature of relationships between females
abandon her pup before it is old enough to survive on its and their grown offspring are currently in progress in the
own. Three of the mothers who were in poor physical northern part of the range in California (Riedman et al.
condition (two of which died 1-2 days after separation) 1988 * ).
abandoned their pups, which weighed only 6--9 kg at
separation (Garshelis 1983). It is possible that periods of Alloparental Care and Adoption in Wild and
severe storms and rough sea conditions also promote Captive Sea Otters
premature separation of female and pup pairs in Califor- An alloparent is an animal, other than the genetic par-
nia (Morejohn et al. 1975; Riedman et al. 1988 *; Ames ent, that provides care for conspecific young (Wilson
unpublished data; Jameson, unpublished data) and at Am- 1975). Most alloparental and fostering behaviors are re-
chitka Island (Kenyon 1969). ported among mammals and birds, where systems of
It is unknown to what extent adult females associate parental care are especially well developed. Because
with their offspring after weaning. In Prince William many social mammals live in groups characterized by
Sound, Garshelis (1983) observed one instance in which matrifocal networks, and the primary burden of parental
a female pup, weaned at an estimated 7 kg, reunited with care usually falls on the female, it follows that most cases
her mother about 1 year after birth. The pup foraged of alloparenting and adoption in mammals involve female
independently throughout winter before rejoining her rather than male assistants or foster parents (Riedman
mother, who did not have a second pup at this time. The 1982).
mother and pup pair remained together continuously for Parental behavior directed toward nonfilial young su-
over 4 months, during which time the juvenile often took perficially seems to be a form of altruism in which the
food from her mother, especially when the mother cap- foster parent assists other individuals at its own expense
tured more food items or larger prey than did the pup. (Hamilton 1964) by investing its limited resources into
Separation of the pair seemed to be initiated by sexual promoting the survival of another's offspring. However,
interactions between the mother and a male. Observations individuals that care for foreign young may acquire ad-
of females accompanied by or caring for two pups of vantages associated with increased inclusive fitness
different ages have been made in Alaska (Lensink 1962; (based on kin selection), parental experience, reciprocal
Kenyon 1969) and in the·commander Islands (Barabash- altruism, and exploitation of the fostered young. In many
Nikiforov 1947; Barabash-Nikiforov et al. 1968), al- cases, environmental constraints (such as scarce breeding
though in all these instances it was unknown if the larger sites or food resources requiring cooperative foraging strat-
pup was the female's previous offspring or an adopted egies) seem to influence the occurrence of alloparenting and
orphan. Barabash-Nikiforov (1947) reported that "a adoption. In addition, proximate factors incorporating repro-
grown cub often remains with the mother even after a new ductive errors may be involved in some instances of foster-
one is born, so that the mother is seen together with the ing. Often, several selective benefits, along with various
newborn and a yearling." We regard this as unlikely in environmental pressures or reproductive mistakes, may
view of the infrequent nature of such sightings in subse- collectively promote the evolution of alloparental care
quent studies. and adoption (Riedman 1982).
Along the Monterey peninsula, many females and their Reproductive mistakes, as well as selective benefits
adult female offspring (some of which have produced associated with increased parental experience for juvenile
daughters of their own) have resided in the same general female sea otters and reciprocal cooperation in the form
 THE SEA 0TIER: BEHAVIOR. EcoLOGY. AND N.-\TL:RAL HisTORY 71

of "babysitting" behavior (allowing potentially increased though to survive, a young pup requiring milk would
foraging freedom for females with pups), might seem to certainly need the care of a lactating female. Kenyon
theoretically promote the occurrence of some degree of (1969) describes one allomothering incident in which a
allomothering and adoption among sea otters; however, wild adult female cared for two pups of similar size,
few instances of alloparental behavior or adoption have allowing both pups to nurse. However. most of the mater-
actually been observed in the wild. In captivity, the po- nal care was directed towards only one of the pups, and
tential for fostering behavior to occur, based on reproduc- Kenyon concluded that the other pup was probably an
tive mistakes made by female sea otters, seems to be orphan. A number of other cases of females accompanied
relatively high. by two pups of different (as well as similar) ages have
Wild Otters. Explanations for the scarcity of foster-par- been reported in Alaska (Lensink 1962: Garshelis 1983)
ent incidents among wild sea otters include the possibili- and in the Commander Islands (Barabash-Nikiforov
ties that (1) fostering behaviors are difficult to observe in 1947; Barabash-Nikiforov eta!. 1968). In most instances
the field and (2) such behaviors actually occur very infre- it was not clear if one pup was the female's previous
quently. The latter seems more likely. Given their social offspring or an orphan, although Barabash-Nikiforov
organization and breeding behavior, fostering opportuni- ( 1947) believed that a grown pup often remained with its
ties are rare for sea otters, unlike other mammals that give mother after she gave birth to a new pup. Kenyon ( 1969)
birth synchronously and raise their young in crowded suggested that in a noncaptive situation. an adult otter that
breeding colonies. such as several species of bats (Brosset tolerates or cares for an orphaned pup might enhance the
1962; Davis et a!. 1962), pinnipeds (Riedman and pup's chances of surviving; he also speculated that the
LeBoeuf 1982), and ungulates. Under those more extent of alloparenting behaviors observed may decrease
crowded circumstances, mother-pup separations and op- during stressful conditions (such as during storms or a
portunities for allomothering and adoption of orphaned shortage of food resources).
pups frequently arise. In California. a form of male exploitation of dependent
Among the California population of sea otters, females pups has been occasionally observed: it resembles the
give birth throughout the year and raise their pups in exploitive a!loparental care that occurs in many species
low-density groups in the water rather than in crowded of primates, in which the male with an infant in his
breeding colonies. The chances of an orphaned sea otter possession may derive benefits such as increased social
pup encountering a potential foster mother-particularly status, protection from aggressive conspecifics, or vari-
one that has recently lost her own pup-are probably ous reproductive opportunities (Riedman 1982). In sea
remote. otters, the benefits resulting from possession of a depen-
However, one well documented adoption in Monterey dent pup seem to be related to "free" food: many incidents
lasted 2-3 weeks (Staedler and Riedman 1989). The have been observed in which an adult male stole the pup
foster mother was a tagged adult female of known history. of a foraging female and relinquished the pup only when
She cared for a large female pup that had apparently the mother gave the male her prey (R1edman eta!. 1988 *;
0

recently lost its mother. The adoptive female nursed, Faurot, Schusterman, and Vandevere, personal communi-
shared food with, and rested with the orphan for at least cation). However, the male did not actually provide care
2 weeks. However, the orphan, was found dead on a for the pup (Riedman eta!. 1988 *).
nearby beach 3 weeks after being adopted. (The pup was Captive Otters. Numerous instances of allomaternal
30% underweight when it died, probably of starvation.) care, foster-parenting behaviors, and adoption of pups
Staedler and Riedman ( 1989) attributed this case of adop- have been observed among captive Alaskan sea otters at
tion to reproductive mistakes on the part of the female, the Seattle Aquarium (C. J. Casson, personal communi-
who evidently lost her own pup soon after its birth, several cation), the Vancouver Aquarium, and Point Defiance
days before she adopted the orphaned pup. Zoo and Aquarium (S. Hewlett, personal communica-
In Alaska, orphaned wild sea otter pups, as well as tion). All of the fostering events occurred naturally-
juveniles. are sometimes observed with a tolerant adult of there was no human intervention, and no animals were
either sex (Kenyon 1969). In the Monterey area, depen- artifically primed to accept a pup.
dent pups as well as recently weaned juveniles are some- At the Seattle Aquarium, all the allomothering incidents
times observed trying to suckle from mothers with pups occurred at successive intervals between one adult female
or from independent females (Riedman et al. 1988 *, and four different pups that were unrelated to the female.
Deutsch. personal communicatioQ.)-for instance, near The adult male never exhibited interest in the pups. All
Monterey, a tagged juvenile weaned in late August near four pups (both males and females) were offspring of the
Monterey was observed about 3 months later in its natal same female, and each pup grew to adult status. During
area attempting to suckle a tolerant subadult female. the fostering incidents, the pups' ages varied from 2
The quality and extent of care given to orphaned pups months to 10 months. The all om other was observed to
by accompanying adults is unclear in many cases, al- care for each of the four pups for short periods of several
72 BIOLOGICAL REPORT 90 ( 14)

minutes while the genetic mother was present. The and 4-year-old female (Ma-Linke) remained in the dis-
allomother's caretaking behavior involved grooming the play with Nooka and her adopted pup. Although the male
pup, offering the pup solid food, and protecting it from showed no interest in the pup (at least during daylight
adult males. hours, when the staff was present), the young female wa:-,
Two separate cases of adoption lasting 2-3 days were allowed to act as allomother and to hold the pup several
observed between the adult female and the two most times.
recently born pups. The adoptions took place when the On 7 August 1984, Ma-Linke gave birth to a healthy
pups were about 7 and 10 months old, at which time their male pup. Cordova and Nooka both attempted to steal
mother temporarily abandoned them. During the 2-3 days Ma-Linke's pup, and the newborn was subsequently
of abandonment, the mother seemed to be in estrus and killed within 24 h because of tugging and pulling by the
spent most of her time close to, or mating with, the adult two adult females.
male. At this time, the foster mother became the pup's On 4 February 1985, Nooka delivered a stillborn male
exclusive caretaker, feeding the pup solid food, grooming pup and was placed on temporary loan to the Seattle
it, sleeping with it on her chest, and protecting it. Nursing Aquarium. On 17 February 1985, Cordova gave birth to
was not observed, although the adopted pup attempted to a healthy male pup. On 26 March 1985, Ma-Linke gave
suckle its foster mother several times. After the 2-3 days birth to a female pup. Although both females raised their
of mating activity, the genetic mother took the pup away own young, both pups were allowed to play on top of
from its foster mother imd began to care for it again Ma-Linke with no apparent concern from Cordova. How-
(Casson, personal communication). ever, both pups were killed during the night, on separate
At the Vancouver Aquarium, one case of adoption has occasions in early May, probably from injuries inflicted
been observed in which the foster mother stole the 4- by the adult male Sitka.
month-old pup of another female (who had cared for it Jim Short (personal communication) of the Point Defi-
successfully up to that point) and adopted it for several ance Zoo and Aquarium concludes that if a mother were
months. At the time of adoption, the foster mother had to be removed from the display, another female would
recently lost her own 8-month-old pup. The genetic adopt and attempt to raise her pup. An immature female
mother never seemed to offer resistance to the foster would probably also exhibit interest in the pup, al-
mother that took the pup or tried to regain it. The adoption though her level of interest might eventually decline as
was terminated by the aquarium staff when the foster the pup aged. Adult males seem to either ignore pups
mother gave birth to her own pup; this allowed her to care or behave aggressively and destructively toward them.
for the newborn. The adopted pup was well cared for and It is possible that the killing of young pups by adult
apparently healthy and in excellent condition (Hewlett, male otters parallels the occurrence of infanticide among
personal communication). mammals such as langurs (Presbytis spp.; Sugiyama
At the Point Defiance Zoo and Aquarium, it is fairly 1967, Hrdy 1974), lions (Panthera leo; Schaller 1972),
common for either nonlactating or lactating adult females and bears (McCullough 1981), so that the female that
to care for another female's pup. For example, a 6-year- has lost her offspring comes into estrus sooner. Al-
old, 23-kg adult female (named Cordova) gave birth to a though some of the captive sea otter pups may have
healthy male pup (pup 1) on 16 June 1984 at 9:00a.m. At been offspring of the male that killed them, this situa-
about I :00 p.m. on the same day, another adult female tion would be less likely in the wild. Infanticide by
(Nooka) of the same age and weight, stole Cordova's pup adult males has never been reported among wild. sea
and began to care for it. One hour later, Nooka gave birth otters.
to her own pup (pup 2). Both adult females ignored pup Kenyon ( 1969) documented one case of experimentally
2, which was removed from the display and revived twice induced allomothering that occurred in captivity. A
by the staff from near-drowning. Due to Nooka's persis- recently captured adult female was placed in an enclo-
tence in keeping pup l-and the possibility of injury to sure with an orphaned juvenile (8.2-kg) female several
the pups in a tug-of-war between the two females--Cor- months old. The juvenile approached the female within
dova was separated into a holding pool with pup 2 for the a few minutes, and she allowed it to suckle. The female
night. Cordova immediately tossed pup 2 against the wall also exhibited protective behavior towards the juve-
and the impact killed it. nile, clasping it around the neck when alarmed. The
Cordova was returned to the display on 22 June. How- female subsequently nursed and protected the juvenile
ever, within 24 hours, the adult females (both of whom for 8-9 days, with increasingly longer intervals elaps-
wanted the pup) managed to mortally injure Nooka's ing between caretaking behaviors. After the ninth day,
adopted pup with their pulling. The adoption of Cordova's the female did not allow the juvenile to suckle and
pup by Nooka therefore lasted 7 days, but it might have often stole its food, although the pair rested in close
continued throughout the pup's dependency if it had proximity and clasped one another with their forelegs
survived. During this time, the 8-year-old male (Sitka) when alarmed.
'
-

Population Dynamics
THE SEA OrrER: BEHAVIOR. EcoLOGY..\ND NATURAL HISTORY 73

that sea urchin size varies predictably with the presence

or absence of sea otter predation. Habitats without sea
otters contain sea urchins ranging from 60 to 80 mm in
Historical Distribution and Abundance test diameter, whereas sea urchins >35 mm test diameter
are almost never found where sea otters are present.
Historically, the sea otter's range extended from the regardless of how long the otter population has been
northern Japanese archipelago (from at least northern present. Thus, the presence of 60-80 mm test diameter
Hokkaido and southern Sakhalin) northward along the sea urchins throughout the kitchen middens indicates that
east coast of Kamchatka, eastward through the Com- sea otters were absent from at least certain areas during
mander Islands, Aleutian archipelago, and Pribilof Is- the era of Aleut prehistory. However, it is unlikely that
lands to the Alaska Peninsula. and along the Pacific coast any such effect was widespread because abundant popu-
of North America south to about central Baja California, lations were encountered by the Russians and other early
Mexico (Fig. 7). The exact southern extent of the range fur hunters.
in Baja California is unclear due to the lack of adequate Extensive exploitation of sea otters began in 1741,
historical records. According to Scammon ( 1870), sea following the discovery of Alaska. the Aleutian Islands.
otters occurred at Isla de Guadalupe and Isla de Cedros. and the Commander Islands by the Bering expedition.
Kenyon (1969) concluded that the sea otter's range ex- Subsequent exploitation in the eighteenth and nineteenth
tended to Morro Herrnoso, about 50 km south of Isla de centuries reduced the species throughout its range. By
Cedros. Because of coastal habitat distribution and pres- 1911, when protection for sea otters was established
ent day oceanographic conditions, sea otters probably under the International Fur Seal Treaty, only 13 small
could have lived at least as far south as Punta Abreojos, remnant populations are thought to have persisted. These
Baja California. This location marks the southern limit of occurred in the Kuril Islands and along the Kamchatka
extensive rocky habitat and coastal upwelling along the Peninsula, the Commander and Aleutian islands, south-
Pacific coast of North America. However, the southern western Alaska, the Alaska Peninsula and northern Gulf
limit of distribution probably varied with the northward of Alaska, the Queen Charlotte Islands in British Colum-
intrusion of anomalously warrn, nutrient-poor waters dur- bia. the Point Sur area in California, and Islas San Benitos
ing particularly strong ENSO (El Nino) events, or with in Mexico (Fig. 7). The total population at this time may
the southward extension of cold, nutrient-rich water dur- have contained as few as I ,000-2,000 animals (Ogden
ing periods when the California current was especially 1941; Kenyon 1969). Several of the remnant populations
strong. declined to extinction, including those in Mexico and
Before commercial exploitation, the worldwide popu- British Columbia (Kenyon 1969: Estes 1980).
lation of sea otters was estimated to be 150,000 (Kenyon Sea otter populations from the Kuril Islands northeast
1969) to 300,000 (Johnson 1982) animals. At that time, to Prince William Sound have subsequently recovered
the population in California was estimated to be 16,000- and presently occupy most of their historical range. How-
20,000 (California Department of Fish and Game 1976; ever, sea otters became extinct along the Pacific coast of
U.S. Fish and Wildlife Service 1982) and 20,000 (Johnson, North America from Prince William Sound to central Baja
personal communication, cited in Ralls et al. 1983). Ac- California, except for the remnant population in central
cording to Everrnann (1923), the estimated total number California and, more recently, translocated populations in
of otters killed in California and Baja California between southeastern Alaska, British Columbia, Washington, and
1786 and 1868 was 200,000, an average of 2,400 per year. Oregon. Legal protection of sea otters began in 1911;
Ogden (1941) estimated that 100,000 pelts were taken in recovery patterns following this action are poorly known.
California between 1776 and 1911, an average of 800 per Kenyon (1969: 192-193) concluded that " ... an isolated
year. Historical records suggest that the population may population having ample unused habitat may grow
have been especially abundant in the central and northern through local reproduction (no immigration) at a rate of
portions of the State and in the Channel Islands of south- about 10 to 12 percent per year." However, an analysis of
em California (Ogden 1941; Kenyon 1969). survey data from several recently reestablished sea otter
Aboriginal hunting of sea otters took place throughout populations (the naturally recolonized population at Attu
the range. In some areas, localized overexploitation and Island and the populations translocated to southeastern
substantial reduction of sea otter populations by indige- Alaska, British Columbia, and Washington State) indi-
nous people apparently occurred (Simenstad et al. 1978). cates that these populations all have increased at rates of
Evidence for this conclusion comes from faunal remains 17-20% per year (Estes 1990a). In contrast, the popula-
in the Aleut kitchen middens at Amchitka Island. The tion in California has increased at a rate of 4-5% per year
calcareous remains of sea urchins, from which size of (Estes 1990a). Chapman's ( 1981) analysis of Kenyon ·s
living urchins can be estimated, are abundant throughout data indicates that the population at Amchitka Island
the middens. Ecological studies of this area have shown grew 19% per year, an estimate consistent with Estes's
 74 BrOLOGJCALREPORT 90 (14)

Table 6. Size and probable status of sea otter (Enhydra lutris) population in the North Pacific Ocean. Data from
International Union for the Conservation of Nature, Otter Action Plan, and Estes, /990b.
Date Count or Population
Location surveyed estimate a statusb Comments Source

Soviet Union
Kuril Islands 1984 6,000...7 ,000" Survey methods and estimation Maminov 1984*
teclm ique unknown
<
Kamchatka Peninsula 1984 2,132 3 Survey methods unknown; population Khromovskikh 1984
may be limited by winter sea ice

Commander Islands 1988 4,714 2 Survey methods unknown; Medny A. Zorin and A. Burdin
Island at or near equilibrium density; (personal communication)
Bering Island below equilibrium density

Alaska
Near Islands 1986 1,599 2 Skiff and shore survey, Attu Estes 1990a
Island only; Agattu Island unsurveyed

Rat Islands 1965 3,145 Aerial survey; presently may Kenyon 1969
support 14,420-20,650 otters (see text)

Andreanof Islands 1969 2,393 Aerial survey; population probably Sclmeider and Faro 1969*
much larger

Islands of 1982 69 2 Skiff survey; small colony Bailey and Trapp 1986'
Four Mountain established recently

Fox Islands 1986 858 3 Aerial survey Brueggeman et al. 1987'

Alaska Peninsula 1986 15,244 3 Aerial survey Brueggeman et al. 1987

Pribilofislands 1988 7 2 Occasional sightings; may be A. L. Sowls

wanderers from Bristol Bay (personal communication
to A. DeGange)

Kodiak archipelago 1985 2,811 2 Aerial survey Simon-Jackson et al. 1986*

Kenai Peninsula 1982 880 3 Aerial survey Schmidt 1983*

.·.·. Prince William 1984-85 4,747 3 Skiff survey within 200m of shore; Irons et al. 1988
Sound occasional offshore areas surveyed

... Northern Gulf of 1986 1,432 2 Aerial survey; all sightings between Simon-Jackson 1986*
Alaska Orca Inlet and Cape Suckling Simon-Jackson and
.. Hodges 1986*

:,.:. Southeast Alaska 1988 4,520 2 Skiff and shore surveys Pitcher 1987* and
unpublished data

British Columbia 1987 380 2 Aerial survey MacAskie 1987

Washington (State) 1989 211 2 Aerial, skiff, and shore surveys R. Jameson (personal
communication)

Central California 1989 1,864 3 Shore and aerial surveys R. Jameson and
J. &tes (unpublished data)

San Nicolas Island 1989 15-20 2 Shore surveys U.S. FISh and Wildlife
Service (unpublished data)
a Estimate.
• • . .r b I =at or near equilibrium; 2 =below equilibrium; 3 =unknown or uncertain population status .
 THE SEA OTTER: BEHA \IOR. EcoLOGY ..>.ND NATURAL HISTORY 75

calculation of rmax for sea otters. known. although all available data are summarized by
Sea otters occur throughout most of their historical Ratterman and Simon-Jackson ( 1988) and in Table 6. Sea
range from Prince William Sound west (Table 6). Al- otters probably are at or near equilibrium density through-
though the size of these populations is not precisely out the Aleutian archipelago. except for the western end
known, they may total more than 150.000 (Estes 1980: (Near Islands) and from the eastern Andreanof Islands
Johnson I 982; Calkins and Schneider 1985*: Ratterman through part of the Fox Islands. It is likely that the most
and Simon-Jackson 1988). Populations in the Kuril Is- recent survey data from the Rat and Andreanof islands
lands presently number an estimated 6.000-7.000 (Fig. 24) grossly underrepresented the size of these pop-
(Maminov, personal communication). Most of the avail- ulations. For example, 3.145 otters were counted in a
able habitat along the Kamchatka Peninsula also is occu- 1965 survey of the Rat Islands even though Estes ( 1990a)
pied and contains an estimated 2.500 otters estimated that Amchitka Island alone supports a popula-
(Khromovskikh, personal communication). In the Com- tion of 5.500-8.500 otters. Recent surveys of the Alaska
mander Islands, Medny Island contains 900-1,200 indi- Peninsula, Kodiak archipelago. Kenai Peninsula, north-
viduals, which are probably resource-limited. whereas em Gulf of Alaska, southeastern Alaska, and Prince Wil-
Bering Island has an estimated population of 1,500-1.800 liam Sound provided respective counts of 15,244, 2,811,
and is still increasing. Alaska populations are less well 880, 4,747. 1..+32, and 4.520 sea otters (Table 6).

\
Fig. 31. Large group of sea otters discovered at Bixby Creek cove in Big Sur. California. on 15 April 1938 (W. L. Morgan).
76 BIOLOGICAL REPORT 90 (14)

Status of the California Sea Otter Population 1969 * ; Wild I 973 * ). Most were aerial surveys of part or
all of the range, and some were supplemented with vari-
ous types of shore-based counts. Results of these surveys
Population Growth and Abundance (1914-1984) are summarized in Boolootian ( 1961 ), Carlisle (1966),
In 1914, the total California population was estimated Wild and Ames (1974), California Department of Fish
to be about 50 animals (California Department of Fish and and Game (1976 *), and Geibel and Miller (1984). From
Game 1976 *), after Bryant (1915) reported at least 32 otters 1980 to 1983, I 6 aerial surveys of the entire range were
observed near Point Sur. In 1938, a group of about 50 conducted (Bonnell 1982; Bonnell et a!. 1983*). Estes
otters was observed off Bixby Creek (Bolin 1938; Fig. 31 ), ( 1982 *) also conducted aerial surveys in I 981 and 1982.
at which time the population size was estimated at 100-150 Since different methods were used in these various sur-
(Fisher 1939) to 300 animals (Boolootian I 961; Califor- veys, it is not possible to determine population changes
nia Department ofFish and Game 1976 * ). The population from the data, except for general trends. Quality of the
was estimated to be approximate! y 1,000 animals by 1960 early data is particularly difficult to evaluate-to some
(California Department of Fish and Game 1976 *). extent, apparent population increases have probably re-
Periodic surveys of the California sea otter population sulted from improved methodology. In I 982, standard-
were conducted from 1958 to 1979, primarily by the ized survey methods, primarily involving shore-based
California Department of Fish and Game (Miller I 958*, counts, were adopted to eliminate this source of variation
1976 *; Carlisle 1965 * ; Wilson 1968a* , 1968b * ; Odemar from future counts.

Table 7. Results of 1982-89 shore-based California sea otter (Enhydra lutris) censuses of the entire range. These data
were cooperatively collected by the Fish and Wildlzfe Service and California Department of Fish and Game. Small
pups are <3 months. and large pups are ?:.3 months (Payne and Jameson 1984).
Number of
independent Number of Number of Total Total
Census otters small pups large pups pups otters
a a
!982 Spring !,124 222 !,346
Fall 1,!94 72 72 !44 I ,338

1983 Spring 1,153 56 66 122 1.275

Fall 1,062 94 70 164 1,226

1984 Spring 1,181 84 39 123 1,304

b b b b b
Fall

1985 Spring 1,124 144 92 236 1,360

Fall 1,066 74 81 !55 1,221

1986 Spring 1,345 128 97 225 1,570

Fall 1,088 59 54 113 1,201

1987 Spring 1,430 81 139 220 1,650

Fall 1,261 47 61 108 1,369

1988 Spring 1,505 136 83 219 1,724

b b b b b
Fall

1989 Spring 1,574 142 148 290 1,864

Fall 1,484 52 63 115 1,599
1990 Spring 1,464 130 84 214 1,678

a Not separated.
b Not surveyed.
 THE SEA OITER: BEHAVIOR. ECOLOGY, AND .'J"ATURAL HISTORY 77

The most recent method involves shore-based censuses seem to have declined slightly. The same pattern is evi-
of approximately 80% of the population, supplemented dent in changes in rate of increase in the number of otters
with aerial surveys of the remaining 20%. These surveys counted, although the magnitude of change is somewhat
have been conducted twice each year (in spring and fall) higher. indicating that density has declined within the
since 1982. Results to date (spring 1990) are summarized established range. Patterns of change in rate of increase
in Table 7. These data indicate a stable population through between sequential estimates are more variable, but they
about 1983-84 and then an increasing population from indicate a distinct reduction of growth during the last
the mid-1980's to the present, with the exception of a 10% several decades and a modest decline in numbers from the
decline in the total number of otters counted in the 1990 mid-1970's. These data indicate that the California sea
spring census compared to the 1989 spring census. The otter population has never increased more than about
reason for this decline is unknown; most of it occurred in 6-7% each year, at least during this century. At best, the
the center of the range between Mal paso Creek and Dolan California population has increased at an average rate of
Rock Uust south of Esalen). about half to one-third the 17-201} per year growth rate
To estimate the number of sea otters not seen during these of populations in Alaska (Estes, 1990a).
surveys, a calibration study was begun in 1984. The calibra-
tion was done by a double-counting technique in which two Range Expansion (1914-84) and Present
teams of observers simultaneously counted sea otters in Distribution
predetermined areas, otherwise using the same methods The range of the California population encompasses
employed during the rangewide surveys. These counts were approximately 353 km of coastline extending from near
replicated five times in each of six areas, and the proba- Afio Nuevo Point in San Mateo County to the Santa Maria
bility of sighting individual otters was estimated as P = River in San Luis Obispo County. :\1ost of the established
2A/2A + B, where A = the number of otters seen by both population-which includes the consistent presence of
teams and B = the number of otters seen only by either female and pup pairs or groups of three or more animals-
one ofthe teams. Data from this study indicate an average is centered between Afio Nuevo Point and the Santa Maria
probability of 0.945 that otters counted from shore will River. However, widely scattered individuals or pairs of
be sighted by a single team (Estes and Jameson 1988). otters occur north and south of these limits (Leatherwood
During the most recent survey (spring 1990), 1,464 et al. 1978). Temporal changes in distribution that have
independent sea otters (that is, all but dependent pups) occurred from 1914 to 1984 (Fig. 33; Table 8) indicate
were counted. When the correction factor of 0.945 is that the rate of range expansion to the south has been more
applied to this count, it provides an estimate of 1,549 rapid than that to the north (Lubina and Levin 1988).
independent otters. However, this is probably conserva- Lubina and Levin (1988) analyzed the historical data on
tive since aerial counts-which detect a lower proportion range expansion with a mathematical model incorporat-
of sea otters than do shore-based counts-were included ing population growth, diffusion. and advection. They
in the survey total. concluded that growth and diffusion largely account for
The number of pups in the population varies seasonally the observed patterns. Ames et al. (1983 ~) suggested that
and possibly among years, with actual pup counts ranging the rate of range expansion may be limited in part by
from 122 to 290. Pup abundance usually is highest in mortality from entanglement in shallow water set-net
spring, which reflects the peak pupping period of January fisheries, white shark attacks, and shooting.
to March (Estes and Jameson 1983a*, 1983b *). The ratio The northern peripheral group of males moved north-
of dependent pups to independent animals from 1982 to ward from Seaside (near Monterey) to Soquel Point (near
1990 during spring surveys varied form 10.4 to 21.0 pups Santa Cruz) in February 1977 (Estes and Jameson 1983a* ,
per 100 independent otters, averaging about 16:100. 1983b *). Before then, the male penpheral
. group at the
Population changes can be estimated from the data in northern end of the range was located along Cannery Row
Table 8. We based these calculations on estimated numbers off Hovden Cannery in Monterey (Loughlin 1977). In the
and lineal extent of range. For each of these data sets, we 1970's, sea otters were occasionally observed singly or in
made two series of calculations for average annual rate of pairs along the north coast between Santa Cruz and Afio
population change. The calculations in one series were based Nuevo Island; most sightings probably were of males,
on changes in estimated population size and range from 1914 although in one case, a female and pup were seen crossing
through each succeeding year for which estimates were the channel between Afio Nuevo Island and the mainland
made. The other series of calculations was based on each (Wilson et al. 1970-1976 *; Yellin et al. 1977 *; Riedman,
sequential pair of years for which data were available- unpublished data; F. Wendell, California Department of
for example, 1914 and 1938, 1938 and 1947, and so forth. Fish and Game, Morro Bay, personal communication).
From 1914 to 1984, the annual rate of increase in From 1980 to 1983, the abundance of otters between Afio
population size and range was about 5% (Fig. 32). Aver- Nuevo Island and Santa Cruz increased slightly. Most of
age rates of range increase, calculated from 1914 onward, these animals were centered at Sand Hill Bluff. where at
 -...1
Table 8. California sea otter (Enhydra lutris) population growth and range expansion, 1914-88 (updated from California Department of Fish and Game 1976 *, U.S. 00

Fish and Wildlife Service 1982).

a t::C
Limit Qf rang~ In~:reas~ in r!l!lg~ (km) A v~rage <Jnnual in~:reas~ (in km) Linear km Total estimated Total Years between 0
r
Year Northern Southern North South Total North South Total of range population counted estimates 0
Cl
n
>-
r
1914 Point Sur Pfeiffer Point - - - - - - (II )b (50)b - - 10
1938 Rocky Point Slate Hot Springs II 21 32 0.46 0.88 1.34 43 310 - 24 .,171
0
1947 Malpaso Creek Mill Creek 8 23 31 0.89 2.56 3.45 74 530 - 9
1950 Yankee Point (1951) Gorda 2 13 15 0.67 4.33 5.00 89 660 - 3
"'
--l
'D
0
1955 Point Lobos Ragged Point 3 16 19 0.60 3.20 3.80 100 800 - 5 .....
""""
south shore !;
1957 Pescadero Point Point Sierra Nevada II 6 17 5.50 3.00 8.50 125 880 - 2
1959 Point Joe Point Piedras Blancas 6 6 12 3.00 3.00 6.00 137 1,050 - 2
1963 Otter Point San Simeon 5 10 15 1.25 2.50 3.75 152 1,190 - 4
1966 Lover's Point Pico Creek 0 6 6 0.00 2.00 2.00 158 1,260 - 3
1969 Seaside Point Estero 6 13 19 2.00 4.33 6.33 177 1,390 - 3
1972 Seaside Cayucos Point 0 15 15 0.00 5.00 5.00 192 1,530 - 3
1973 Moss Landing Point Buchon 23 29 52 23.00 29.00 52.00 244 1,720
1974 Pajaro River Diablo Cove 6 5 II 6.00 5.00 11.00 255 I ,730
e
1975 Sunset State Beach Diablo Cove 8 0 8 8.00 0.00 8.00 263
1976 Rio Del Mar Pecho Rock 10 6 16 10.00 6.00 16.00 279 1,789c
c
1977 Soquel Point Point San Luis 8 6 14 8.00 6.00 14.00 293
e
1978 Soquel Point Point San Luis 0 0 0 0 0 0 293
1979 Soquel Point Sunset Palisades 0 6 6 0.00 6.00 6.00 299 1,443d
e
1980 Soquel Point Oceano 0 13 13 0.00 13.00 13.00 312 - I
e
1982 Soquel Point Oceano 0 0 0 0 0 0 312 1,338 2
e
1983 Sand Hill Bluff Santa Maria River 10 15 25 10 15 25 337 1,216 I
1984 Sand Hill Bluff Santa Maria River 0 0 0 0 0 0 337 1,372 I ,304 (USFWS) I
I ,203 (CDFG)
e
1985 Sand Hill Bluff Santa Maria River 0 0 0 0 0 0 337 1,360
e
1986 Sand Hill Bluff Santa Maria River 0 0 0 0 0 0 337 1,570
e
1987 Afio Nuevo Santa Maria River 16 0 16 16 0 16 353 1,650
e
1988 Afio Nuevo Santa Maria River 0 0 () 0 0 0 353 1,724

Totals 133 209 342 1.38 1.61 2.99 353 74

" Ground count initiated 1982.
b No records, rough assumptions made (see text).
" Some small pups included.
d Poor weather conditions during survey led to lack of confidence in final figure; also some large pups included.
c No estimates calculated.
 THE SEA OTTER: BEHAVIOR. EcoLOGY, AND NATURAL HISTORY 79

2000
1800
Q)
N 1600
·-
(J) 1400
c 1200
0
.....j-..J
1000
0 800
:::J
o_ 600
0 400
()_
200

1930 1950 1970 1990

Year
Fig. 32. Trends in the California sea otter population, 1914-88.

least one mother and pup pair was consistently observed ulation decline of79 otters from 1976 to 1982 in the area
(Bonnell et a!. 1983 *). In February 1984, a group of 19 between Diablo Canyon and Point San Luis, while there
otters containing 5 female and pup pairs was observed was a net increase of 16 otters south of Point San Luis.
near Sandhill Bluff (Ames and Hardy, unpublished data). The southernmost established group of otters, centered
During 1980-83, the size of the large male raft at Soquel in the Shell Beach to Oceano area, appears to be predom-
Point decreased (Bonnell et al. 1983 * ; Estes, unpublished inantly composed of males. Female and pup pairs have
data), and the abundance of otters occupying the eastern not been observed south of Shell Beach. A number of
Monterey Bay from La Selva Beach to Marina corre- otters, presumably males, were seen south of Oceano to
spondingly increased (Bonnell eta!. 1983\ A group of the Santa Maria River. Several otters, mostly single ani-
otters, presumably males, inhabited lower Elkhorn mals, have been sighted between the Santa Maria River
Slough and Moss Landing in winter of 1984. The size of and Point Conception from 1983 to the present (February
this group seems to fluctuate seasonally (K vitek and 1989; Bonnell eta!. 1983 *; California Department ofFish
Oliver 1988; Kvitek eta!. 1988), as does the male group and Game, unpublished data).
near Soquel Point (Estes, unpublished data), both reach- There have been recent changes in abundance through-
ing highest numbers in winter and spring. out the center of the range. From 1981 to 1983 the density
From 1977 to 1982, southward range expansion oc- of otters declined in the Monterey Bay area and along the
curred from Pecha Rock to Oceano (about 25 km); in Big Sur coast from Pfeiffer Point to Gamboa Point; cor-
1983-84, it expanded an additional 15 km from Oceano respondingly, density increased from Cypress Point to
Pmnt. Sur (Bonnell et a!. 1983 *; Estes and Jameson
south to the Santa Maria River (Figs. 33 and 34; Estes and
Jameson 1983b *). From 1973 to 1979, southern periph- 1983b*). Estes and Jameson ( 1983b*) reported an overall
eral groups of males occurred at Point B uchon and Diablo decline in numbers from Monterey Harbor to Diablo
Cove. In 1979, females began to occur in this area, which Canyon between 1976 and 1982.
at latest observations contained a lqw-density population Environmental Variables Affecting Distribution
of females, pups, and territorial males (Benech 1981 *; Patterns
Estes and Jameson 1983a* ; California Department of Fish Small-scale, local distribution patterns throughout
and Game and U.S. Fish and Wildlife Service, unpub- most of the range seem to be affected by weather and sea
I!.shed data). Estes and Jameson ( 1983b *) reported a pop- conditions, and especially by the abundance and distribu-
80 BIOLOGICAL REPORT 90 (14)

30'

37° 37°

30' 30'

1938

36° 1947

1959

1972

1975

35°

Pacific Ocean
30' 30'
Point
Conception

Fig. 33. Sea otter range expansion in California, 1938-89.

 THE SEA OTTER: BEHAVIOR, EcoLOGY, AND NATURAL HISTORY 81

Pigeon Point

Aria Nuevo Point

Fig. 34. Central California coastline,

indicating range of sea otter (hatched
areas) and areas referred to in text.

Pacific Ocean

tion of the kelp canopy, all of which vary seasonally. The ocean swell, at which time sea otter distribution becomes
location of protected rafting areas also influences sea more dense as the animals aggregate in the few available
otter distribution, especially during winter-spring periods kelp beds. The winter-spring reduction in kelp canopy
of high winds and rough seas (Sandegren et a!. 1973; may also increase male-male competition for suitable
Riedman 1984a* , 1984b * ; Jameson, unpublished data). territories, in part affecting the seasonal movement of
Sandegren et al. (1973) found that during prolonged pe- adult males from the center of the range (Jameson 1989).
riods of inclement weather or rough seas, mothers with In summer and fall, distribution becomes more dispersed,
pups moved to calmer, protected coves. In addition, pre- and otters may rest farther offshore, reflecting the sea-
liminary information suggests that rough seas, high sonal increase in kelp canopy abundance and offshore
winds, and heavy rain may cause a more dispersed distri- kelp distribution (Jameson 1989; VanBlaricom and Jame-
bution pattern by disrupting groups of resting otters in son, unpublished data).
California (Sandegren et al. 1973; Estes et al. 1986; Ried-
man, unpublished data) and in Alaska (Garshelis 1983).
Local distribution patterns of sea otters are correlated Demographic Variables Affecting Dynamics
with seasonal changes that occur jn the surface kelp of the California Population
canopy (Estes and Jameson 1983a ; Riedman 1984a ,
1984b*; Jameson 1989; VanBlaricom and Jameson, un- Population changes could be affected by three general
published data). In winter and early spring, the kelp factors: emigration, natality, and mortality. Each factor
canopy typically is substantially reduced; kelp that re- may vary with age and sex, and each may be affected by
mains is usually in areas protected from heavy seas and density-dependent and density-independent processes
82 BIOLOGICAL REPORT 90 (14)

(Estes 1981; U.S. Fish and Wildlife Service 1982; Ralls reasoned that juvenile females were at a competitlve
et al. 1983). disadvantage with other age and sex classes in foraging,
Extralimital occurrences of sea otters are relatively rare so they experienced a resulting higher rate of mortality.
and do not seem to constitute a significant level of emi- Consequently, food availability was probably limiting
gration. Over the past 30 years, extralimital sightings of further population growth because of the high reproduc-
sea otters have been made north of the established range tive value of juvenile females. The possibility also exists
as far as Tillamook Bay, Oregon (Pederson and Stout that density-dependent processes may be operating in the
1963), and Cape Mendocino, California (Orr and Poulter center of the range, where the population has been estab-
1964; Bonnell et al. 1983 *; Wendell, personal communi- lished for the longest time, while density-independent
cation), and as far south as central Baja California, Mex- factors may be affecting population growth at either end
ico (Leatherwood et a!. 1978; Estes, unpublished data; of the range, where the frequency of mortality due to
Wendell, personal communication). Because extralimital set-net fishing, shark attacks (northern periphery), and
sightings are infrequent (and in some cases probably shooting incidents (southern periphery) is highest (Ames
represent consecutive sightings of the same individual), eta!. 1983\
and since large numbers of otters are not seen concentrat- Sin iff and Ralls ( 1988b) found that half (8) of 19 sea
ing outside of the established range, it seems unlikely that otter pups born to radio-instrumented adult females in
substantial losses to the population have occurred through California survived to weaning. Similar data obtained by
emigration (Estes 1981; ·u.s. Fish and Wildlife Service Garshelis (1983) in Prince William Sound led S iniff and
1982). Ralls to suggest that early pup survival rate is lower in
Annual recruitment to the California population seems central California than in Alaska. This conclusion is fur-
to be comparable to that observed in Alaskan populations ther supported by the work of Monnett and Ratterman
(but see Estes 1990a). In both California and Alaska, ( 1988b · ), who found that. excluding human-caused
average proportions of 20-30 pups per 100 independent deaths, nearly 100% of the pups they studied in Prince
otters are found during censuses taken near the end of the William Sound survived from the time they were in-
pupping season; average proportions of 15-16 per 100 are strumented to the time they were weaned. These differ-
observed throughout the year, although rangewide cen- ences could account for the lower growth rate of the
suses conducted in California indicate that this ratio may California sea otter population compared with that in the
vary from year to year. Overall birth rates appear similar Aleutian Islands, Washington State, British Columbia,
in both populations (Estes 1981; Estes and J arne son and southeastern Alaska (Estes 1990a). It should be noted,
1983a*); therefore, the recent lack of growth (even possi- however, that Monnett and Ratterman ( 1988b * ) found
ble decline in numbers) shown by the California popula- pups to survive in Prince William Sound that were
tion probably is due to elevated mortality (Estes 1981 ). weaned only an estimated 2.5 months after birth. Heisey
Growth-limiting mortality of the California sea otter and Fuller (1985) developed methods for estimating an-
population may result from density-independent or den- nual survival from telemetry data; with these methods,
sity-dependent factors. Miller ( 1980) believed that the Siniff and Ralls ( 1988 *) estimated the following survival
California population was at equilibrium density and that rates for sea otters in California: adult females, 0.91; adult
starvation was the principal (density-dependent) limiting males, 0.67-0.71; juvenile females, 0.77-0.85; and juve-
factor. However, Estes et al. ( 1986) found that the propor- nile males, 0.86-0.88. Because these radio-tagged sea
tion of time allocated to foraging was indicative of pop- otters were also flipper-tagged, Siniff and Ralls (1988*)
ulations below equilibrium density in Alaska and Oregon. were able to estimate annual flipper tag survival to be 0.74.
Estes et al. ( 1986) believed this conclusion to be further They found, in addition, that significantly more of the
supported by the facts that (1) unoccupied habitat into radio-tagged otters lost both flipper tags than expected
which the population presumably could grow exists at from the single tag loss rate, indicating that individual sea
both ends of the present range, and (2) recent estimates otters have different tendencies to lose tags. Riedman.
of sea otter entanglement mortality in the coastal set-net Staedler, and Estes (unpublished data) have also found
fishery are 7-8% of the total population each year (Wen- individual variation in rate of tag loss among otters in the
dell et al. 1985 *). However, by using radiotelemetry, Ralls Monterey Bay area.
and Siniff (1988 * ) found that juvenile females in the Sea otter natural mortality outside California is known
central part of the range spent more time foraging and mainly from studies done in Prince William Sound (Gar-
experienced higher mortality than other age and sex . 1983; Monnett and Ratterman 1988b * ) and the
shehs
classes (except adult males, which had the lowest survival western Aleutian Islands (Kenyon 1969). Kenyon ( 1969)
rates). They believed these data were inconsistent with reported that as the sea otter population at Amchitka grew
the conclusion of Estes et al. ( 1986), thus implying that toward food limitation, starvation-related mortality in-
further growth in the California sea otter population was creased substantially. From carcasses found on the beach.
limited by food availability. Ralls and Siniff ( 1988 *) he determined that about 70% of these animals were
 THE SEA OTTER: BEHAVIOR, ECOLOGY, AND NATURAL HISTORY 83

juveniles, and that the sex ratio was biased toward males. lungs is the principal source of buoyancy (Kooyman
Few data are available from other populations because 1973). In addition, some sea otter carcasses have been
those that are probably food limited have not been stud- known to drift considerable distances; therefore, the area
ied, and carcasses from those that are below food limita- of recovery along the coast does not necessarily indicate
tion are seldom found on the shore. This is probably the area of death.
because individuals in populations that are not food lim- The proportion of dependent pups recorded is probably
ited rarely haul out, and because the mortality rate, espe- especially low relative to actual mortality, due to difficul-
cially among juveniles, is low. In their study of radio- ties associated with recovering small pup carcasses. Be-
tagged weanling sea otters, Monnett and Ratterman cause of the rapid rate of decomposition and the likeli-
(1988b *) showed that males and females died or disap- hood of sand and other debris obscuring them, dead pups
peared in nearly equal proportions. However, female are less conspicuous than adults when floating in kelp
losses were concentrated in January-April whereas male beds or lying on the beach. In addition, females some-
losses were more evenly distributed among the seasons. times care for dead pups for several days, further reducing
This pattern is different from the one reported by Ken- the likelihood of recovery (Ames et al. 1983).
yon ( 1969) at Amchitka Island. Unfortunately, whether Sea otter carcasses are recovered most frequently at the
food is an important limiting resource to sea otters in ends of the range (Fig. 35). Some possible explanations
Prince William Sound is unclear. Since the habitat there for this pattern inc! ude ( 1) systematic salvage efforts were
is very different from that at Amchitka Island (Prince not conducted in much of the center of the range until
William Sound consists mainly of soft-sediment benthos 1983; (2) the remoteness and low human population
and is protected from ocean swells, whereas Amchitka density in the center of the range result in few public
Island is a highly exposed, rocky benthos system), these reports of otter mortality; and (3) mortality may be com-
apparent differences in juvenile mortality patterns are paratively low in the center of the range.
hard to interpret. Monthly salvage efforts in the relatively isolated central
and southern portions of the range have resulted in in-
creased carcass recoveries in these areas (Jameson 1983 *,
1984* , Bodkin, personal communication) Information
collected during a study in the northern part of the range
Sources of Documented and Potential from March to August of 1984 showed that monthly
Mortality salvage efforts increased the number of carcasses re-
trieved in isolated areas but not in areas of high accessi-
bility or human population density (Riedman 1984c* ).
Documented Mortality Weekly salvage efforts conducted by the Fish and Wild-
life Service near Point Piedras Blancas have shown that
Introduction and Summary a sea otter carcass remains on the beach for an average of
The California Department of Fish and Game has in- 18 days, although there is considerable variation (maxi-
vestigated sea otter mortality in California since 1968. mum= 100 days; Bodkin, personal communication).
Ames et al. (1983 *) and Ames (unpublished data) sum- From 1968 to 1984, the number of sea otter carcasses
marized information on 1, 733 sea otters that died or were recovered generally increased (Table 9). However, the
otherwise removed from the population from 1968 to number of dead sea otters reported each year has also
1989. Percentage of the total mortality that is recovered increased over this period, along with an increase in
is unknown, and recovered animals undoubtedly repre- public awareness of the California Department of Fish
sent only a portion of the total sea otter mortality. and Game salvage program. After 1984, sea otter mortal-
Ames et al. ( 1983 *) pointed out that a number of vari- ity declined, probably because fewer otters were being
ables relating to temporal and spatial differences in car- drowned in gill and trammel nets. Gerrodette ( 1983 *)
cass recoverability and search effort must be considered reviewed sea otter salvage efforts conducted from 1968
when interpreting trends in these data. The following to 1983 and discussed inadequacies in the available data.
factors may influence the likelihood that a dead otter will The causes of death classified by California Depart-
wash ashore and be recovered: cause of death, wind ~nd ment of Fish and Game (CDFG) and the number and
current patterns, the presence and density of kelp cano- proportion of otters within each mortality category are
pies, location, age of the otter (pup versus independent presented .m Table 9. Ames et al. (1983 *) and Ames
animal), search effort, and public awareness of the sal- (unpublished data) provided a description of each mortal-
vage program. Recoverability may be influenced by ity category. Of the 1, 73 3 sea otters that died or were
cause of death (e.g., sea otters drowned at depth in gill otherwise removed from the California population from
nets tend to sink, but otters that are shot tend to float on 1968 to 1989, 53 were animals either accidentally killed
the surface). This is because normal air volume in the or captured for public display or research purposes. Of the
84 BIOLOGICAL REPORT 90 (14)

Fig. 35. California Department of Fish and

Game mortality recovery areas in central
California.

Pacific Ocean

remammg 1,680 recorded deaths, 933 (56%) died of quency of adult mortality often peaked in summer-fall.
unknown causes (CDFG mortality categories 1, 2, and 3). The winter-spring peak in pup mortality, which occurs
Many of these carcasses were badly decomposed. The during the peak pupping season, suggests that many fe-
cause of death was conclusively or probably determined males may lose their pups at a young age. Males predom-
in.402 (24%) of the cases (CDFG categories4, 5, 7, 8, 10, inated in the sample of small dead pups (<75 em total
11, 14, and 16). Mortality involving dependent pups length). Mortality of females and pups was generally
(categories 12, 13, and 15) represented 301 cases, or 18% higher in the center of the range (Point Pinos to Cambria),
of the total mortality.. while the proportion of male carcasses recovered was
Information on 1,027 dead sea otters collected from highest at either end of the range.
1968 to 1982 showed that when. sex, age, and state of The most significant sources of sea otter mortality in
decomposition were recorded, 525 (58%) were males and California seem to be ( 1) incidental drowning in commercial
386. (42%) were females; 525 (52%) were adults, 183 set nets, (2) white shark attacks, (3) a combination of condi-
(18%) were subadults, and 293 (29%) were pups; 607 tions related to pathological disorders, starvation, and ad-
(60%) were decomposed, and 402 (40%) were relatively verse winter weather, and (4) possible shooting incidents
fresh or in fair condition (Ames et al. 1983 *). occurring primarily in the southern part of the range.
Ames et al. (1983 *) documented the. followmg . trends
with respectto sea otter mortality. Monthly mortality data Mortality Caused Directly by Humans
W!;!re characterized by a· bimodal frequency distribution, Net Entanglement. Several kinds of evidence indicate
with mortality peaking in early spring (March-April) and that incidental drowning of sea ot~ers in gill and trammel
summer (June-August), The frequency of pup mortality nets may represent a significant source of mortality. From
almost always peaked in winter-spring, while the fre- June 1982 to January 1985, 29 otters were observed
Table 9. Causes of sea otter (Enhydra lutris) mortality, and the number and proportion of otters within each category, 1968-89. Modified from Ames et al. 1983*
and Ames, unpublished data.

Mortality
category Year Total Percenta
1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989
I. Unknown 3 II 16 4 9 20 II 23 38 32 43 28 57 42 22 3 21 14 13 II 9 12 452 26.9%
2. Uncertain with I 4 7 2 6 7 I 2 4 5 4 8 13 5 4 7 II 4 9 9 4 10 127 7.6%
trauma.
3. Uncertain with 2 8 2 5 10 3 2 18 II 6 28 46 32 48 29 12 28 23 25 354 21.1%
no trauma
4. Shark-bitten ~ 0 0 0 0 2 0 3 2 5 2 3 6 7 I 10 4 I 2 7 3 2 61 3.6%
5. Probably shark- 3 4 4 7 6 4 6 3 2 4 2 3 6 3 2 7 4 2 6 4 3 86 5.1%
bitten
6. Lacerated 2 2 6 6 6 6 I I 0 2 3 I 0 2 I 0 2 3 ~ 2~
7. Shot 5 .2 0 3 I 0 2 4 I I 3 5 5 3 6 6 3 9 3 ~ ~1%
8. Probably shot 0 3 0 0 I 0 0 0 I 0 0 0 0 0 0 0 0 0 0 8 US%
9. Research and 0 6 0 5 0 0 4 6 7 3 0 0 0 0 8 3 6 E
display
I 0. Other man-causes 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 4 2 0 II 0.7% ~
(entanglement in fii
(/l
fishing line)
I I. Other natural 0 0 2 0 2 4 0 2 0 7 2 3 6 2 7 2 4 8 9 63 3.7%
~
causes (patho- 0
logical disorders)
12. Dependent animal 4 3 3 0 3 13 II 7 7 17 9 8 26 30 16 20 24 5 II 17 4 249 14.8%
~
t:C
13. Dependent animal 0 2 () 4 6 3 0 0 2 0 4 2 0 2 0 0 0 0 0 28 1.7% ti1
with trauma
::r:
>
<:
14. Mating wounds 0 0 2 2 5 2 2 0 2 3 2 2 0 6 0 3 2 38 2.3% 0
in females ?'
15. Dead pups with 0 0 ·o 0 0 0 0 0 0 2 3 4 2 0 2 3 2 2 24 1.4% ~
mother ?l
0
16. Net-drownedb 0 0 0 0 0 0 0 0 0 0 0 0 6 6 16 12 3 5 5 II 66 3.9%
~
Total 16 36 52 21 49 82 44 52 64 99 81 69 147 153 99 118 132 70 80 91 86 92 1733 ~
0
z
;,-
Total (without re- 16 30 51 21 44 82 44 48 58 92 80 66 147 153 99 118 131 69 79 83 83 86 1680
search category 9) ;:!
a Using total without research category 9. ~
b Category 16, previously "immature females with bite wounds," was discontinued; these animals are included in Category 14. Category 16 now comprises net-drowned otters. ;;
~
~
...;

00
u.
86 BIOLOGICALREPORT90 (14)

Table 10. Estimates of incidental drowning of sea otters the monthly fishing effort (defined as the landing and sale
(Enhydra lutris) in gill and trammel nets, calculated of starry flounder [Platichthys stellatus] or California
from estimates of set-net effort 1973-83. (From Wendell halibut [Paralichthys californicus] by fishermen using
eta!. 1985 * ). entangling nets) with monthly fluctuations in numbers of
Number of Estimated number decomposed, independent otters that died of unknown
a
Year landings of dead sea otters causes and were recovered from areas close to intensive
set-net fishing. From 1979 to 1982, there was a high
1973 457 49 correlation (r = 0.88; P < 0.1) between the two variables;
1974 645 69
b that is, summer was the peak for both halibut set-net effort
1975 69
105
and mortality involving independent, decomposed otter
1976 980
1977 663 71 carcasses near intensive fishery areas. There was also a
1978 874 93 correlation in previous years, although the sample size of
1979 1,449 !54 dead otters was low in some areas during certain years.
1980 1,407 !50 Decomposed beach-cast sea otters were used in the
1981 1,578 168 analysis because evidence suggests that net-drowned ot-
1982 1,057 113 ters sink and remain underwater until decomposition
1983 696 73 gases accumulate (Ames, personal communication).
a Estimate of effort is based on the number of landings of set-net boats Ames et al. ( 1983) found that the frequency of beach-cast
within the sea otter range. Estimated take is based only on the rate of otter carcasses in fresh condition peaked in late winter,
take observed in 1983 and part of 1982. Therefore. the estimated number while the number of decomposed otter carcasses tended
of dead sea otters is only a rough approximation in years before 1982.
b No data. to peak in summer, when set-net fishing operations were
most intensive.
Although gill and trammel net fishing occurs through-
out the sea otter's range, the principal set-net commercial
fisheries-starry flounder and California halibut-are
drowned (or otherwise known to have drowned) in com- situated in sandy-bottom areas at both ends of the sea
mercial fishing nets: 6 in 1982, 6 in 1983, 16 in 1984, and otter's range: in Monterey Bay and in the Morro Bay and
1 in 1985 (to January 5; Ames et al. 1983 *; Bishop 1983 *, Avila Beach areas (Fig. 34). Monofilament and multifil-
1984*; Croll and Keating 1983 * ; Wendell et al. 1985 *). ament nylon set nets have incidentally caught and
However, only a small proportion of the set-net fishing drowned thousands of diving marine birds and numer-
effort within the sea otter's range was sampled for sea ous marine mammals, especially in the early 1980's in
otter mortality. For example, 3% of the halibut set-net the Monterey Bay area (Croll and Keating 1983 *). Before
effort in 1982 was sampled for recovery of dead otters 1979, the gill net fishery in Monterey operated at a fairly
(Ames et al. 1983*), 10% was sampled in 1983, and 15% low level, with about five boats fishing in the bay each
was sampled in 1984 (California Department ofFish and year. In the early 1980's, set-net fishing operations in-
Game, unpublished data). Therefore, the actual frequency creased to include about 18-26 commercial fishing boats
of net-entanglement mortality for the California popula- per year (Croll and Keating 1983 *; Wendell et a!.
tion was presumed to be substantially higher than indi- 1985\ set-net fishing activity subsequently declined
cated by the confirmed observations of drownings. Ex- to about 8-10 commercial fishing boats per year (Hardy.
trapolations from the number of otters observed drowned personal communication).
and the proportion of the set-net fishery sampled indicated Because many sea otters were suspected of being
that from June 1982 to June 1984, an average of 80 sea drowned in gill nets-and since it is difficult to positively
otters drowned in gill and trammel nets each year (Wen- determine that drowning was the cause of death, even in
dell et al. 1985*). Wendell et al. (1985*) attempted to fresh carcasses (e.g., Yagil et al. 1983)-a number of
estimate annual entanglement mortalities between 1973 observer programs were implemented to monitor inciden-
and 1983 and found that they may have ranged from 49 tal take of sea otters in set nets. In the Monterey Bay.
to 168 otters per year (Table 10). However, the estimates observations of gill and trammel net fishing operations
before 1982 were based on a rough approximation of set- were conducted by the California Department of Fish and
net fishing effort as well as uncertain changes in the Game (CDFG) in 1980 and by students of both CDFG and
distribution of otters and fishing activity that varied from Moss Landing Marine Laboratories in 1981 and 1982
year to year (Hardy, personal communication). (Croll and Keating 1983). CDFG has maintained an ob-
An analysis of set-net effort and temporal and spatial server program in Monterey since 1983 (C. Haugen.
aspects of sea otter mortality also supports the idea that a California Department of Fish and Game, Monterey,
significant proportion of otter mortality is associated with Calif., personal communication). The Morro Bay and Port
commercial set-net fishing. Ames et al. ( 1983) compared San Luis set-net fisheries have been monitored since 1982
 THE SEA OrrER: BEHAVIOR. EcoLOGY. AND NATURAL HISTORY 87

*
(Bishop 1983,1984; * CaliforniaDepartmentofFishand ing was responsible for a greater proportion of mortality
Game, unpublished data). Direct observations of entan- in the southern part of the range. From 1968 to 1983.
glement mortality are made from shore through tele- about 9% of the sea otter carcasses found south of Cam-
scopes or at sea from small boats stationed close to the bria had been shot, while 2% of those recorded north of
fishing boats. Observers record the number of sea otters Cambria had been shot (Ames et al. 1983 *). Ames et al.
caught during each occurrence of net pulling; they also ( 1983 *) suggest that shooting incidents occurring near the
record the number of birds, fish, and other marine mammals southern edge of the range may tend to curb southward
and the depth, location, and estimated net length. emigration of sea otters.
The use of large mesh set nets in Monterey Bay was Collisions with Boats and Propeller Injuries. Mortality
prohibited within the 10-fathom (18-m) isobath (depth associated with laceration and trauma resulting from col-
contour) by California law in 1982; use was restricted lision with boats and contact with propeller blades seems
from water <15 fathoms (27m) in spring 1984. Since the to be negligible. Propeller injuries have been suspected
15-fathom closure, fewer sea otters have been drowned of causing significant mortality associated with lacerated
in gill or trammel nets in the Monterey Bay area. In late carcasses (e.g., Wild and Ames 1974; Morejohn et al.
January 1985, a temporary emergency closure prohibited 1975). However, subsequent reexamination of mortality
the use of entangling fishing nets (with mesh >3 inches) records revealed that most cases thought to be propeller
within the 15-fathom isobath from Monterey to the mouth injuries were actually attributable to white shark bites,
of the Santa Maria River. On 24 May 1985, the governor and that boat collisions and propeller injuries were rare
of California signed into law a similar closure to gill and (Morejohn et al. 1975; Ames and Morejohn 1980; Ames
trammel net fishing (with net mesh ~3.5 inches). et al. 1983 *).
Hardy (personal communication) estimated that the Only one incident has been documented in which a sea
effect of the 1985 closure was to reduce net entanglement otter was known to have been injured by a boat propeller:
by about 50%; in 1982-84, an estimated 80 otters In 1970, a small salmon boat (powered by a 65-hp out-
drowned each year in gill and trammel nets, but since board engine) traveling at full speed struck an otter just
1985, the yearly number of net-drowned otters declined beyond Monterey Harbor. Although the otter was not
to an estimated 3~0. Ten otters were observed drowned retrieved, a considerable amount of blood was observed
in gill nets throughout the range between 1 February 1985 in the water. A beached, lacerated otter was found two
and 1 April 1986. All but one of the net drownings days later in the vicinity of the incident and died a week
occurred in the southern and central parts of the range later (Ames and Morejohn 1980).
(south of Point Sur), especially in the area between Cape The definitive criteria for diagnosing boat propeller
San Martin and San Simeon Point; this area was subse- lacerations are unclear, but preliminary information (de-
quently closed to 20 fathoms. In addition, only 69 otter rived from a California Department of Fish and Game
mortalities were recorded in 1985; this represents a de- experiment in which two sea otter carcasses were inten-
cline from the 131 otters recorded in 1984 (Ames, unpub- tionally struck by a vessel traveling at full speed) indi-
lished data). cated that one carcass sustained two parallel lacerations
The importance of entanglement mortality to other sea preceded by a distinctive shaved area, while the other
otter populations is largely unknown, although various carcass was evidently destroyed (Ames and Morejohn
nets and traps that are probably capable of entangling and 1980).
killing sea otters are used throughout much of the species' Entanglement in Fishing Lines. Sea otter mortality
range. Significant numbers of sea otters seem to be lost from entanglement in fishing lines with and without fish-
to fishing gear in Prince William Sound and the nearby ing hooks is extremely rare. From 1968 to 1989, only 11
Copper River Delta (Simon-Jackson and Ratterman (0.7%) of 1,680 otters died after becoming entangled in
1987; Monnett and Ratterman 1988b*). fishing lines (Ames, unpublished data).
Shooting. About 4.6% (77 of 1,680) of the recorded sea Accidental Mortality Associated with Field Research
otter mortalities from 1968 to 1989 was attributed to Operations and Capture for Public Displays. This Cali-
known or probable instances of shooting (Mattison and fornia Department of Fish and Game mortality category
Hubbard 1969 *; Wild and Ames 1974; Morejohn et al. (9) includes all sea otters that incidentally died as a result
1975; Ames et al. 1983*; Ames, unpublished data). Cases of field research and capture operations, as well as those
of shooting can be conclusively determined by the pres- removed from the population for actual public display or
ence of visible bullet wounds or \
by X-ray photography, research purposes (some of which are still alive). Two
which allows the detection of bullets, shotgun pellets, or otters that drowned in entangling nets set by researchers
fragments of bullets. to sample fish (near Point Piedras Blancas and Moss
Each year the recorded number of sea otters that died Landing) were included within another mortality cate-
from being shot ranged from 0 to 9 animals and showed gory (16), encompassing all sea otters drowned in com-
no clear pattern of increase or decrease. However, shoot- mercial fishing nets (Ames eta!. 1983\ A total of 53 of
 88 BIOLOGICAL REPORT 90 (14)

1,680 otters (3% of the total otters lost) either died or were species (particularly elephant seals) over the past 20-30
placed in captivity for research, rehabilitation, or public years (Ainley et al. 1981, 1985; McCosker 1981; Le
display (Ames et aL 1983 *; Ames, unpublished . data). Boeuf et a!. 1982). Sea otter remains have not been
discovered in white shark stomachs. although few sharks
Natural Mortality have been caught or examined from within the sea otter's
Predation by White Sharks. White sharks occur in tem- range (Klimley 1985). Furthermore, it seems unlikely that
perate coastal waters worldwide. On the west coast of sea otters have the agility or speed necessary to escape an
North America, the species is known from Washington to attacking white shark, as some pinnipeds might (Ainley
Baja California, with large individuals in nearshore wa- et al. 1985). Therefore, the large number of otter carcasses
ters seeming to be most abundant in central and northern sustaining shark bites may represent animals that the
California (Klimley 1985). Large white sharks(> 3m total shark mistook for another prey species, such as harbor
length) attack and feed on marine mammals (Tricas and seals. and chose not to consume after the initial attack.
McCosker 1984; Klimley 1985). Recent increases in According to McCosker ( 1981, 1985) and Tricas and
white shark attacks on pinnipeds (Ainley et al. 1985) and McCosker (1984 ), the attack strategy of white sharks is
humans (Lea and Miller 1985) in California and Oregon to severely lacerate their prey during a single, initial hit.
have caused some people to speculate that shark popula- then to return and eat it after the prey has bled to death.
tions also have increased, probably in response to grow- Based on the wounding patterns of humans (Miller and
ing pinniped populations. However, Lea and Miller Collier 1980), pinnipeds (Ainley eta!. 1985), and small
( 1985) and Klimley ( 1985) pointed out that these patterns cetaceans (Arnold 1972), white sharks usually attack
may well have been caused by increasing numbers of marine mammals from beneath their posteriors. This
people and pinnipeds in coastal waters, regardless of any strategy seems to minimize risk of injury to the shark, that
change in size of the shark population. might be incurred in a struggle with the large, powerful
Attacks on sea otters by white sharks may represent a animals on which they typically prey. In view of the
significant source of natural mortality in the California extensive tissue damage often inflicted on large-sized
population. Sea otter carcasses with definitive white pinnipeds (LeBoeuf eta!. 1982), it is peculiar that shark-
shark bites have been documented since 1959 (Orr 1959; bite injuries on sea otter carcasses are comparatively
Wild and Ames 1974; Morejohn et aL 1975; Ames and mild, which also suggests that white sharks often do not
Morejohn 1980; Ames eta!. 1983 *) and probably have follow through after initial attacks on sea otters. It may
occurred throughout the historical association of the two also be that the comparatively small mass of a sea otter
species. Ames (unpublished data) attributed about 12% has insufficient static inertia for a shark to work against.
(195 of 1,680 otter deaths) of the recorded mortality from in effect causing an attacked otter to be knocked aside
1968 to 1989 to white shark attacks; 61 of the carcasses rather than sliced apart.
were definitely shark-bitten, 86 were probably shark- Although shark-bitten sea otters in California have been
bitten, and 48 were lacerated. Ames and Morejohn ( 1980) found throughout their range, the highest proportion of
determined that white shark bites seemed to be responsi- shark-bitten carcasses are recovered north of Point Sur,
·. ble for 9-15% of all recorded mortalities in California especially in the Monterey peninsula area. Between Cy-
from 1968 to 1979. press Point and Point Pinos, for instance (Fig. 35), 36%
The frequency of white shark attacks on sea otters could of the otter mortality from 1968 to 1983 (including all
be higher than the number of definite or probable shark- undiagnosed, lacerated carcasses) may have been due to
bitten, beach-cast otter carcasses if many of the badly white shark attack (Ames and Morejohn 1980; Ames et
decomposed carcasses that were not examined were al. 1983 *). This pattern is consistent with the distribution
shark-bitten. Moreover, it is unknown if white sharks of white shark attacks on humans (Lea and Miller 1985)
regularly prey on sea otters, nor is it known whether they and pinnipeds (Klimley 1985), most of which have been
actually consume many otters following an attack. If so, reported north of Point Sur. Klimley (1985) speculated
the proportion of otter mortality from shark attack would that the number of pinnipeds in this area attracts large
be still higher. Because of the relative size of the two white sharks to the nearshore environment.
species, and the fact that surface shark attacks typically Shark-bitten and lacerated sea otter carcasses have been
involve jaw protrusions that produce a large mouth gape observed throughout the year, although they have been
(Tricas 1985), sea otters could easily be consumed with- recovered most frequently in late winter and spring and
out leaving any remains. least frequently in fall (Ames and Morejohn 1980; Ames
Several lines of evidence, however, suggest that white et al. 1983 * ). In comparison, at Aiio Nuevo (LeBoeuf et
sharks prefer to prey on pinnipeds, such as northern al. 1982) and the Farallon Islands (Ainley et al. 1985),
elephant seals and harbor seals, and that the apparent most shark-bitten northern elephant seals were observed
increase in white shark attacks along the California coast in late fall and winter. Ainley et al. ( 1985) further reported
is related to increases in abundance of these pinniped that white shark attacks on harbor seals at a coastal site in
 THE SEA OrrER: BEHAVIOR. EcoLOGY. AND NATURAL HISTORY 89

the Gulf of the Farallones were most frequent during doned by their mothers-however. this is unlikely, since
spring and summer, from which they speculated that adult female sea otters are highly attentive to, and rarely
sharks may make inshore-offshore movements in re- become separated from, their newborn pups. Further-
sponse to seasonal availabilities of the relatively vulner- more, several pup captures have been observed, and in
able pups of the pinnipeds. These observations suggested each instance the pup was taken while its mother was
that the increased occurrence of shark-bitten sea otters in diving for food. Often the pups vocalize loudly while their
late winter and spring may be caused by the seasonal mothers are diving, and bald eagles that prey on sea otter
movement of sharks towards shore in search of young pups may cue on this stimulus.
phocid seals, for which the sea otters are perhaps mis- Monnett and Ratterman (1988b \ working in north-
taken. Although the annual number of shark-bitten sea eastern Prince William Sound, reported that newly
otter carcasses observed from 1968 to 1982 has varied weaned sea otters were killed and eaten by coyotes. The
from year to year (Ames et a!. 1983), shark attacks on presence of fresh blood at the kill site suggests that (as
elephant seals north of the sea otter's range near Afio with the bald eagle) these otters were killed rather than
Nuevo and the Farallon Islands have increased since the scavenged. The tidal range in Prince William Sound is
mid-1970's along with the increasing abundance of pin- extreme, and Monnett and Ratterman (1988b) speculated
niped populations in these areas (Ainley eta!. 1981, 1985; that after hauling out at high tide, the otters became
LeBoeuf eta!. 1982). separated from the water as the tide receded, so that their
Predation by Other Predators. There have been other awkwardness on land made them easy prey for the coy-
documented cases of predation on sea otters, although otes.
such interactions may often go unnoticed because most A final example of predation on sea otters is by brown
of the species' range is remote and poorly studied. Al- bears on the Kamchatka Peninsula (A. Zorin, personal
though a Soviet biologist (Nikolaev 1965) observed a communication). Zorin reported that numerous otters are
killer whale (Orcinus orca) capture one sea otter in the captured and eaten by the bears in late winter to early
Soviet Union, this type of predation is probably very rare spring, when many otters appear to haul out in a weakened
(Kenya 1969, 1982). On several occasions, Kenyon condition from winter storms, and when hungry bears are
( 1969) observed killer whales swimming within a few emerging from hibernation.
meters of resting or feeding sea otters; the whales never Pathological Disorders. About +% (63 of 1,680 otter
attacked an otter, although active or foraging otters some- deaths) of the total recorded in California mortality was
times became inactive or lay still on the surface until the directly related to disease conditions, particularly enteri-
whale passed. Sherrod eta!. (1975) found that bald eagles tis and pneumonia. Enteritis, or inflammation of the in-
captured and consumed newly born sea otter pups at testinal tract, is common in necropsied sea otters in Cali-
Amchitka Island, Alaska (also discussed in Maternal Care fornia (Mattison and Hubbard 1969; Morejohn et a!.
and Pup Development). Amchitka Island supports high- 1975; Ames eta!. 1983 *), as well as in Alaska (Kenyon
density populations of sea otters and bald eagles, both of 1969). The presence of enteritis is associated with other
which probably were food-limited at the time of the diseases, poisoning, and various types of stress (Stulken
Sherrod et a!. (1975) study. Prey captures were deter- and Kirkpatrick 1955).
mined by examining food remains in eagle nests during Other fairly uncommon direct or contributing causes of
the birds' breeding season, which coincides with the death include perforated intestine, twisted intestine, in-
seasonal peak in sea otter pupping. Apparently, only tussusception (an unfolding of one part of the intestine
certain breeding pairs or individual eagles prey on sea into another), intestinal infection, stomach ulcers, pro-
otter pups, as the distribution of otter remains among nest lapsed uterus, prolapsed vagina, prolapsed rectum, acute
sites was strongly skewed toward some of the nests, and hepatitis, diaphragmatic hernia, valley fever, aspergillo-
pup remains were never found in about half of the nests. sis in the liver, severe peritonitis (inflammation of the
The consumption of otter pups by bald eagles was known membrane lining the abdominal cavity and enclosing the
to occur from earlier studies, although Kenyon ( 1969) viscera), and one case of twin fetuses lodged in the birth
presumed that the otter pups had been scavenged by canal (Morejohn eta!. 1975; Williams eta!. 1980; Ames
eagles following some other cause of death. In fact, this et a!. 1983 *).
may have been true in some cases; however, hemorrhagic Heavy infestations of acanthocephalan parasites (such
tissue around talon puncture wounds in several closely as Polymorphus) in the gastrointestinal tract are rare, but
examined fresh otter carcasses demonstrated that these may occasionally contribute to mortality from resulting
individuals were killed by the e'agles. In addition, since intestinal perforations. However, nonlethal cases of gas-
newborn dead pups were rarely found during beach sur- trointestinal tract parasites are common among sea otters
veys, Sherrod et a!. ( 1975) concluded that most of the in California (Mattison and Hubbard 1969 *; Hennessey
otter pups found in eagle nests probably were not scav- 1972; Wild and Ames 1974; Morejohn et a!. 1975;
enged. It is also possible that eagles captured pups aban- Hennessey and Morejohn 1977; Hennessey eta!. 1979 *;
90 BIOLOGICAL REPORT 90 (14)

Ames eta!. 1983 *) and in Alaska (Rausch 1953; Kenyon increased during periods of winter storms, and that
1969; Dailey and Brownell 1972; Margolis and Dailey human-caused mortality peaked during summer when
1972 *). Nasal mite (Halarachnidae) infections occur in- human activity, including gill-net fishing, was greatest
frequently in Alaskan otters; the few observed infesta- along the coast.
tions were mild and did not affect the health of wild otters, Mating Wounds in Adult Females. During copulation.
although severe nasal mite infestations may have contrib- the male grasps the female's nose between his teeth.
uted to the death of captive sea otters (Kenyon et. a!. 1965; causing nasal and facial injuries and scars that are fre-
Kenyon 1969). quently observed in live adult female otters (Vandevere
One case of systemic coccidioidomycosis (a respiratory 1970 *; Foott 1971; Brosseau et a!. 1975). Severe or in-
disease) has been reported as a cause of death in one sea fected nose wounds have been reported in carcasses of
otter near Morro Bay (Cornell eta!. 1979). Williams and adult females (Mattison and Hubbard 1969 *; Wild and
Pulley (1981) found uterine leiomyomas (a rare, benign, Ames 197 4: Ames eta!. 1983\ Although records of nose
smooth muscle tumor) in 2 of 112 female sea otters injuries in female carcasses are incomplete, mating
necropsied in California. wounds do not seem to represent a significant source of
Starvation. Many of the pathological disorders or un- mortality. Severe nasal damage was recorded from 1968
known causes of death included in CDFG mortality cat- to 1989 for at least 38 dead females (2.3% of the total
egories 1 (case of death unknown), 3 (uncertain with no mortality); of these, about half appear to have died as a
trauma), and 11 (other natural causes)-which collec- direct result of injuries incurred during mating. Ames et
tively account for 52% (869 of 1,680) of the total recorded al. (1983 * ) and Jameson (personal communication) sug-
mortality-are observed in conjunction with an emaci- gested that complications and infections stemming from
ated condition indicative of starvation. However, it is mating bite trauma may be a contributing cause of death
difficult to determine if the emaciated condition of the in a some females, and they speculate that very young,
carcass resulted from ( 1) insufficient availability of food very old, and unhealthy females may be especially sus-
resources, (2) the inability of a diseased otter to forage ceptible, not only to severe nose damage but also to
adequately, (3) the inability of mother and pup pairs, drowning resulting from vigorous breeding activity. On
juveniles, or aged animals to forage successfully (espe- two occasions, the same territorial male was observed
cially during harsh weather conditions); or (4) whether mating with the carcass of an adult female; it was known
diseases such as enteritis and pneumonia partially re- that he killed one of the females during mating activity,
sulted from a previously weakened condition caused by and he may have killed the other female as well (Riedman,
. (Ames et al. 1983 *).
starvatwn Staedler, and Estes, unpublished data).
From the evidence, many small and large dependent At least 10 immature female carcasses (about 1% of the
pups (included under CDFG mortality category 12: de- total recorded mortality from 1968 to 1983), measuring
pendent animals with no trauma) died of starvation. 90-105 em total length, sustained severe bite injuries,
About 15% (249 of 1,680 otter deaths) of the total re- particularly on the nose and feet. Similar sorts of wounds
corded mortality from 1968 to 1989 was composed of pup were found on some juvenile female carcasses measuring
carcasses showing no signs of trauma (Ames et al. 1983 ; <90 em, but these females were placed in CDFG mortality
Ames, unpublished data). Starvation might occur if the category 13 (dependent animal with trauma; Ames et al.
pup became separated from its mother or if the mother did 1983 *). It is possible that most of the severe bite injuries
not provide sufficient nourishment in terms of milk or on young females resulted from males attempting copu-
solid food obtained while foraging. According to Ames et lation. Jameson (personal communication) suggested that
al. ( 1983 *) harsh weather conditions are likely to promote it may be the younger. sexually immature males that
instances of mortality involving starvation. inflict most of the injuries.
.
Adverse Weather Conditions. Ames et al. ( 1983 *) found Fight Injuries in Males. Potential mortality resulting
that the number of emaciated carcasses recovered show- from injuries incurred during male-male aggression
ing increased indications that starvation contributed to seems to be negligible. Although overt fights between
death (whether the primary cause or secondary effect) males are rarely observed (Loughlin 1977, 1980), at least
increased during the winter period of severe storms. There 20 male carcasses examined from 1968 to 1982 sustained
was a positive correlation between rough sea conditions, severe fresh or old fight injuries. Most of the injuries were
the winter peak in mortality (other than human-caused), found on the hind feet, but occasionally wounds were on
and the proportion of recovered emaciated carcasses and the nose, face, and penis. Fighting injuries were observed
otters that died from unknown causes. .
more frequently molder males (Ames eta!. 1983 *). Ames
Thus, rather than chronically occurring throughout et al. (1983 *) suspected that complications from fight
the year, starvation appears to be associated with in- trauma (included within category 11) were the probable
clement winter weather. Morejohn et al. (1975) also cause of death for some of the males that sustained
found that sea otter mortality (not caused by humans) injuries during aggressive interactions.
 THE SEA 0TIER: BEHAVIOR, ECOLOGY, Al\D NATURAL HISTORY 91

Potential or Undocumented Sources of From 1968 to 1980, California sea otter tissue samples
Mortality or Pathological Disorders were analyzed for residues of chlorinated hydrocarbons.
heavy metals, and other elements by Shaw (1971), Rote
(1976), Martin (1979\ and the California Department of
Potential Reduction of Genetic Diversity in the Fish and Game's Fish and Wildlife Water Pollution Con-
California Sea Otter Population trol Laboratory. There was no evidence of a detrimental
Any population that has been reduced to a small size cause-and-effect relation between any environmental
may lose some of its natural genetic variability and thus, toxicant and mortality or pathological condition in sea
some adaptability (e.g., Denniston 1978). The sea otter otters, with the possible exception of potentially harmful
population along the Pacific coast of the United States levels of naturally occurring cadmium found in tissues of
was reduced to an estimated 50 animals in 1914 (Bryant several old females (Ames et al. 1983 *; Risebrough
* ~
1915; California Department of Fish and Game 1976\ 1984 ). The residue levels of heavy metals, polychlori-
this created a potential "genetic bottleneck." However, nated biphenyls, and organochlorine pesticides in sea
theoretical analysis indicated that significant loss of ge- otter tissues generally appeared to be below levels known
netic variation in the California sea otter population is to be the principal cause of debilitation or mortality,
unlikely (Ralls et al. 1983), and the population has sub- although PCB residues in a number of liver samples were
sequently increased to about 1,700 independent animals higher than levels known to cause reproductive failure in
(Estes and Jameson 1983a*, 1983b *; California Depart- mmk. (Ames et al. 1983 *; R1sebrough 1984*). However,
0

ment of Fish and Game and U.S. Fish and Wildlife Ser- few tissue samples of sea otters that died after 1980 have
vice, unpublished data). A reduction in genetic diversity been analyzed to determine levels of environmental con-
may occur in small populations by inbreeding and genetic taminants, because such contaminants in mussels within
drift, frequently leading to increased homozygosity, the sea otter range have been routinely monitored since
which in tum may result in reduced fertility, higher mor- then by the California Department of Fish and Game's
tality of young, and a decreased ability of offspring to (CDFG) State Mussel Watch Program.
adapt to changing environmental conditions (Kimura and Based on data collected by Shaw (1971), Rote (1976),
Crow 1963; Crow and Kimura 1970; Cavalli-Sforza and Martin (1979 *), and the CDFG Fish and Wildlife Water
Bodmer 1971; Packer 1979). Pollution Control Laboratory, Ames et al. (1983*) con-
Ralls et al. (1983) calculated that the current California cluded that there were some significant relations between
sea otter population should theoretically retain a signifi- sea otters and residue levels of environmental contami-
cant proportion (minimum of 77%) of the genetic diver- nants in their tissues. Temporal variation in the levels of
sity that occurred in the original population. Lidicker and pesticide residues (DDT, DDD, and DDE), which accu-
McCollum ( 1981 *) investigated genetic biochemical mulates primarily in fat tissues, indicated that residues
variation in sea otters from California, as well as Alaska, were lowest among otters that died between May and
and found 16.7% polymorphisms among 30 loci and a August and highest in otters that died between January
mean heterozygosity of 6.0%. No rare alleles were de- and April. The higher levels of pesticide residues found
tected. No fixed differences were found between the in otters that died in winter may be caused by agricultural
Alaska and California specimens, although the sample runoff, which is heaviest during rainy winter months. No
size from Alaska was too small to conclusively establish significant differences in pesticide accumulation patterns
differences between the two populations. Lidicker and were found in relation to sex or size of the otters.
McCollum (1981 *) concluded that the only effect of the However, variation in accumulation patterns of heavy
genetic bottleneck in the California population was the metals and trace elements in the liver and kidneys were
loss of rare alleles at variable loci. found in relation to sex and size of the otter. The amount
of cadmium, copper, iron, mercury, and zinc residues in
Environmental Contaminants the liver or kidneys increased with sea otter size or were
Adverse effects on sea otters from environmental toxi- higher in animals > 100 em total length, while the level of
cants have not yet been documented, although variable magnesium and silver residues in the liver were higher in
residue levels of a number of polychlorinated biphenyls otters measuring < 100 em. The levels of cadmium, man-
(PCB 's), chlorinated hydrocarbons (DDT and its deriva- ganese, and silver in the liver or kidneys were highest in
tives), and heavy metals have been found in sea otter females, and levels of iron and mercury in the kidneys
tissue samples. Because eqvironmental contaminants were highest in males. Silver and calcium residues in the
(e.g., organochlorine pesticides and some heavy metals) liver were higher in otters that died before 1974. Mean
exhibit biomagnification as they progress through the levels of calcium residues in the liver consistently de-
food chain (Keith 1966; Meeks 1968), top-level predators creased over time. Ames et al. (1983*) and Risebrough
such as sea otters may accumulate high and potentially (1984 *) noted that different methodologies employed by
toxic residue levels of such contaminants. the various laboratories in analyzing sea otter tissue sam-
92 BIOLOGICAL REPORT 90 (14)

pies may have affected some of the resultant conclusions concentrations of complex hydrocarbon mixtures (princi-
suggested by the collective data between residue levels pally petroleum) in mussels were the lowest in the State
and sea otter size, sex, and time of year. and were equaled only by locations on the open coast of
Smith eta!. (1990) evaluated postindustrial lead accu- northern California; concentrations in San Francisco Bay
mulation in sea otters at Amchitka Island by comparing and Los Angeles Harbor averaged 20-30 times greater
lead concentrations and isotopic compositions in teeth (Martin and Stephenson 1984). However, in Monterey
collected from the modem population and preindustrial Bay very high concentrations of some metals and pesti-
middens. Although lead concentrations in the North Pa- cides have been detected. Unusually elevated concentra-
cific Ocean have increased 5- to 15-fold since preindus- tions of lead and zinc, for example, have been found
trial times, there was no detectable difference in lead between Point Pinos and Monterey Harbor-lead concen-
concentration between preindustrial and modem sea otter trations were 22 times those of ambient levels elsewhere
teeth, perhaps because of lead biodepletion with in- in the range (Martin and Castle 1984). While the source
creased trophic status in marine food webs. However, lead of the contaminants has not been identified, it is believed
isotope analysis indicated that preindustrial animals con- to be leachate from waste dumps associated with histori-
tained lead derived from natural deposits in the Aleutian cal cannery activity (Loehr and Collias 1983). In addition.
arc, whereas contemporary animals contained primarily very high levels (about one part per million) of tributyltin
industrial lead from Asia and western Canada. (a toxic marine paint used on the bottom of vessels) were
The level of cadmium residues found in sea otter tissues found in the livers of two sea otters that were found dead
were high compared to other marine mammals. Cadmium in Monterey Harbor (M. Martin, California Department
accumulated with age, especially in the kidneys. Old of Fish and Game, Monterey, Calif., personal communi-
females were found to possess the highest levels of cad- cation).
mium (Martin 1979 * ; Ames et al. 1983 *). Because simi- Rote (1976) found that PCB levels in sea otter tissues
larly elevated levels of cadmium may be toxic in other throughout the range were highest in the Monterey area
species, the high cadmium residue levels found in aged and speculated that industrial activity and vessel leakage
female sea otters may present potential health risks from may have been responsible. However, data collected by
cadmium toxicity (Martin 1979; Risebrough 1984). The the State Mussel Watch Program indicated an overall
cadmium found in coastal waters of central California decline in PCB levels in California coastal waters since
occurs naturally in many of the molluscs used for food by the 1970's, corresponding to the prohibition of PCB use
sea otters. Risebrough ( 1984) speculated that sea otters in the United States.
may have evolved a biochemical mechanism of cadmium Municipal sewage outfalls are an additional source of
detoxification, as piscivorous marine mammals have, to marine pollution within the sea otter's range. Water qual-
reduce the toxic effects of mercury and possibly selenium, ity has been degraded (containing increased coliform
which are present in fish. concentrations) in Monterey Bay and Morro Bay due to
Information collected by Rote (1976), Martin (1979), dairy operations and treated municipal sewage. A large
Martin and Castle (1984), and the CDFG State Mussel outfall currently operates south of Moss Landing, about
Watch Program (which monitors the marine environment 1 mile from shore; it discharges secondary wastes into
for pollutants; Stephenson et al. 1979) indicates an in- Monterey Bay from the communities of Monterey, Sea-
crease in the following environmental toxicants within side, Pacific Grove, Salinas, and Castroville (L. Espinosa,
certain areas of the sea otter's range: synthetic organic California Department of Fish and Game, Monterey, per-
compounds, such as chlorinated hydrocarbons, Endosul- sonal communication). Other potential sources of marine
fan I, and Dieldrin; petroleum hydrocarbons; and trace pollution in the sea otter's range include the Pacific Gas
and heavy metals, including cadmium, copper, lead, mer- and Electric power plant and magnesia refractory at Moss
cury, silver, and zinc. Landing, the Pacific Gas and Electric gas- and oil-fired
The U.S. Fish and Wildlife Service (1982) noted that power plant at Morro Bay, the nuclear power plant at
the high degree of pesticide use associated with Salinas Diablo Canyon (Point Buchon), tanker (and other ship)
Valley agricultural development, maritime traffic, and traffic, and outer Continental Shelf oil resource develop-
discharge of industrial and municipal wastes seemed to ment.
be the primary sources of environmental contaminants The debilitating effects of PCB 's and organochlorine
within the sea otter's range. High concentrations of pes- pesticides, especially to the reproductive system, have
ticides entered Monterey Bay from agricultural runoff in been documented in mammals and birds: river otters
the Salinas River and Elkhorn Slough; the most common (Halbrook eta!. 1980; Renny eta!. 1980), mink (Platonow
were Endosulfan I, toxaphene, and DDT and its metabo- and Karstad 1973; Aulerich and Ringer 1977; Jensen et
lites (Martin and Stephenson 1984 ). al. 1977; Renny et al. 1980; O'Shea et al. 1980), rabbits
In general, the sea otter's range has low concentrations (Oryctolagus cuniculus; Hart et al. 1972), California sea
of most environmental pollutants. Along the open coast, lions (LeBoeuf and Bonnell 1971; DeLong eta!. 1973;
 THE SEA 0ITER: BEHAVIOR. EcoLOGY. AND N.-\TURAL HisTORY 93

Buhler et al. 1975; Gilmartin eta!. 1976), ringed seals The most harmful effect of direct exposure to oil in-
(Phoca hispida; Helle et al. 1976a, 1976b), mallards volves fouling of the otter's fur, which causes the fur to
(Anas platyrhynchos; Heath et al. 1969); brown pelicans lose its insulative properties. Loss of thermal insulation
(Pelecanus occidentalis; Anderson and Hickey 1970; subsequently leads to thermoregulatory distress, along
Gress 1970 * ), double-crested cormorants (Phalacrocora.;r with an abnormally high rate of heat production, loss of
auritus; Gress et al. 1973), bald eagles (Wiemeyer et al. buoyancy, hypothermia, pneumonia. and weight loss, any
1972), and ospreys (Pandion haliaetus; Wiemeyer et al. of which may cause death (Stulken and Kirkpatrick 1955;
1975). Deleterious effects of heavy metals, primarily Kenyon 1969, 1975; Geraci and Smith 1977; Kooyman
methylmercury, have been found in mink (Wobeser and et al. 1977 * ; Williams 1978 *; Kooyman and Costa 1979*;
Swift 1976; Wobeser et al. 1976; O'Connor and Nielsen Costa and Kooyman 1979 *, 1980. * 1982; Environment
1980), river otters (O'Connor and Nielson 1980), domes- *
Canada 1982 ; Siniff et al. 1982; Engelhardt 1983). Even
tic cats (Davies and Nielsen 1977), domestic dogs (Da- partial oil contamination of the fur. equal to 30% of the
vies et al. 1977), swine (Sus scrofa; Tryphonas and Niel- total body surface, will result. in death (Kooyman and
sen 1973), and California sea lions (Braham 1973; Buhler Costa 1979 *).
et al. 1975; Martin eta!. 1976). In addition to the documented loss of thermal insula-
Nearly complete reproductive failure has occurred in tion, another direct effect of oil contamination is the
mink when experimentally allowed to eat food containing ingestion of oil, which is acutely or chronically toxic to
PCB 's, even at levels as low as 0.6 ppm. The livers of sea otters. Substantial mortality associated with direct
female mink that exhibited reproductive failure sustained effects of oil contamination were documented in 1964,
PCB levels of 1.2 ppm (Platonow and Karstad 1973; when over 100 sea otters died from a gasoline and diesel
Aulerich and Ringer 1977; Jensen et al. 1977; 0' Shea et fuel spill that took place in the Kuril Islands (Barabash-
al. 1980; Risebrough 1984), which is lower than PCB Nikiforov et al. 1968), and during the 1989 Exxon Valdez
levels found to be in the liver of a number of California oil spill in Prince William Sound.
sea otters. Ames et al. ( 1983 *) found PCB residues > 1.2 Although little information is available on sea otters
ppm in about 20% (21) of the 102 sea otter liver samples. concerning the indirect effects of crude oil environmental
Because mink and sea otters are both mustelids, the contamination, effects may include (I) loss of habitat and
reproductive system of otters might be similarly sensitive (2) food reduction, due to mortality or unpalatability of
to the effects of PCB 's (Risebrough 1984 *). However, prey organisms resulting from direct contact of oil with
censuses conducted in California by the U.S. Fish and marine invertebrates and overall degradation of the
Wildlife Service and California Department of Fish and nearshore marine ecosystem (e.g., Evans and Rice 1974;
Game suggested that yearly pup-to-independent animal Moore and Dwyer 1974; Hodgins et al. 1977; Malins
ratios (averaging 15-16 pups to 100 independents) and 1977; Atlas et al. 1978; Roesijadi et al. 1978; Cross and
annual levels of recruitment to the population were sim- Thompson 1982 *; National Research Council 1985).
ilar to those observed in open-ended Alaskan populations The toxic or deleterious effects of oil contamination
(Estes 1981; Estes and. Jameson 1983a; Estes 1990). have been demonstrated in a number of sea otter prey
Therefore, birth rates among California sea otters seem to species (or closely related forms), including the following
be within the expected range and unaffected by accumu- macroinvertebrates: sea urchins (Strongylocentrotus and
lated levels of PCB 's in liver tissues. Paracentrotus; North et al. 1965; Allen 1971; Wells and
Keizer 1975; Axiak and Saliba 1981; Hose and Puffer
1983), crabs (Cancer and Uca; Caldwell et al. 1977 *;
Potential and Documented Effects of Oil Krebs and Burns 1977; Johns and Pechenik 1980; Sanders
Contamination et .al. 1981), clams (Protothaca, Mya, Mercinaria, and
Dona.x; Avolizi andNuwayhid 1974; Dow 1975; Gilfillan
Introduction and Summary and Vandermeulen 1978; Pearson et al.1981; Hartwick et
Sea otters are among the most sensitive marine mam- al. 1982; Olla et al. 1983 ), mussels (Mytilus; Dixon 1982),
mals to the effects of oil contamination (Kooyman et al. and possibly turban snails (Chan 1973\
1977 * ; Geraci and St. Aubin 1980; Englehardt 1983). It is still unclear whether or not sea otters are able to
Unlike most other marine mammals, the sea otter has little detect an oil slick in natural surroundings. However,
subcutaneous fat, and therefore depends on an elevated captive otters do not seem to avoid oil (e.g., Barabash-
rate of heat production and an e{ltrapped air layer within Nikiforov 1947; Barabash-Nikiforov et al. 1968; Kenyon
its dense, water-resistant underfur, which provides insu- 1969; Williams 1978 * 1989; Siniff et al. 1982). The fact
lation against the cold as well as buoyancy (Kenyon 1969; that many sea otters were killed by the 1989 Ex.xon Valdez
Iverson and Krog 1973; Morrison et al. 1974; Tarasoff spill in Prince William Sound established that free-rang-
1974; Costa and Kooyman 1982). ing otters are unable to avoid large oil slicks in nature.
94 BIOLOGICAL REPORT 90 (14)

Direct Effects tion, with the metabolic rate of some otters returning to
Loss of Thermal insulation. The contamination of a normal levels much more slowly than others. Natural oils
sea otter's fur with sufficient quantities of crude oil will in pelt samples were removed by cleaning, although water
result in loss of warmth, buoyancy, and thermoregula- repellency was retained (Williams et a!. 1988); in live
tory abilities due to the destruction of the insulative animals, the natural oils removed by cleaning had not
barrier of entrapped air maintained in the dense under- been restored after 7 days. Davis et a!. (1988a, 1988b *)
fur (Kooyman et a!. 1977 * ; Kooyman and Costa 1979 *; concluded that oiled sea otters required 1-2 weeks to
Costa and Kooyman 1979 * , 1982). Sea otters cope with restore their fur and recover from the stress of cleaning.
the problem of thermal stress not only by means of their Following the Exxon Valdez spill, oiled sea otters that
insulative fur, but also by maintaining an elevated rate were properly captured, cleaned, and dried quickly recov-
of heat production, which is higher than that of similar- ered their thermal insulation (G. VanBlaricom, Fish and
sized mammals (Kenyon 1969; Iverson and Krog 1973; Wildlife Service, Santa Cruz, Calif., personal communi-
Morrison et a!. 1974; Costa 1978a; Costa and Kooyman cation).
1982, 1984 ). A sea otter could not maintain the increase Additional experiments have shown that wild sea otters
in heat production for the prolonged period that would be seem able to survive levels of oil contamination $:10% of
necessary to compensate for a reduction in thermal insu- their total body surface for 4 days to 3 weeks, at least
lation resulting from oil fouling of the fur (Costa and during summer months (Costa and Kooyman 1979 * ;
Kooyman 1982). Siniff et a!. 1982). However, in a major oil spill, otters
Kooyman and Costa ( 1979 *) found that the normal encountering oil slicks would probably contaminate more
metabolic rate of captive sea otters immersed in water than 10% of their total body surface. The effects of oil
(15° C) increased by about 40% when 25% of the fur contamination on otters may be accentuated during win-
surface was contaminated with oil. Metabolic rate in- ter, when energy expenditure may be higher due to colder
creased 110-130% above normal when the oil was re- water temperatures, and ability to forage effectively is
moved with detergents. One of the experimental otters diminished because of rough seas. In all studies, an in-
died and two contracted pneumonia. Kooyman and Costa crease in grooming activity was documented, as otters
( 1979 *) estimated that oil fouling of 30% or more of the attempted to remove the oil from their fur (Costa and
sea otter's pelage surface will result in death from Kooyman 1979 *; Siniff et a!. 1982).
hypothermia or pneumonia. Subsequent studies have con- Little is known concerning the effects of weathered oil
firmed the loss of thermal insulation and resultant in- on sea otters. Englehardt (1983) suggested that a heavy,
crease in metabolism associated with oil contamination viscous oil would be most likely to adhere to an animal's
of sea otter fur, especially following detergent washing, pelage or skin. However, studies on the effects of oil
which appears to remove the natural fur oils and thus contamination on sea otter pelts showed that fresh crude
reduce the fur's water-repellent quality (Costa and Kooy- oil and oil dispersant mixtures caused water to penetrate
man 1979 *; Costa and Kooyman 1982; Siniff eta!. 1982; most of the pelt, while 5-day weathered crude oil caused
.
Wilhams eta!. 1986*; Davis eta!. 1986*, 1988a, 1988b*; the least change in thermal conductance. This was appar-
Williams eta!. 1988). Crude oil applied to pelt samples ently due to higher oil viscosity, which tended to remain
caused a 2- to 4-fold increase in thermal conductance on the guard hair tips, reducing oil penetration into the
(Williams eta!. 1988). fur, and maintaining insulating air pockets. The effect of
Davis et al. (1988a, 1988b *) contaminated 20% of the weathered crude oil on living sea otters, however, may be
fur surface area of several captive Alaskan sea otters with comparable to that of fresh crude, since the otters would
fresh crude oil and found that average metabolic rate probably spread the oil and compress air pockets during
increased 1.9 times and whole body thermal conductance grooming (Williams et a!. 1988).
increased 1.8 times. After application of the oil, the otters Controlled experiments have demonstrated that oil-
exhibited several changes in behavior: time spent groom- contaminated fur also results in a loss of thermal insula-
ing increased from 35% to 61%, time spent swimming tion and increase in metabolism in polar bears (Hurst et
increased from 10% to 17%, and time spent resting de- a!. 1982) and muskrats (Ondatra zibethica; McEwan et
creased from 49% to 12%. Grooming attempts worsened a!. 1974 ). Kooyman et a!. (1977 *) measured thermal
the effects of the oil contamination by spreading oil to conductance in oil-fouled northern fur seal pelts and
clean areas and pushing oil deeper into fur. All visible concluded that a light oiling would substantially impair a
evidence of oil was removed after 40 min of washing with fur seal's thermoregulatory abilities.
Dawn detergent (Proctor and Gamble; 1:16 in water) Potential Toxicity of Ingested Oil. Sea otters may ingest
along with adequate rinsing. Within 3-6 days, core body petroleum compounds in an oil-contaminated area by
temperature, average metabolic rate, and thermal conduc- grooming soiled fur or by feeding on oil-tainted prey.
tance returned to normal control levels, although the Resultant effects of oil ingestion could involve acute and
metabolic response to cleaning showed individual varia- immediate impairment to the otter's health or latent
 THE SEA OTTER: BEHAVIOR. EcoLOGY, AND NATURAL HISTORY 95

pathological disorders, including gastrointestinal, renal, Behavioral Avoidance of Oil Slicks

and hematological abnormalities (Baker et al. 1981; En- It is unclear if sea otters are able to detect and effec-
gelhardt 1983; Oritsland et al. 1981 ). Pathological effects tively avoid an oil slick in natural surroundings. The large
of oil were demonstrated conclusively following the 1989 number of sea otters that died from oil contamination
Exxon Valdez spill in Prince William Sound: pulmonary following the Exxon Valdez spill in Prince William Sound
emphysema, subcutaneous emphysema, hemmorrhagic demonstrated that, even if sea otters attempted to avoid the
enteritis, and liver and kidney dysfunction (DeGange oil, many of them were unable to do so. Williams ( 1978 *·)
1990 * ) resulted from the ingestion, inhalation, and exter- and Siniff et al. ( 1982) found that sea otters did not avoid
nal exposure to oil. A number of petroleum hydrocarbons oil in a captive situation. Two otters were placed in a small
are known to be highly carcinogenic. pool (5-m diameter), half of which was covered with
Potentially toxic effects of ingested oil may especially crude oil. Although both otters spent comparatively little
be of importance in cases of lightly oiled otters that do time in the oiled side of the pool. each otter repeatedly
not die of thermoregulatory failure, hypothermia, or entered the oil-contaminated area for brief periods and
pneumonia, since free-ranging sea otters are evidently became covered with oil. One of the otters was not
able to survive crude oil covering :::;10% of the fur surface cleaned by the researchers and subsequently died.
(Costa and Kooyman 1979 *; Siniff et al. 1982). Costa and According to Barabash-Nikiforov (1947), free-ranging
Kooyman ( 1982) did not find any evidence of oil toxicity sea otters may have avoided areas purposely contami-
in captive, oil-contaminated sea otters, although the oil nated with petroleum products by Japanese fishermen to
was cleaned from the fur within 12 h in all but one case repel sea otters; Barabash-Nikiforov assumed that the
(in which it was removed after 6 days). According to petroleum odor caused avoidance. However, sea otters did
Siniff et al. ( 1982), it was possible that oil toxicity con- not avoid a gasoline and diesel fuel spill near Paramushir
tributed to the death of one captive otter that had remained Island (Kuril Islands) that may have killed > 100 otters
in an oil-contaminated pool for 12 h. Wild sea otters that (Barabash-Nikiforov et al. 1968). Baker et al. ( 1981) found
were partially oiled (on about 10% of the total fur surface) that free-ranging European otters did not avoid oil slicks
and monitored for 2-3 weeks did not have any visible in the water or patches of oil on shore (the result of a large
toxic reactions, although it was possible that oil toxicity oil spill). Polar bears and many pinnipeds do not seem to
could have occurred after the relatively short observation consistently avoid oil (Englehardt 1983).
period (Costa and Kooyman 1979*; Williams et al. 1981; Under certain conditions a major oil spill will come
Siniff et al. 1982). ashore (e.g., VanBlaricom and Jameson 1982), trapping sea
Other marine or aquatic mammals have exhibited vari- otters between the shore and the oil slick. This can create a
able sensitivities to ingested oil. Acute toxicity resulted situation in which the otters are forced to swim through or
when three captive polar bears ingested oil while groom- under the oil slick, in which case the animals almost
ing their oil-contaminated fur. A number of serious patho- certainly become contaminated with oil.
logical disorders developed 5-6 weeks after oil ingestion Exxon Valdez Oil Spill. The effects of oil spills on sea
in all three bears, resulting in the deaths of two (Oritsland otters, until recently, remained largely a matter of specu-
et al. 1981 *). Baker et al. (1981) found that at least 13 lation since there had been no well-documented case in
European otters (Lutra lutra) died following an oil spill- which an oil spill had come into contact with sea otters.
hemorrhagic gastroenteropathy from ingestion of oil dur- The first such case occurred in December 1988 near
ing grooming seemed to be responsible for the deaths, Gray's Harbor, Washington. This spill spread northward
although hypothermia may also have been a contributing through the ranges of sea otter populations in Washington
factor. and British Columbia. Although several sea otter car-
Phocid pinnipeds have shown varied tolerance to the casses contaminated with oil were found on the beaches
presence and ingestion of crude oil. Duguy and Babin following this spill, it has not been established that these
( 1976) reported that a harbor seal died of oil toxicity from animals were actually killed by the oil. Subsequent sur-
ingested oil. Geraci and Smith (1976) found that ringed veys of both populations have indicated no detectable
seals immersed in a simulated crude oil slick for 24 h did effects on the population.
not exhibit any lasting toxic or pathological reactions, On 24 March 1989, the Exxon Valdez ran aground on
although eye irritation and lesions temporarily occurred. Bligh Reef in Prince William Sound, spilling more than
Engelhardt et al. (1977) reported low levels of hydrocar- 11 million gallons of Prudhoe Bay crude oil and resulting
bons in ringed seal tissue samples. Ringed seals fed 5 mL in the largest and most catastrophic oil spill in U.S.
of crude oil daily for 5 days accumulated hydrocarbons history. This spill eventually spread>700 km to the south-
in the blubber and liver; however, the seals were able to west, affecting coastal areas along the Kenai Peninsula,
clear tissues and blood of the accumulated residues within Kodiak archipelago, and Alaska Peninsula. Although
7 days by excreting hydrocarbons in the urine and bile much was learned about the effects of oil contamination
(Engelhardt 1978). on sea otters, work is still ongoing, and many of the results
96 BIOLOGICAL REPORT 90 (14)

are litigation-sensitive and thus unavailable to us. For never cleaned up and probably never can be. The long-
these reasons, we provide only a brief and preliminary term effects of the oil on the environment of the northern
overview of this event. Much of this information was Gulf of Alaska remain to be seen.
provided through personal communications from A.
DeGange (U.S. Fish and Wildlife Service, Anchorage,
Alaska) and G. VanBlaricom (U.S. Fish and Wildlife Review of Sea Otter Reintroductions
Service, Santa Cruz, California). A review of the effects
of the Exxon Valdez oil spill on sea otters is presented in in North America
Bayha and Kormandy ( 1990).
Effects of the Exxon Valdez spill on the population and Introduction
ecosystem of the sea otter are largely unknown, and they
are likely to remain so. Although numerous studies had As mentioned earlier. sea otters were exterminated
been conducted on sea otters in Prince William Sound, along the North American coast from Prince William
the size and distribution of the population in the area Sound to central Baja California, except for the remnant
influenced by the spill was poorly known. Limited sur- population in central California. During the 1960's and
veys were conducted in several areas before and after they early 1970's, in collaboration with various State and
were affected by spilled oil, but due to the imprecision of Provincial wildlife management agencies, the Alaska De-
sea otter counts and the ability of sea otters to move long partment of Fish and Game attempted to facilitate recov-
distances over short periods, these surveys may be im- ery by reintroducing small numbers of sea otters into
possible to interpret. Even so, there are several general areas that otherwise might not have been recolonized for
points to be made about the effects of oil on sea otter decades or centuries. From 1965 to 1972, 708 sea otters
populations there (Bayha and Kormandy 1990). First, captured at Amchitka Island and in Prince William Sound.
contrary to initial expectations, local populations were Alaska, were reintroduced into unoccupied habitat in
not exterminated over large areas of coastline, even at Alaska, Canada, Washington, and Oregon (Jameson et al.
sites that were very heavily affected. However, many 1982). In most cases, sex ratios of the initial populations
animals died. Eight hundred seventy-eight carcasses were were approximately 2:1, favoring females. In 1969. 17
recovered from the area during the response phase of the sea otters captured at Cambria, California, were released
spill (through 15 September 1989); most of these were about 72 km north into occupied habitat within the sea
killed by oil. An additional 135 animals died during otter's range. In 1988-89, 19 sea otters were captured at
capture and rehabilitation efforts. Thus, at least 1,013 sea Shell Beach and released at Moss Landing. In 1987,
otters died as a result of the spill, and the number could reintroduction of sea otters from central California to San
be much larger. The known causes of mortality were Nicolas Island, in the southern California Bight, was
briefly discussed earlier in this section. initiated. This project is ongoing. Figure 36 shows the
One of the main efforts associated with the Exxon locations of capture areas and reintroduction sites from
Valdez spill was to capture and rehabilitate oiled wildlife. Alaska to California and indicates the status of each
Most of this effort was directed toward sea otters. Many reintroduced population. Results of each reintroduction
people were involved and the estimated cost for sea otter effort are summarized in Table 11.
rehabilitation alone was $18.3 million. Otter rehabilita-
tion facilities were constructed at several sites. Three
hundred sixty-one sea otters were brought to the rehabil- Alaska
itation centers, where they were cleaned and cared for;
about 45% of these animals were found to be either The first five sea otter reintroductions were attempted
unoiled or only lightly oiled. One hundred ninety-seven in 1951, 1955, 1956, 1957, and 1959. In each of these
were eventually released back into the wild, 45 of which early instances, otters were captured at Amchitka Island
were instrumented with surgically-implanted radio trans- and transported to various sites in Alaska. All of the early
mitters for study. These studies are ongoing, but prelimi- reintroductions failed. Most of the relocated otters died in
nary results indicate that an unexpectedly high number captivity during transport or immediately following re-
have died or are missing. lease. Death resulted primarily from hypothermia, be-
Finally, the Exxon Valdez spill confirmed the fears of cause the fur of captive animals became soiled and matted
many that spilled oil could not be cleaned up or contained. during transport and handling (and consequently lost its
The weather was clear and calm for 2 to 3 days following insulative properties). Therefore, failure of the early rein-
the spill, so that conditions were ideal for containment. troductions was due to inadequate transport facilities and
Nonetheless, the oil was not contained and probably insufficient knowledge of the importance of keeping the
could not have been contained with available equipment otters' fur clean (Kenyon and Spencer 1960*; Kenyon
and technology. Furthermore, most of the spilled oil was 1969).
 THE SEA OTTER: BEHAVIOR, EcoLoGY, AND NATURAL HISTORY 97

180

Pribilof Islands
\0q

,.a•#
Fig. 36. Location and release sites of trans-
.oe:::. .o.otPt:? located sea otter populations.
Amchitka Island

Pacific Ocean

Capture Sites A
Release Sites -
Status of Population
Extinct or nearly extinct o
Status questionable "
Reestablished and increasing •

On 20 May 1959, seven otters (four females and three southeastern Alaska population increased about eightfold
males) captured at Amchitka were released at St. Paul (K. W. Pitcher, Alaska Department of Fish and Game.
Island in the Pribilof Islands. All the otters appeared to be unpublished data). In a 1988 survey of southeastern
in good health immediately following the release, and Alaska, 4,500 otters were sighted between the Barrier
subsequent sightings were made near St. Paul Island until Islands near Dixon Entrance to the south, and north of
spring 1961. However, the relocated population did not Cape Spencer (Pitcher, unpublished data). The total pop-
survive and reproduce, probably due to its small initial ulation in southeastern Alaska probably contains 5,000 or
size or to mortality from winter sea ice, which limits the more sea otters. The ratio of pups to older otters was 1:5.
northern extent of the species' range (Schneider and Faro Johnson et a!. (1983 *) reported that there seemed to be
1975). excellent sea otter habitat for future population expansion
In 1968, 55 sea otters captured at Amchitka Island were and predicted that the populations should increase 4- to
released at St. George Island in the Pribilof Islands. The 5-fold during the 1990's. This population has increased at
St. George population eventually became extinct. During a rate of 17.6% annually (Estes 1990a).
a 1977 survey of the area, only three otters were sighted.
Little or no reproduction appears to have taken place
within the relocated colony, and no pups have been ob- British Columbia
served since the 1968 relocation (Jameson et al. 1982). In
1971 and 1972, the sea ice extended unusually far south, From 1969 to 1972, 89 sea otters were reintroduced to
to the north side of Unimak Island (Schneider and Faro the Bunsby Islands in British Columbia: 29 in 1969, 14
1975), and may have reduced or eliminated the popula- in 1970, and46 in 1972. Of the relocated otters, 33% were
tion at the Pribilof Islands. It is uncertain whether subse- captured at Amchitka Island, and the remainder were
quent sightings are remnants from the reintroduction or from Prince William Sound (Cameron 1972; MacAskie
animals that dispersed northward from southwestern 1975). Bigg and MacAskie (1978) suggested that the high
Bristol Bay. Seven otters were seen at St. George Island postrelease mortality that took place during the 1969
by A.L. Sowls during summer 1988, and local residents relocation occurred due to soiled pelage incurred during
claim that up to 30 otters are present (A. DeGange, U.S. transport-the otters were not kept in holding pens before
Fish and Wildlife Service, Anchorage, personal commu- release and were therefore unable to feed or adequately
nication). groom and clean their fur before being liberated.
From 1965 to 1969, 412 otters (89% captured at Am- During a 1977 aerial survey, Bigg and MacAskie ( 1978)
chitka, 11% from Prince William Sound) were reintro- sighted 70 sea otters at the Bunsby Islands (55 otters) and
duced to various sites in southeastern Alaska (Fig. 37). Bajo Point (15 otters), including several pups (although
These efforts were successful, and the sea otter population they did not specify the number of pups observed). The
in southeastern Alaska is currently well established and populations seemed unchanged in 1978 (Breen et al.
increasing in size and range. From 1975 to 1987, the 1982). Based on the 1977-78 surveys, Farrand Bunnell
~f;~ff+~;fii;~-~~~~;;:~~ro· ~···:\~t-~~~~~~~0, :ti;;i;;.:;~i;~i:rj:;~':".~~.~:,.;.~:~'· J

\0
Table II. Number of sea otters (Enhydra lutris) reintroduced into unoccupied habitat in Alaska, Canada, Washing/on, Oregon, and California, and the size of 00
a
reintroduced populations during the most recent survey.
Otters tc
Number counted during Status of 6
r
Reintroduction Release Capture of otters Year of Total number most recent Ratio of pup: reintroduced 0
0
b n
site location site released reintroduction reintroduced survey (year) independentc population ;..
r
:;o
Pribilof Islands St. George Amchitka 55 1968 55 3 (1977) 0:100 Uncertain
.,m
0
(Alaska) Island ::1
\0
.
Southeastern
Alaska
d
89% from Amchitka;
II% from Prince
William Sound
23
30
301
1965
1966
1968
412 4,520 ( 1988) 13:100 Established
-
0
,-..,

58 1969

British Columbia Bunsby 33% from Amchitka; 29 1969 89 380 ( 1987) Some pups Established
Islands 67% from Prince 14 1970 observed
William Sound 46 1972

Washington Point Grenville Amchitka 29 1969 59 211 (1989) 8:100 Established

La Push Amchitka 30 1970

Oregon Point Orford Amchitka 29 1970 93 I ( 1981) 0:100 Extinct

24 1971
Cape Arago Amchitka 40 1971

California San Nicolas Central California 44 1988-89 103 15 ( 1990) 13:100 Uncertain
Island

a Sources of data: Jameson et aL 1982; Johnson et aL 1983"; Ja~~son, unp-ublished data; Bigg and MacAskie 1978; Pitcher 1987 and unpublished data; MacAskic 1987; Rathbun et aL 1989.
b Total includes pups.
c Number of pups sighted varies according to time of year.
In southeastern Alaska, otters were released at various sites along the exposed west coasts of Yakobi, Chichagof, Baranof, and Prince of Wales islands. Otters were released at Yakutat Bay and Cape
Spencer on the Alaska mainland.
 THE SEA 0TIER: BEHAVIOR, EcoLoGY. AND NATURAL HISTORY 99

l+60km~

Fig. 37. Southeastern Alaska, indicating

areas referred to in text.

Pacific Ocean

(1980) estimated that the population contained 70-120 located about the same distance away from these areas as
animals. In 1984, MacAskie (1984) found that the popu- are the Bunsby Islands (Bigg and MacAskie 1978).
lation in British Columbia had split into two main groups,
which together contained an estimated 345 individuals;
370 otters were counted in a 1987 survey (MacAskie Washington
1987). From these data, Estes (1990a) estimated that the
British Columbia sea otter population increased at 17.7% From 1969 to 1970, 59 sea otters were relocated from
annually. Amchitka Island to Washington. In 1969, 29 sea otters
Since the relocations to British Columbia, sea otters were released at Point Grenville; at least 16 died within 2
have been sighted as far northwest of the reintroduction weeks of the reintroduction (J arne son and Kenyon 1977*;
site as 320 km (to the Queen Charhme Islands and north- Jameson et al. 1982). Most of the mortalities occurred
ern mainland) and 220 km southeast along the Vancouver among otters whose fur became soiled in transit (Farrand
Island coast. However, ~ightings extralimita1 to the main Bunnell 1980). A second reintroduction of 30 otters was
British Columbia population may represent sea otters made to La Push in 1970. During a 1983 survey of the
from reintroduced populations in southeastern Alaska and Washington coast, 52 otters (including 4 pups) were
western Washington, since these reintroduction sites are sighted, from the Destruction Islands in the south to the
100 BIOLOGICAL REPORT 90 (14)

Bodelteh Islands in the north. The Washington population Jameson et a!. ( 1982) speculated that the sea otters
was again surveyed in 1985, during which 65 animals relocated from Amchitka might have been better adapted
were counted (Jameson et a!. 1986), of which 5 were for survival in northern waters. Because Oregon and
dependent pups. A 1987 survey recorded 90 sea otters, Washington lie within a transitional zoogeographic prov-
including 12 dependent pups. More than 200 otters were ince between the Aleutian and California provinces
counted during a 1989 survey (Jameson, personal com- (Ekman 1953), the more southerly habitat may have been
munication), although some of these were in a large group less than suitable for otters originating from the Aleutian
offshore in an area that had not been examined in previous Islands. However, the reason for failure of this relocation
surveys. The small proportion of pups (8%) observed in effort is, in fact, unknown.
the Washington population during the 1983 survey prob-
ably reflects the fact that the survey was conducted in
September, when most pups had been weaned (Jameson, California
unpublished data). Jameson et a!. (1986) reported that
from 1977 to 1983, the average rate of population growth In 1969, the California Department of Fish and Game
was 18.3% and predicted that the population should con- relocated 17 sea otters, captured and tagged near Camb-
tain > 160 otters by 1990. Estes ( 1990a) estimated that the ria, to Big Creek, located about 72 km north of Cambria.
Washington population increased at 20.6% annually from This relocation differed from those discussed previously:
1978 to 1987, a rate similar to that of other increasing the California otters were released a fairly short distance
populations in Alaska and British Columbia. from the capture site and into habitat already occupied by
sea otters. In addition, whereas the other relocations were
done to expand the otter's range, this one was done tu
Oregon limit it. The relocations in California took place during
January, April, July, and August. At least 30% (5) of the
In 1970 and 1971, 93 sea otters from Amchitka Island relocated sea otters returned to the capture site at Cambria
were released in Oregon in three relocations: 29 at Port within 9 months of their release (Wild and Ames 1974).
Orford in 1970, 24 at Port Orford in 1971, and 40 at Cape On 25 September 1969, the first relocated otter was
Arago in 1971. From 1972 to 1974, 21-23 otters were observed off Cambria (Odemar and Wilson 1969b *). On
sighted during surveys of the Oregon coastline; pup-to- 12 October 1969, four otters released at Big Creek were
independent otter ratios varied from 1:20 to about 1:3. sighted 6 km south of Cambria. According to Wild and
The Oregon populations declined dramatically after 1975 Ames ( 197 4 ), it is likely that the proportion of otters that
(Jameson 1975; Jameson et a!. 1982). In a 1981 survey, returned to the capture site was greater than indicated by
only one otter was sighted (Jameson et al. 1982). Sea the five otters actually sighted.
otters have not been seen since, and the population is Another translocation of California sea otters from the
considered extinct (Jameson, personal communication). southern to the northern part of their current range was
Eleven sea otter mortalities (including one stillborn conducted in 1988-89 by Doroff et a!. (1989 *), who
pup) were recorded in the Oregon population (Jameson investigated the movement patterns of the translocated
and Kenyon 1977 *; Jameson eta!. 1982). Although little. animals. Sea otters from the southern part of the range
postrelease mortality was documented, it is possible that were captured and moved, because animals in this area
the incidence of mortality immediately following the two may be at higher risk to oil spills if the proposed oil
1971 translocations was high. High postrelease mortality development in the Santa Maria basin takes place. If an
caused by exposure and thermoregulatory distress may oil spill occurred in this area, attempts would be made
have resulted from an unseasonal storm, which prevented to capture, clean, and relocate oil-contaminated otters;
the otters from recuperating (by cleaning their fur and therefore, the movements of such relocated otters after
feeding) in holding pens; instead, the animals were re- release in the northern part of the range are of interest; if
leased directly into open water from their carrying cages they return to their capture site, they may risk oil recon-
(Jameson 1975). tamination.
Jameson and Kenyon ( 1977 *) and Jameson et al. ( 1982) Doroff et a!. ( 1989 *) captured 19 sea otters at Shell
suggested that failure of the Oregon reintroductions may Beach and released them at Moss Landing during 3 peri-
have been due to emigration, mortality, or habitat unsuit- ods: 9 during 17-20 May 1988, 6 during 18-19 January
ability. Several sightings were made considerable dis- 1989, and 4 during 27 April-2 May 1989. A 60-day
tances from the Oregon reintroduction sites. In 1972, 4-5 radio-transmitter tag was attached to each otter's
otters were observed 204 km north of Cape Arago in June, hindflipper. One of the otters was a juvenile female, and
and 3 otters were reported 290 km north of Cape Arago the rest were juvenile, subadult, or adult males. Nine of
in August; the same otters could have been involved in the otters were released soon after being moved to Moss
both sightings (Jameson et al. 1982). Landing, while the remaining 10 were held in a flotation

£&13i212 bblOAZUJ&C£2 2322 Zii!i aaxeaC&&.&Jemmxau:

•
 THE SEA 0TIER: BEHAVIOR. EcoLOGY. AND NATURAL HISTORY 101

pen at Moss Landing harbor for 48 h to determine the for a period of time before they are released influences
effect of such containment on homing behavior. homing behavior, possibly making them less likely to
All otters detained in the holding pen remained between return to their capture site.
Monterey and Point. Afio Nuevo for the entire study. Yet The 1969 and 1988-89 California experiments demon-
56% (five) of the nine otters not held returned to the Shell strated that relocations across continuous rocky sub-
Beach capture site, about 291 km south of Moss Landing, strate-kelp forest habitat (apparently preferred by sea
traveling this distance in an average of 12 days (range= otters) could not effectively prevent otters from dispers-
7-21 days). The remaining four otters moved southward ing from the release site and traveling back to the original
only once during the monitoring period. Four of the otters capture site (Wild and Ames 1974). However, other fac-
that returned to Shell Beach immediately moved north tors such as the age of animals, presence of territorial
to Soquel Point (an area inhabited primarily by males, males, and seasonal movements of males to and from the
27 km north of the Moss Landing release site) before range peripheries (Jameson 1989), may have influenced
returning to Shell Beach. attempts to relocate male otters to a specific area within
After being released without being held for 48 h, one the established range in California. Doroff eta!. (1989)
adult male (captured 17 May 1988) moved 27 km north pointed out that all five otters that returned to their Shell
to Soquel Point where he remained for 6 days; he was Beach capture site were released in spring (late April to
found back at Shell Beach 7 days later. Interestingly, after mid-May).
34 days, he returned to Soquel Point, and was last located Jameson eta!. (1982) suggested that sea otters (espe-
28 days later near Cayucos, 250 km south of Soquel Point. cially adults) have an affinity for a specific home range.
After the expiration of his radio-transmitter, the otter was Those most likely to return to their capture site when
again sighted 3 times at Soquel Point, identified by his relocated to an unfamiliar area, therefore, may be the
hindflipper tags; the last sighting was 12 May 1989. adult otters. Jameson ( 1989) found that some adult males
One old adult male died during the monitoring period, near San Simeon, California, returned to the same terri-
and two old adult males were found dead after the study tories for 6 consecutive years. Jameson et a!. (1982)
ended, at Half Moon Bay (116 km north of Moss Land- suggested that subadult otters, especially males, may be
ing) and San Gregorio Beach (100 km north of Moss more likely to remain at the relocation site due to their
Landing); causes of all three deaths were unknown. This tendency to disperse to new areas from their natal site. In
translocation experiment indicates that holding sea otters many species of mammals, it is the juveniles, particularly

Fig. 38. San Nicolas Island translocation zone,

where the relocated population of California
sea otters is protected. Sea otters in the man-
agement zone are to be removed and trans-
ported back to the sea otter range north of
Point Conception.
102 BIOLOGICAL REPORT 90 (14)

juvenile males, that disperse from the natal area seeking Washington. Reintroductions to Oregon and to the Pribi-
reproductive opportunities (Murray 1967; Gadgil 1971; lof Islands in Alaska failed. The reasons some attempts
Hamilton and May 1977; Hom 1978). In the California succeeded and others failed are largely unknown, al-
sea otter population, evidence suggests that juvenile though postrelease dispersal has occurred in all the relo-
males tend to disperse a greater distance from the natal cation efforts (Estes eta!. 1989); failure of the reintroduc-
area than juvenile females (Ralls et a!. 1988a*; Riedman tion to St. George Island in the Pribilof Islands may have
et a!. 1988 *; Jameson, unpublished data). However, been due to mortality caused by unseasonal winter sea ice
Doroff et a!. (1989 *) found that 30% (3) of their sample in the area (Kenyon 1969; Jameson et al. 1982).
of 10 subadult males returned to their capture site within The Oregon reintroduction probably failed because of
their monitoring period. emigration from the release area coupled with a high
mortality rate. Some degree of habitat unsuitability for the
San Nicolas Island transplanted Amchitka otters may possibly have pro-
In August 1987, the U.S. Fish and Wildlife Service moted the decline in the Oregon population (Jameson et
began a major effort to reintroduce sea otters to San a!. 1982), although there is no evidence for this. The
Nicolas Island in the southern California Bight (Fig. 38). reintroductions to southeastern Alaska, British Columbia,
This effort is ongoing. Unlike all previous sea otter rein- and Washington apparently succeeded because of the
troductions, this project included an intensive follow-up larger number of otters relocated (although the Oregon
study of the fate and behavior of the relocated otters reintroduced population was larger than the one to Wash-
(Rathbun eta!. 1989\ As of June 1990, 137 animals had ington and comparable in size to the British Columbia
been moved to San Nicolas Island (U.S. Fish and Wildlife population), immigration of otters from other popula-
Service 1990). Each of these animals was marked with tions, or highly suitable habitat available at the reintro-
color-coded flipper tags, and some were instrumented duction site (1 ameson et al. 1982)
with radio transmitters. By June 1990, 15 animals were Based on the results of previous reintroduction efforts
known to have remained at San Nicolas Island. Of the for sea otters, Jameson eta!. ( 1982) concluded the follow-
other translocated animals, 30 returned to the mainland, ing: (1) Soon after release, the number of sea otters at a
9 died from human-related causes (including capture reintroduction site may decline substantially; (2) emigra-
stress), 3 were recaptured and returned to their original tion probably is the main cause of the decline; (3) it is
capture site (after they swam into the "no-otter" zone near difficult to predict specific locations where the relocated
the southern California mainland), and 80 were unac- populations will become established, although it is possi-
counted for (Rathbun et al. 1989 *). Adults(> 1.8 kg) seem ble to reintroduce otters to a general area; and (4) the
to be more likely to return to their capture sites than do successful reintroduction of sea otters into unoccupied
subadults and juveniles. Eight pups were born on San habitat probably will require a fairly large nucleus popu-
Nicolas Island; of these, one was weaned, three are still lation. Jameson et al. (1982) suggested that relocation of
with their mothers, and the fate of the remaining four is 25-30 otters annually over 3-5 years would be necessary
unknown (U.S. Fish and Wildlife Service 1990 *). The to ensure adequate growth of the reintroduced population.
success or failure of this project is still undetermined.

Summary and Conclusions Acknowledgments

Failure of all efforts to reintroduce sea otters in the We sincerely appreciate the helpful comments on an
1950's was principally due to a high mortality that oc- earlier draft of the manuscript provided by many individ-
curred during and immediately after transportation to the uals: J. Ames, C. Benz, R. Brownell, P. Dayton, M. Foster,
release site. Mortality in transit was caused by thermoreg- c: Fulton, B. Hardy, C. Harrold, R. Jameson, R. Kolpack.
ulatory distress resulting from soiled and matted fur, S. Ladd, D. Pleschner, R. Saunders, B. Steel, G.
which lost its insulative properties when the otters were VanBlaricom, and F. Wendell. J. Watanabe, C. Harrold,
released into open water. During subsequent attempts, and G. VanBlaricom provided especially useful com-
this problem was largely resolved by preventing the ani- ments on the ecology section; G. VanBlaricom helped us
mals from becoming soiled in transit and by placing them with the section on oil spills; and D. Wilson reviewed the
in holding facilities containing clean seawater before St+tion on taxonomy and classification. We are particu-
release allowing the animals to feed and to clean and lai-ly grateful to M. Bonnell, D. Carlson, and M. Pierson
groom their fur. . for invaluable help with the preparation of an earlier draft
From 1965 to 1972, attempts to reestablish populations or the manuscript, to B. Doyle for his overall support of
of sea otters into unoccupied habitat were successful in the project, and to R. K vitek and J. Zuboy for reviewing
southeastern Alaska, British Columbia, and probably the final draft of the manuscript. We thank R. K vitek and

-!lllSII_WI_I_!IJki!Wlkll.l_ll_ll#!J,4liJ.!!!J~:&I.~UI.
_II&I!IILILIIJI.. IIJIJIII!Jti.~II~I~IWI-
~~--rf.~-~..,ll'JIIb!!llfi~_.!P!-_.,,.I.ZIJ_,I_,III·········. .
 THE SEA OTTER: BEHAVIOR, EcoLOGY. AND NATURAL HISTORY 103

G. VanBlaricom for supplying unpublished data, J. Ames, Avolizi, R. J., and M. Nuwayhid. 1974. Effects of crude oil and
C. Deutsch, G. Haderlie, B. Hardy, J. Hymer, R. Jameson, dispersants on bivalves. Mar. Poll. Bull. 5:149-153.
Axiak, V ., and L. J. Saliba. 1981. Effects of surface and sunken
K. Lyons, M. Martin, M. Staedler. G. VanBlaricom, J. crude oil on the behaviour of a sea urchin. Mar. Poll. Bull.
Vandevere, F. Wendell, T. Williams. and many other indi- 12:14-19.
viduals for providing helpful information; and K. Kenyon Baker, J. R., A.M. Jones, T. P. Jones, and H. C. Watson. 1981.
for generously allowing us to reproduce many of his Otter (Lutra lutra) mortality and marine oil pollution. Bioi.
photographs. We also thank F. Bavendam, D. Buchich, C. Conserv. 20:311-321.
Barabash-Nikiforov, I. I. 1947. Kalan (The sea otter). Soviet
Fulton, J. Mattison, R. Mattison, L. Minden, C. Monnett, Ministry RSFSR. (Translated from Russian by Israel Program
T. Ransom, V. Scheffer, K. Schneider, and J. Watson for for Scientific Translation, Jerusalem. Israel, 1962.) 227 pp.
providing photographs. R. Saunders and A. Baldridge Barabash-Nikiforov, I. I., S. V. Marakov, and A.M. Nikolaev.
kindly allowed us to duplicate some of their library ma- 1968. Otters (sea otters). Izd-vo Nauka, Leningrad. 184 pp.
terial for an earlier draft of the manuscript. We would like [In Russian].
Bayha, K., and J. Korrnendy, technical coordinators. 1990. Pro-
to thank C. Hitchcock, P. Anderson, and especially P. ceedings of the sea otter symposium: Effects ofthe T(V Exxon
Himlan for typing the manuscript, and J. Shoemaker for Valdez oil spill. U.S. Fish Wildl. Serv., Bioi. Rep. 90(12). In
providing many of the illustrations. Funding for this re- press.
view was provided by the Banbury Foundation, Institute Bechstein, J. M. 1800. Thomas Pennant's allgemeine Uebersicht
of Marine Sciences, Monterey Bay Aquarium, and the der vierfuessigen Thiere. Weimar 2:401--418.
Beck, B. B. 1980. Animal tool behavior. Garland Press, New
U.S. Fish and Wildlife Service. The cover photograph was York. 307 pp.
graciously provided by J. Foott. Benech, S. V. 1977. Preliminary investigations of the giant red
sea urchin resources of San Luis Obispo County, California,
Strongylocentrotusfranciscanus (Agassiz). M.S. thesis, Cal-
ifornia Polytechnic Institute and State University, San Luis
References Obispo.
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 THE SEA OTTER: BEHAvioR. EcoLOGY. AND NATURAL HISTORY 113

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 114 BIOLOGICAL REPORT 90 (14)

program. Final rep., U.S. Marine Mammal Commission sea otter (Enhydra lutris) predation around Kodiak Island,
MM269677-5. U.S. Dep. Cammer., Nat!. Tech. Inf. Serv. Alaska. Unpubl. ms.
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Gotshall, D. W., L. L. Laurent, and F. E. Wendell. 1976. Diablo the Fourth Biennial Conference on the Biology of Marine
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Jameson, G. L. 1984. Trial systematic salvage effort in the range Conference on Biological Sonar and Diving Mammals, Stan-
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the Biology of Marine Mammals, 7-11 October 1979. Seattle, Mar. Res. Oper. 5 pp.
Wash. (Abstract) Monnett, C., and L. Ratterman. 1988a. Movement patterns of
Jameson, R. J., and A.M. Johnson. Reproductive characteristics adult female and weanling sea otters in Prince William Sound,
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Jameson, R. J., and K. W. Kenyon. 1977. Results of the 1977 sea tion status of California sea otters. Final report to the Minerals
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1977. U.S. Fish Wild!. Serv. 11 pp. Monnett, C., and L. Ratterman. 1988b. Sex-related patterns in
Johnson, A. M., R. J. Jameson, T. Schmidt, and D. C. Calkins, the post -natal development and survival of sea otters in Prince
1983. Sea otter survey, southeast Alaska, 1983. U.S. Fish William Sound, Alaska. Pages 162-190 in D. B. Siniff and
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meeting concerning research and conservation of sea otters, North, W. J. 1965. Urchin predation. Pages 57-67 in W. J. North,
I• Nadhodka, USSR, September 1984. (Available from author.) ed. Kelp Habitat Improvement Project annual report, 1 Feb-
,I
~ :
Kooyman, G. L., and D. P. Costa. 1979. Effects of oiling on ruary 1964-31 March 1965. California Institute of Technol-
temperature regulation in sea otters. Yearly progress report, ogy, Pasadena.
Outer Continental Shelf Energy Assessment Program. North, W. J. 1974. A review of the studies supporting sea urchin
Kooyman, G. L., R. W. Davis, and M. A. Castellini. 1977. control as a means of restoring kelp beds. Pages 95-114 in
Thermal conductance of immersed pinniped and sea otter Kelp Habitat Improvement Project annual report 1973-74.
pelts before and after oiling with Prudhoe Bay crude. Pages California Institute of Technology, Pasadena.
151-157 in D. A. Wolfe, ed. Fate and effects of petroleum Odemar, M. W. 1969. Flight report 69-C-10 sea otter-abalone.
hydrocarbons in marine ecosystems and organisms. Proceed- Calif. Dep. Fish Game, Mar. Res. Oper. 2 pp.
'l ings of a symposium, 10-12 November 1976, Seattle, Wash. Odemar, M. W., and K. C. Wilson. 1969b. Results of sea otter
l Kvitek, R. G., A. R. DeGange, and M. K. Beitler. Paralytic capture, tagging and transporting operations by the California
shellfish poisoning toxins mediate sea otter food preference Department ofFish and Game. Pages 73-79 in Proceedings
and distribution. Ecology. In review. of the Sixth Annual Conference on Biological Sonar and
Kvitek, R. G., A. K. Fukuyama, B. S. Anderson, and B. K. Diving Mammals, 17-18 October 1969, Stanford Research
Grimm. 1985. Sea otter foraging on deep-burrowing bivalves Institute, Menlo Park, Calif.
in the Elkhorn Slough, a California coastal lagoon. Paper Oritsland, N. A., F. R. Englehardt, F. A. Juck, R. J. Hurst, and
presented at the Western Society of Naturalists 66th Annual P. D. Watts. 1981. Effect of crude oil on polar bears. Dep.
Meeting, 27-30 December, Monterey, Calif. Indian Affairs and Northern Develop. Canada. Pub!. QS-
Kviteck, R. G., J. S. Oliver, A. R. DeGange, and B.S. Anderson. 8283-020-EE-Al. Environ. Stud. 24. 268 pp.
Changes in soft -bottom prey communities along a gradient in Pearse, J. S., M. E. Clark, D. L. Leighton, C. T. Mitchell, and

''
'
 THE SEA OTTER: BEHAVIOR, EcoLOoY.ANDNATURALHisToRY 115

W. J. North. 1970. Marine waste disposal and sea urchin and chlorinated hydrocarbons by sea otters Enhydra lutris in
ecology. Pages 1-93 in W. J. North, ed. Kelp Habitat California. Report to be submitted to the U.S. Marine Mam-
Improvement Project, California Institute of Technology, mal Commission.
Pasadena. Roest, A. I. 1971. A systematic study of the sea otter (Enhydra
Pietz, P., K. Ralls, and L. Ferm. 1988. Age determination of lutris). Pages 133-135 in Proceedings of the Eighth Annual
California sea otters from teeth. Pages 106-115 in D. B. Siniff Conference on Biological Sonar and Diving Mammals. Bioi.
and K. Ralls. Population status of California sea otters. Final Sonar Lab., Mar. Mammal Stud. Cent., Stanford Research
report to the Minerals Management Service, U.S. Dep. Inter. Institute, Menlo Park, Calif.
14-12-001-3003. Roest, A. I. 1979. A re-evaluation of sea otter taxonomy. Paper
Pitcher, K. W. 1987. Studies of southeast Alaska sea otter popu- presented at sea otter workshop, 23-25 August, Santa Barbara
lations: distribution, abundance, structure, range expansion, Mus. Nat. Hist., Santa Barbara, Calif. 14 pp.
and potential conflicts with shellfisheries. Alaska Dep. Fish Rosenthal, R. J., and D. C. Barilotti, 1973. Feeding behavior of
Game, Coop. Agreement 14-16-0009-954 with U.S. Fish transplanted sea otters and community interactions off
Wild!. Serv. 29 pp. Chichagof Island, Southeast Alaska. Pages 74-88 in W. J.
Ralls, K., T. Eagle, and D. B. Siniff. 1988a. Movement patterns North, ed. Kelp Habitat Improvement Project, annual report.
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Siniff and K. Ralls. Population status of California sea otters. Schmidt, W. T. 1983. Aerial survey of sea otters in the Cordova
Final report to the Minerals Management Service, U.S. Dep. vicinity. Unpubl. rep., U.S. Fish and Wild!. Serv., Anchorage,
Inter. 14-12-001-3003. Alaska. 9 pp.
Ralls, K., B. Hatfield, and D. B. Siniff. 1988b. Feeding patterns Schneider, K. B. 1971. Reproduction in the female sea otter.
of California sea otters. Pages 84-105 in D. B. Siniff and K. Project progress report, Federal Aid in Wildlife Restoration
Ralls. Population status of California sea otters. Final report Project W -17-4. Alaska Dep. Fish Game. 38 pp.
to the Minerals Management Service, U.S. Dep. Inter. 14-12- Schneider, K. B. 1972a. Reproduction in the female sea otter.
001-3003. Federal Aid in Wildlife Restoration Project W-17-4. Project
Ralls, K., and D. B. Siniff. 1988. Time budgets and activity progress report. Alaska Dep. Fish Game. 36 pp.
patterns of California sea otters. Pages 64-83 in D. B. Siniff Schneider, K. B. 1972b. Sex and age segregation of sea otters.
and K. Ralls. Population status of California sea otters. Final Federal Aid in Wildlife Restoration Project W-17-4. Project
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14-12-001-3003. Schneider, K. B. 1972c. Age determination of sea otters. Project
Ralls, K., D. Siniff, C. Monnett, T. Eagle, and L. Ferm. 1985. progress report, Federal Aid in Wildlife Restoration Project
Summary of information pertaining to California permit to W -17-4. Alaska Dep. Fish Game. 8 pp.
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Fish and Game Commission, 30 August 1985, San Rafael. Federal Aid in Wildlife Restoration Project W-17-4 and W-
101 pp. 17-5. Project progress report. Alaska Dep. Fish Game. 13 pp.
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Eighth Biennial Conference on the Biology of Marine Mam- 17 -5. Project progress report. Alaska Dep. Fish Game. 15 pp.
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Minerals Management Service, U.S. Dep. Inter., Alaska, 14- otters-Aleutian Islands, Alaska Peninsula, and Shumagin
16-0009-78-937, 57 pp. Islands. Alaska Dep. Fish Game. Unpubl. rep. 22 pp.
Riedman, M. L. 1984b. Effects of sounds associated with petro- Simon-Jackson, T. 1986. Sea otter survey, Cordova, Alaska-
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California. Pages D1-Dl2 in C. I. Malme, P.R. Miles, C. W. Anchorage, Alaska. Unpubl. rep. 32 pp.
Clark, P. Tyack, and J. E. Bird. Investigations of the potential Simon-Jackson, T., and J. Hodges. 1986. Sea otter survey, Gulf
effects of underwater noise from petroleum industry activities of Alaska-1987 (Cape Spencer to Point Martin). U.S. Fish
on migratory gray whale behavior. Phase II. Final report to Wild!. Serv., Anchorage, Alaska. Unpubl. rep. 16 pp.
the Minerals Management Service, U.S. Dep. Inter. 14-12- Simon-Jackson, T., M. Vivion, and D. Zwiefelfofer. 1986. Sea
0001-29033. otter survey, Kodiak Island-1985. Unpubl. rep., U.S. Fish
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cast sea otter carcasses in central and northern portions of the Simon-Jackson, T., and L. M. Rotterman. 1987. The sea otter in
sea otter range in Calfomia. Six-month summary of results: Alaska (Enhydra lutris): species account with research and
March to August 1984. Unpubl. rep. management recommendations. Prepared for the Marine
Riedman, M. L., J. A. Estes, and M. M. Staedler. 1988. Behav- Mammal Commission, Washington, D.C.
ioral and biological studies on the California sea otter in the Siniff, D. B., and K. Ralls. 1988. Reproduction, survival and tag
northern part of its range. Monterey Bay Aquarium, Res. Rep. loss in California sea otters. Pages 13-32 in D. B. Siniff and
Unpubl. ms. K. Ralls. Population status of California sea otters. Final
Riedman, M. L., M. M. Staedler. ~- A. Estes, and B. Habrich. report to the Minerals Management Service, U.S. Dep. Inter.
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lutris). Paper presented at the Eighth Biennial Conference on gered species of the seacoast of the United States-southern
the Biology of Marine Mammals, 7-11 December, Monterey, sea otter. National Fish and Wildlife Laboratory. Biological
Calif. Services Program. 8 pp.
Risebrough, R. W. 1984. Accumulation patterns of heavy metals U.S. Fish and Wildlife Serivce. 1990. Southern sea otter translo-

______________ .............,.,.,......,_,_,_~~·-, ---"-----· .. - ..

 116 BIOLOGICAL REPORT 90 (14)

cation to San Nicolas Island, August 1989-July 1990. Third Institute, Menlo Park, Calif.
annual report to the Ventura Endangered Species Recovery Wendell, F. E., R. A. Hardy, and J. A. Ames. 1985. Assessment
Office, Ventura, Calif. 13 pp. of the accidental take of sea otters, Enhydra lutris, in gill and
V andevere, J. E. 1969. Feeding behavior of the southern sea otter. trammel nets. Mar. Res. Branch, Calif. Dep. Fish Game.
Pages 87-94 in Proceedings of the Sixth Annual Conference Unpubl. rep. 30 pp.
on Biological Sonar and Diving Mammals. Stanford Research Wild, P. W. 1973. Flight report 86-4, sea otter-abalone. Calif.
Institute, Menlo Park, Calif. Dep. Fish Game, Mar. Res. Oper. 2 pp.
Vandevere, J. E. 1970. Reproduction in the southern sea otter. Williams, T. D. 1978. Chemical immobilization, baseline hema-
Pages 221-227 in Proceedings of the Seventh Annual Con- tological parameters, and oil contamination in the sea otter.
ference on Biological Sonar and Diving Mammals. Stanford Final report to U.S. Marine Mammal Commission, Contract
Research Institute, Menlo Park, Calif. MM7 AD094. 27 pp.
Vandevere, J. E. 1971. Fecal analysis of the southern sea otter. Williams, T. M., R. A. Kastelein, R. W. Davis, and J. A. Thomas.
Pages 1-7 in Proceedings of the Eighth Annual Conference 1986. Procedure for cleaning sea otter fur contaminated with
on Biological Sonar and Diving Mammals. Stanford Research fresh or weathered crude oil: thermal implications of contam-
Institute, Menlo Park, Calif. ination and cleaning. Sea otter oil mitigation study. Prepared
Vandevere, J. E. 1972. Behavior of southern sea otter pups. Pages by Hubbs Marine Research Institute for the Minerals Man-
21-35 in Proceedings of the Ninth Annual Conference on agement Service. U.S. Dep. Inter. 14-12-0001-30157.
Biological Sonar and Diving Mammals. Stanford Research Wilson, K. C. 1968a. Flight report 68-4 sea otter-abalone. Calif.
Institute, Menlo Park, Calif. Dep. Fish Game, Mar. Res. Oper. 2 pp.
Vandevere, J. E. 1973a. Behavior of the southern sea otter, Wilson, K. C. 1968b. Flight report 68-5 sea otter-abalone. Calif.
Enhydra lutris nereis. Paper presented at the 53rd annual Dep. Fish Game, Mar. Res. Oper. 2 pp.
meeting of the American Society of Mammalogists, 14 June Wilson, K. C., M. Odemar, and P. W. Wild. 1970-1976. Sea otter
1973. Asilomar, Calif. flight reports. Calif. Dep. Fish Game, Mar. Res. Reg. Calif.
Vandevere, J. E. 1973b. Occurrences of hauling-out in the south- State Fish. Lab., Terminal Island.
ern sea otter, Enhydra lutris nereis. Proceedings of the Tenth Woodhouse, C. D., Jr., R. K. Cowen, and L. R. Wilcoxon. 1977.
Annual Conference on Biological Sonar and Diving Mam- A summary of knowledge of the sea otter, Enhydra lutris L.,
mals. Stanford Research Instutute, Menlo Park, Calif. in California and an appraisal of the completeness of biolog-
Vandevere, J. E. 1978. Gestation period. Otter Raft 19. ical understanding of the species. Final report. U.S. Marine
Vandevere, J. E. 1979. The dependency period for Enhydra lun·is Mammal Commission, Contract MM6AC008. 71 pp.
nereis. Paper presented at sea otter workshop 23-25 August, Woodward, R. 1981 a. Observation of a sea otter giving birth on
Santa Barbara Mus. Nat. Hist., Santa Barbara, Calif. land at Point Lobos State Research. Unpubl. draft rep.
Vandevere, J. E., and A. Baldridge. 1973. Occurrences of haul- Yellin, M. B., C. R. Agegian, and J. S. Pearse. 1977. Ecological
ing-out in the southern sea otter, En hydra lun·is nereis. Paper benchmarks in the Santa Cruz County kelp forests before the
presented to the Tenth Annual Conference on Biological re-establishment of sea otters. Final report. U.S. Marine Mam-
Sonar and Diving Mammals, 26 October, Stanford Research mal Commission. Contract MM6AC029.

!I .j;
I
 INDEX 117

Index
Abalone. See Haliotis sea urchins in, 30
Abandonment, of pups, 70 southern, 12
Activity, patterns of, among sea otters, 45-48 southwestern, 12, 73
Adak Island, Alaska, 12, 14 Alaska Peninsula, 12, 73, 75, 95
Adaptation, of sea otters, to a marine environ- Aleutian Islands (archipelago), Alaska, 42 (map), 73
ment, 5-7 diet of gulls in, 31
Adoption, of pups by other females, 71, 72 fish populations in, 30
Aechmoph&rus occidentalis (western grebe), 45 kelp canopy in, 23, 29
Africa, fossils in, 3, 4 lead from, 92
Age (see also Lifespan) sea otters in
estrus and, 65 breeding season of, 60
and pelage color, 21, 22 (illust.) diet of, 36-40 (table), 41
and reintroduction, 102 diurnal activity cycles of, 46
Alariafistulosa (annual kelp), 23 Enhydra lutris (unnamed) in, 10, 12 (table)
l Alaska foraging depth and, 22, 31
t sea otters in growth rates of, 82
I· adoption among, 71 haul-out behavior of, 24
I age of, 15, 54 hunting of, 73
!
annual recruitment of, 82 mating behavior of, 60
competitors of, 31 mortality rates of, 82
diet of, 25-26, 31, 36, 36-40 (table), 40, populations of, 73, 75
40 (illust.), 41 pups of, 66, 67
diurnal activity cycles of, 46-48 range of, 73
effect of, on benthic invertebrates, 25, 26, 27 tool use among, 33
fossils of, 3 travels of, 56, 58
gestation period of, 66 twinning among, 65
habitat of, 22, 23 sea urchins in, 26, 27, 31
haul-out behavior of, 24, 25 (illust.) see also Arnchitka Island
horne range of, 56-58 Aleuts, hunting of sea otters by, 73
hunting of, 73 Algae
as a "keystone" species, 25 articulated coralline. See Pterygophora californica
killer whale vocalizations and, 19 fleshy brown. See Phaeophyta
male territoriality in, 63-64 Alloparenting, among sea otters, 70-72
pathological disorders among, 90 Amchitka Island, Alaska, 92
populations of, 12, 54, 75 kelp forest off, 28 (illust.)
PSPand, 45 sea otters in, 45
pups of, 70 bald eagles as predators of, 68-69, 89
reintroduction of, 96-97, 99 (map) breeding season of, 59
seasonality of breeding among, 59-60 diet of, 33, 36, 40, 40 (illust.), 41
sexual segregation among, 53 effect of, on benthic invertebrates, 25, 26
size of, 13-14 haul-out behavior of, 24, 25 (illust.)
skulls of, 12 male areas of, 53
social structure of, 48-50 mortality rates of, 82-83
swimming speeds recorded in, 15 movements of, 58-59
tool use among, 33 population of, 25, 41, 73, 75
southeastern reproductive cycle of, 66
kelp forest in, 29 sexual segregation among, 54
sea otters in size of, 13-14, 14 (illust.)
diet of, 36-40 (table) skulls of, 12, 16-17 (illust.)
growth rates of, 82 territoriality in, 63
population of, 75 translocation of, 99, 100, 102
translocation of, 73, 97, 99 (illust.) sea urchins in, and otter habitation, 26
118 BIOLOGICAL REPORT 90 (14)

Anarrhichthys ace/latus (wolf-eel), 31 Big Sur, California, 48, 75 (illust.), 79

An as Biphenyls, polychlorinated, (PCB's), 91,92-93
crecca (common teal), 45 Bivalve, infaunal. See Saxidomus nuttallii; Tresus
platyrynchos (mallard), 93 nuttallii
Anchovy. See Engraulis mordax Bixby Creek cove (California), otters at, in 1938,
Andreanoflslands, Alaska, 42 (map), 75 75 (illust.), 76
Afio Nuevo Point, California. 77, 88, 89, 101 Blubber, for heat conservation, 5-6
Aonyx, 2 Boats, as a cause of otter mortality, 87
cinerea (Asian small-clawed otter), visual Bodelteh Islands, Washington State, 100
acuity of, 19-20 Breathing, adaption of sea otters', 5
Aquarium Breeding, seasonality of, 59-60. See also
Monterey Bay (California), 20, 34, 41, 65 Reproduction
Point Defiance Zoo and (Tacoma, Washington), Bristol Bay, Alaska, 23, 49, 49 (illust.), 97
15, 64, 71,72 British Columbia
Seattle (Washington State), 71-72 kelp forest in, 29
Vancouver Public (Canada), 15, 71,72 sea otters in
Asia, lead from, 92 growth rates of, 82
Asteroids, 31 as a "keystone" species, 25
Atascadero State Beach, California, 44 population increase among, 99
Attu Island, Alaska reintroduction of, 73, 97,99
sea otters in sea urchins in, 26, 30
diet of, 36, 36-40 (table) Bunsby Islands, British Columbia, 97, 99
foraging behavior of, 47
reintroduction of, 30, 73 Cabezon. See Scorpaenichtys marmoratus
sea urchins in, 26 Cadmium, 91, 92
Australia, algae in, 5 Calibration, of otter census, 77
Avila Beach, California, 86 California
abalone in, 26-27
Badger. See Taxidea taxus intertidal mussels in, as otter prey, 27
Baja California, Mexico, sea otter range in, 10, kelp forest in, 28 (illust.), 29
11 (map), 12, 73, 82 sea otters in
Bajo Point, British Columbia, 97 age of, 14-15
Balanus spp. (barnacles), 41 annual recruitment of, 82
Bald eagle. See Haliaeetus leucocephalus competitors of, 31
Baranof Island, Alaska, 98 n. diet of, 20, 34-36, 36-40 (table), 41,44
Barnacles. See Balanus spp. diurnal activity cycles of, 45, 46-48
Barrier Islands, Alaska, 97 E. l. nereis, 10, 12 (table)
Bear foraging behavior in, 31-32, 34
brown. See Ursus arctos fossils of, 3
polar. See U. maritimus · gestation period of, 66
Behavior, sea otter habitat of, 22, 23
altruistic, 50 haul-out behavior of, 24, 24 (illust.)
avoidance of oil slicks and, 95-96 as a "keystone" species, 25
"babysitting," 70-71 male territoriality of, 62-63
foraging, 22, 31-32, 34, 35-36 mating behavior of, 60
hostage, 33, 71 movements of, 70
mating, 60-62 pathological disorders among, 89-90
social, 48-59 population of, 53, 76-81
patterns of, 51-52 (table) range of, 10, ll(map), 54-56,80 (illust.), 81
tending, 60 recorded swimming speeds of, 15
of territorial males, 64 reproduction among, 59, 66
Bering Island, U.S.S.R., 75 sexual segregation among, 53
Bering Land Bridge, 3, 4 size of, 13
Bering Sea, 12 skulls of, 12
Big Creek, California, 100 social structure of, 9 (illust.), 48, 50
 INDEX 119

tool use among, 33-34 Clam (see also Donax; Mercinaria; Mya;
translocation of, 96, 100-102 Protothaca, Tresus; Saxidomus), 35, 44
sea urchins in, 26, 31 butter. See Sa.xidomus giganteus
California Department of Fish and Game (CDFG) Pismo. See Tivela stultorum
salvage program of, 83-84 Classification of sea otters, 7-12
sea otter mortality research of, 83-84, 86-87 Commander Islands, U.S.S.R, 42 (map), 73
State Mussel Watch Program, 91,92 sea otters in, 41
California sheephead. See Semicossyphus pulcher adoption among, 71
Callorhinus ursinus (northern fur seal), 20, 65, 94 diet of, 36-40 (table)
Cambria, California, 84, 87, 96, 100 hunting of, 73
Canada parturition among, 68
lead from, 92 population of, 75
reintroduction of sea otters in, 96 and PSPT, 45
Cancer magister (Dungeness crab), as otter prey, pups of, 66, 67, 70
22,26-27,47,48 range of, 73
Canis remanant populations of, 73
familiaris (dog), 20, 93 sexual segregation among, 54
latrans (coyote), as a predator, 6,69,89 species of, 10, 12, 12 (table)
Cannery Row, Monterey, California, 77 travels of, 56
Cape Arago, Oregon, 100 twinning among, 65
Cape Blanco, Oregon, 3 Communication, among sea otters. 50
Cape Mendocino, California, 82 Community, otters' role in marine, 25-31
Cape San Martin, California, 87 Competition, for sea otter food, 31
Cape Spencer, Alaska, 97, 98 n. Copper, 92
Captivity, sea otters in Copper River Delta (Alaska), 87
age of, 15 Copulation, 61-62
alloparenting among, 71-72 Cormorant
consumption of kelp by, 41 See Phalacrocorax spp.
drinking of fresh water by, 20 double-crested. See P. auritus
estrus among females in, 64 Coyote. See Canis latrans
Halarachnidae infection among, 90 Crab, 32,41
infanticide among, 72 Dungeness. See Cancer magister
molting among, 20 kelp. See Pugettia spp.
Capture, otters' method of, 32, 32 (illust.) king. See Lithodes; Paralithodes
Carbon, kelp as a source of organic, 31 pelagic red. See Pleurocodes planipes
Carcasses, recovery of, 83-84, 84, 85 (table) Crab-otters, 2
Carcharodon carcharias (white shark), 6, 88-89 Cryptochiton spp. (chitons), 41
Care, maternal, for sea otter pups, 67 (illust.), Cypress Point, California, 24, 79, 88
67-70
Carmel Bay, California, 26 DDT. See Hydrocarbons, chlorinated
Cats, domestic. See Felis silvestris Deer, black-tailed. See Odocoileus hemionus
Cayucos, California, 53, 55, 101 Dentition, in sea otters
CDFG. See California Department of Fish and Game adaption of, 5
Census, of California sea otters, 76 (table), 76-77 and age determination, 15
Central American Seaway, 3 pattern of, 15, 16-17 (illust.)
Cetaceans, composition of milk of, 65 Depth
Channel Islands, California, 73 diving, 5, 22
Chen canagica (emperor goose), 45 foraging, 31
Chichagof Island, Alaska, 98 n. Destruction Islands, Washington State, 99
Chile, marine otters in, 7 Detergent, use of, to wash off oil contamination, 94
Chimpanzees, diet of, 45 , Diablo Canyon, California, 79, 92
Chitons. See Cryptochiton spp. Diablo Cove, California, 79
Chungungo. See Lutra felina Dieldran, 92
Cladogram, 3 (illust.) Diet. of sea otters
 120 BIOLOGICAL REPORT 90 (14)

in California, 41, 43 (table), 44 renamed, 12

individual variation in, 34-35 taxonomic classification of, 12 (table)
Dinoflagellates. See Protogonyaulax spp. nereis, 10, 12
Disease range of, 12
and oil contamination, 95 taxonomic classification of, 12 (table)
otter mortality and, 89-90 unnamed, 10, 12
Distribution, of sea otters range of, 12
in California, 77, 78 (table), 79, 80 (illust.) taxonomic classification of, 12 (table)
historical, 73-75 macrodonta, 3-4
original and current, in the North Pacific, Enhydriodon, 2, 3
11 (map) africanus, 3
Diving, 5, 22,31-32 falconeri, 3
Dixon Entrance, Alaska, 97 latipes, 3
Dogs. See Canis familiaris reevei, 3
Dolan Rock, California, 77 sivalensis, 3
Donax (clam), 93 Enhydritherium, 2, 3, 4
Drowning, of otters lluecai, 3
during mating, 62,90 terraenovae, 3
in fishing nets, 84-87 ENSO. See E1 Nino Southern Oscillation
Dusisiren dewana, 4 Enteritis, among sea otters, 89
Environment
Eagle, bald. See Haliaeetus leucocephalus contamination of, and otter mortality, 91-93
Ear, external, 19, 19 (illust.) and distribution patterns, in California, 79, 81
Echinoids, strongylocentroid, phenolics and, 4-5 and evolution, 4-5
Ecology, 22-31 marine, mammalian adaptation to, 5-7
Eider, as competition for sea otters, 31 Esalen, California, 77
Elkhorn Slough, California, 27, 44, 79,92 Estrus, 64, 65
El Nino Southern Oscillation (ENSO; "El Nino"), Ethogram, 50, 51-52 (table)
31,44, 73 Eurasia, fossils in, 3, 4
Endosulfan I, 92 Europe, fossils in, 3
Energetics, 21-22 Evolution, 2-7
England, fossils in, 3 Exploitation, alloparental, 71
Engraulis mordax (anchovy), 35 Exxon Valde:, effect of oil spill from, on otters,
Enhydra, 2, 3-4, 4 93-96
lutris (sea otter) Eye, sea otter's, 5, 19
action patterns of, 51-52 (table)
adaptation of, to a marine environment, 5-7 Farallon Islands, California, 88-89
causes of mortality of, 85 (table) Fauna, kelp-associated, 4
census of, in California, 76 (table) Feeding (see also Behavior, foraging)
compared with river otter, 9-10 (table), adaption of sea otters', 5
11 (illust.) time spent, 47-48
distinguished from E. mactodonta, 4 Felis silvestris (domestic cat), 20, 93
drowning of, in nets, 86 (table) Female otter
population of home range of, 55-56, 57
growth in, 78 (table) reproduction in, 64-72
in the North Pacific Ocean, 74 (table) Ferret. See Mus tela putorius
prey of, 43 (table) Fights, and otter mortality, 90-91
range expansion of, 78 (table) Fish
reintroductions of, 98 (table) as competition for sea otters, 31
size of, 7 in the diet of otters, 30-31,36,40,40 (illust.), 41
subspecies of, 10, 12 numbers of, and kelp, 30-31
taxonomic classification of, 12 (table) Fishery, Dungeness crab, effect of otters in Prince
gracilis, 12 William Sound on, 27
t lutris, 10 Fishing, and otter mortality
. '
and E. lutris nereis, 12 lines and, 87
 INDEX 121

nets and, 81 (map), 82, 84-87 Hindlimbs, of sea otters, 8 (illust.), 15

Fish-otters, 2 Hinnites spp. (scallops), 41
Florida, fossils in, 3 Hokkaido, Japan, 73
Flounder, starry. See Platichthys stellatus Home range, 54-59
Food (see also Prey) Hopkins Marine Life Refuge, California, 27
reduction of, from oil contamination, 93 Humans, as a direct cause of mortality in otters,
theft of, by otters, 32-33 84-88
Foraging. See Behavior, foraging Hunting, of otters, 73
Forelimbs,' of sea otters, 15, 18 (illust.) Hydrocarbons, 92, 95
Fossils, 2-3 chlorinated (DDT), 91
Fostering. See Alloparenting petroleum, 92
Fox Islands, Alaska, 75 Hydrodamalis, 4
Fulmar. See Fulmarus sp. gigas (Steller's sea cow), . 4
Fulmarus sp. (fulmar), 45
Fur Implantation, delayed, 65
density of, in sea otters, 20 India, fossils in, 3
effect of oil contamination on, 94-95 Infanticide, among otters, 72
for heat conservation, 5, 6 Insulation, thermal
conservation of, in marine animals, 5-6
Gamboa Point, California, 79 loss of
Gavia immer (common loon), 45 during transportation, 96, 97, 100, 102
Genetics. See Variability, genetic from oil contamination, 93. 94-95
Geoduck. See Panopea generosa Internal organs, of the sea otter, 20
Gestation, duration of, 66 International Fur Seal Treaty (1911), 73
Gibbon Anchorage, Alaska, 54, 57 International Union for the Conservation of Nature
Glacier Bay, Alaska, 26 (IUCN), Red Data Book, 7
Goose, emperor. See Chen canagica Invertebrates, otters' predation on benthic, 25-26
Granite Canyon, California, 30, 45 Isla de Cedros, Mexico, 73
Gray's Harbor, Washington, 96 Isla de Guadalupe, Mexico, 73
Grebe, western. See Aechmophorus occidentalis Islas San Benitos, Mexico, 73
Greece, fossils in, 3 IUCN. See International Union for the Conservation of
Green Island, Alaska, 44, 47, 48, 54, 57, 58 Nature
Greeting, ritualized, 5
Gregariousness, among sea otters, 9 (illust.), 48-50 Japan, E. l. gracilis in, 12
Grimes Point, California, 55 Juan de Fuca, Strait of, (U.S.A.-Canada), E.!. nereis
Grooming, 20-21, 21 (illust.) in, 10
and oil contamination, 94 Juveniles, dispersal of, 56,57-58
Gulf of Alaska, 73, 75
Gull. See Larus Kamchatka Peninsula
sea otters in
Habitat E.!. gracilis, 12
characteristics of, 22-23 E.!. lutris, 10, 12 (table)
loss of, from oil contamination, 93 population of, 75
qualities of, in Alaska, 63 as prey of brown bears, 89
Halarachnidae (nasal mite), 90 range of, 73
Half Moon Bay, California, 101 remanant populations of, 73
Haliaeetus leucocephalus (bald eagle) type locality for E. lutris, 12
effect of PCBs and pesticides on, 93 Kanaga Island, 66
as a predator, 6, 68-69, 89 Kelp
Halibut, California. See Parali{:hthys californicus Alaskan, 28 (illust.)
Haliotis spp. (abalone), 26-27,32-33,41 annual. See A/aria fistulosa
Hauling out behavior, in sea otters, 24-25 (illust.) bull. See Nereocystis leutkeana
Hearing, sea otters' sense of, 5, 19, 19 (illust.) canopy, as a sea otter habitat, 23, 81
Hexagrammos lagocephalus (rock greenling), giant. See Macrocystis pyrifera
30,41 hypothetical radiation of, 5
 122 BIOLOGICAL REPORT 90 (14)

influences on communities in, 31 Macrocystis, 30

and numbers of fish, 30-31 pyrifera (giant kelp)
otter predation of, 28, 29,29-30,41 in otter habitats, 23, 62
see also Laminariales; Laminaria otters' consumption of, 41
J Kelp crab. See Pugettia spp. Males
ii Kenai Peninsula, Alaska, 95 home range of, 54-55,56-57
,
j Kidneys, of the sea otter, 6, 20 reproduction in, 62-64
Killer whale. See Orcinas orca territorial, as food thieves, 32-33
Killing of female sea otters during mating, 62 transient, 63
Kodiak archipelago, Alaska, 30, 36-40 (table), 45, Mallard. See Anas platyrynchos
75,95 Malpaso Creek, California, 77
Kuril Islands, U.S.S.R. Mating
mussels in, as otter prey, 27 and otter mortality, 90
oil spill in, 93 success in, and territory, 63-64
sea otters in, 41,42 (map) Maturity, sexual
diet of, 41,42 (illust.) in females, 64
E. 1. gracilis, 12 in males, 61
E. 1. lutris, 10, 12 (table) Medney Island, U.S.S.R., 41, 75
population of, 73, 75 Melanitta perspicillata (surf scoter), 44 (illust.), 45
Mercinaria (clam), 93
Lactation, duration of, 69 Mercury, 92
Laminariales (kelps), evolution of, and sea otters, Metabolism, of sea otters, 5, 6, 21
4. See also Kelp Metals, heavy, 91, 91-92, 93
Laminaria setchellii (kelp), 30 Methylmercury, 93
Langurs. See Presbytis spp. Milk, composition of sea otter, 65
Larus (gull), 45 Mink. See Mustela vison
glaucescens (glaucous-winged gull), 31 Mirounga angustirostris (northern elephant seal),
La Selva Beach, California, 79 65,88,89
Lead, accumulation of postindustrial, 92 Mite, nasal. See Halarachnidae
Life history, Enhydra lutris and Lutra canadensis Modiolus difficilis, 41
compared, 9-10 (table), 11 (illust.) Mollusc, bivalve, See Modiolus difficilis; Mytilus spp.;
Lifespan, of sea otters, 14-15. See also Age Tellina spp.
Limpets. See Patellogasdropoda Molting, in sea otters, 20
Lineage Monitoring, of otter mortality from commercial
dichotomies in, 3 fishing, 86-87
radiation of, 3, 4 Montague Strait, Alaska, 44
Lion. See Panthera leo Monterey Bay, California, 43-44, 44 (il!ust.), 55,
Lithodes (king crab), 22 56,79,86-87,92
Liver, of the sea otter, 20 Monterey, California, sea otters in
Lobster, spiny. See Panulirus interruptus adoption among, 71
Locomotion, adaption of sea otters', 6, 8 (illust.) breeding among, 59, 60, 61, 62, 64, 67
Loligo opalescens (squid), 35, 44 communication among, 50
Loon, common. See Cavia immer diet of, 35
Los Angeles Harbor, California, 92 foraging by, 31
Lungs, sea otters', 5, 6 (illust.), 20 haul-out behavior of, 24 (illust.)
Lutra, 2 hostage behavior of, 33
canadensis (river otter) pups of, 70
compared with sea otter, 9-10 (table), range of, 53, 55
11 (illust.) shark attacks on, 88
hearingin, 19 tag loss among, 59
felina (South American marine otter; sea cat; territoriality among, 62-63
chungungo), described, 7, 9 tool use by, 33, 34
lutra (European otter), effects of oil contamination translocation and, 101
on, 95 travels of, 55, 56
 INDEX 123

Monterey Harbor, California, 45,79,87,92 toxicity of ingested, 93, 94-95

Moonstone Beach, California, 3 weathered, effect of, on otters, 94
Morphology Olfaction, sea otters', 5, 15, 19
of sea otters, 13-22 Ondatra zibethica (muskrat), 94
Enhydra lutris and Lutra canadensis compared, Orca Inlet, Alaska, 57
9-10 (table), 11 (illust.) Orcinus orca (killer whale), 19, 89
Morro Bay, California, 44, 48, 55, 86, 87, 90, 92 Oregon, sea otters in
Morro Hermoso, Mexico, 73 diet of, 36-40 (table)
Mortality, of sea otters E. l. (unnamed), 10, 12 (table)
accidental, 87-88 foraging behavior of, 47
causes of reintroduction of, 96, 100, 102
documented, 83-91 Organisms, coastal, evolution of, and sea otters. 4
potential (undocumented), 91-96 Oryctolagus cuniculus (rabbit), 93
from the Exxon Valdez oil spill, 96 Osprey. See Pandion·haliaetus
natural, 88-91 Otter
and population changes, 81,82-83 Amazonian. See Pteronura brasiliensis
translocation and, 102 Asian small-clawed. See Aonyx cinerea
trends in, 84, 85 (table) European. See Lutra lutra
Moss Landing, California, 55,56, 79,87-88,92, river. See Lutra canadensis
96, 100-101 sea. See Enhydra lutris
Moss Landing Marine Laboratories (California), 86 South American marine. See Lutrafelina
Movements, patterns, of, among sea otters, 56, southern sea. See Enhydra lutris nereis
58-59 Ovulation, in otters, 65
Muskrat. See Ondatra zibethica Oyster, rock. See Pododesmus cepio
Mussels. See Mytilus
Mustela Pacific Gas and Electric Company, 92
putorius (ferret), 65 Pacific Ocean, North
vison (mink), 45, 91, 92, 93 algae in, 4-5
Mya (clam), 93 kelp in, 28 (illust.), 28-29
My til us lead concentrations in, 92
spp. (mussels), 35, 41, 44, 63,93 sea otters in, 11 (illust.)
contaminants in, 91,92 distribution of, 11 (map)
californianus, 26, 27 population of, 74 (table)
edulis, 26, 27, 41 Pacific Valley, California, 56
Pair-bonding, 60, 64
Natality, and population changes, 81, 82 Pandion haliaetus (osprey), 93
Near Islands, Alaska, 12, 75 Panopea generosa (geoduck), 26
Nelson Bay, Alaska, 48, 57 Panthera leo (lion), 72
Nereocystis leutkeana (bull kelp), in otter habitats, Panulirus interruptus (spiny lobster), 31
23 Paracentrotus (sea urchin), 93
Nets. See Fishing Paralichthys californicus (California halibut), 86
New Zealand, algae in, 5 Paralithodes (king crab), 22
Noise, effect of waterborne and seismic, on otters, Paramushir Islands, U.S.S.R., 41, 95
19 Parasite
North America, fossils in, 3, 4 acanthocephalan, 89
Nose scars, on female otters, 61-62, 61 (illust.), 90 gastrointestinal, 89-90
Parturition, 6, 68
Oceano, California, 79 Patellogasdropoda (limpets), fossil record of, 4
Octopus. See Octopus spp. Pathology. See Disease
Octopus spp. (octopus), 31, 35,41 PCB 's. See Biphenyls, polychlorinated
Odobenids, evolution~d, 4 Pecho Rock, California, 79
Odocoileus hemionus (black-tailed deer), 65 Pelage (see also Fur), 20
Oil color of, 21
contamination, and otter mortality, 93-96 and age, 15
t

II 124 BIOLOGICAL REPORT 90 (14)

Pelecanus occidentalis (brown pelican), 93 mortality and, 81, 82-83

i
I in the North Pacific Ocean, 74 (table), 75
Pelican, brown. See Pelecanus occidentalis
Peru, marine otters in, 7 reintroduction and, 97, 99, 100
Pesticides, and otter mortality, 91-92 sex composition of, 53, 54
Pfeiffer Point, California, 55, 79 variables affecting, 81-83
Phaeophyta (fleshy brown algae), phenolics and, Port Orford, Oregon, 100
4-5 Predation, sea otter
P halacrocorax effect of, 25-28
spp. (cormorant), 19, 45 indirect, 28-31
auritus (double-crested cormorant), 93 Presbytis spp. (langurs), 72
pelagicus (pelagic cormorant), 45 Prey, sea otters', 23
Phalarope. See Phalaropusfulicarius in California, 43 (table)
Phalaropus fulicarius (red phalarope), 60 effect of oil-tainted, 94-95
Phenolics, as a defense against herbivory, 4-5 Pribilof Islands, Alaska, 73, 96-97, 102
Phoca Prince of Wales Island, Alaska, 98 n.
hispida (ringed seal), 93,95 Prince William Sound, Alaska
vitulina (harbor seal), 20,24,31,88,89,95 benthos of, 23
Phyllaria, 4 intertidal mussels in, as otter prey, 27
Phylogeny, 2-4 sea otters in, 46 (map)
Physiology, of sea otters, 13-22 aggregations of, 48, 49 (illust.)
female reproductive, 64-65 breeding season of, 59, 60, 62
male reproductive, 62 diet of, 35, 36-40 (table), 44
Pinnipeds diurnal activity cycles of, 46, 48
adaptation of, to a marine environment, 5 diving depth of, 22
diet of, 45 and Dungeness crab fishing in, 27
ingestion of oil and, 95 effect of oil spill on, 93-96
shark attacks on, 88 E. lutris nereis in, 12
Pisaster spp. (sea stars), 41 E. lutris (unnamed) in, 12
Pismo Beach, California, 27-28 foraging behavior of, 6, 7
Platichthys stellatus (starry flounder), 86 male areas of, 53
Pleurocodes planipes (pelagic red crab), 44 mortality of
Pliopedia, 4 and commercial fishing in, 87
Pneumonia, among sea otters, 89 rates in, 82
Pododesmus cepio (rock oysters), 33 movements of, 46 (illust.), 56-58, 70
Point Buchon, California, 53, 79, 92 populations of, 12, 75
Point Conception, California, 79 predation upon, 69
Point Grenville, Washington State, 99 pups of, 66-67
Point Joe, California, 48 sexual segregation among, 54
Point Lobos, California, 45, 55, 68 size of, 13
Point Lobos State Reserve, California, 24 social structure of, 48-49, 49 (illust.)
Point Piedras Blancas, California, 46, 48, 53, 54, survival rates among, 82
55,56,62,63,66,83,87 territoriality in, 63-64
Point Pinos, California, 70; 84, 88, 92 tool use among, 33
Point San Luis, California, 30, 53, 55, 79, 87 translocation of, 96
Point Sur, California, 55, 73, 76, 88 white-headed, 21
Poisoning, paralytic shellfish (PSP), 25, 45 Propellers, as a cause of otter mortality, 87
Pollutants, effect of, on sea otters' fur, 20 Protogonyaulax spp. (toxic dinoflagellates), 45
Polymorphus, 89 Protothaca (clam), 93
Population, sea otter PSP. See Poisoning, paralytic shellfish
age composition of, 53, 54 Pteronura, 2
change in, 77, 78 (table), 79 (illust.) brasiliensis (Amazonian otter), size of, 7
density of, and substrate type, 23 Pterygophora californica (articulated coralline
dynamics of, 73-83 algae), 30
growth of, 73-74,76-77 Puffinus spp. (shearwater), 45
historical, 73-75 Pugettia spp. (kelp crab), 35 (illust.), 41
 INDEX 125

Punta Abreojos, Mexico, 10 Saxidomus

Pups giganteus (butter clam), 44,45
birth weight of, 13, 14, 14 (illust.) nuttallii, 27, 44
dead, maternal behavior and, 69 Saxitoxin (STX), 45
growth and development of, 13, 69 Scallops. See Hinnites spp.
natal pelage of, 21, 23 (illust.) Scent glands, absence of, 19
newborn, 13, 14, 14 (illust.) Scent recognition, in sea otters, 5
nursing, 67 (illust.) Scorpaenichtys marmoratus (cabezon), 31
period of dependency among, 66, 67 Seabirds, otters' predation upon, 35, 44 (illust.),
relationships with mother after weaning, 70 44-45
survival rate of, 82 Sea cat. See Lutrafelina
Pupping, peaks of, 59-60, 77 Seal
Pycnopodia helianthoides (sunflower star), 31 harbor. See Phoca vitulina
northern elephant. See Mirounga angustirostris
Queen Charlotte Islands, British Columbia, 73,99 northern fur. See Callorhinus ursinus
ringed. See Phoca hispida
Rabbit. See Oryctolagus cuniculus Sea lion, California. See Zalophus californianus
Rafting sites, 50 Seaside, California, 77
Range, of sea otters, 10, 11 (map), 12 Season
expansion of, in California, 77,78 (table), 79, diet and, 41
80 (illust.), 81 (illust.) male territoriality and, 62-64
historical, 11 (map), 73 Sea stars. See Pisaster spp.
Rat Island, Alaska, 42 (map), 75 Sea urchin. See Strongylocentrotus spp.
Red Data Book. See International Union for the Conser- Sea water, otters drinking, 20
vation of Nature Segregation, sexual, among sea otters, 53
Rehabilitation, of oil-polluted otters, 96 Semicossyphus pulcher (California sheephead), 31
Reintroduction, of sea otters, 30, 41, 96-102, Sense, adaptation of sea otters' tactile, 5
97 (map), 98 (table) Sensory organs, of sea otters, 15, 19-20
Reproduction, sea otter, 59-72 Sewage, outfalls of, and otter mortality, 92
adaptation of, 6 Sex, determining, 13, 13 (illust.)
and diet, 35 Shark, white. See Carcharodon carcharias
female cycle of, 66-67 Shearwater. See Puffinus spp.
Research, on otters, and accidental mortality, 87-88 Sheep Bay, Alaska, 44
Rock greenling. See Hexagrammos lagocephalus Shell Beach, California, 79, 96, 100, 101
Runoff, agricultural, and otter mortality, 91, 92 Shemya Island, Alaska, sea urchins in, 26,
28 (illust.)
St. George Island, Alaska, 97, 102 Shooting, as a cause of otter mortality, 87
St. Paul Island, Alaska, 96-97 Shumagin Islands, Alaska, 14, 36-40 (table)
Sakhalin, U.S.S.R., 73 Sight, 19-20. See also Eye
Salinas River, California, 55, 92 Silver, 92
Salinas Valley, California, 92 Simpson Bay, Alaska, 57
Sand Hill Bluff, California, 53, 77, 79 Sirenians, 4, 5
San Francisco Bay, California, 92 Sitka Sound, Alaska, 30
San Gregorio Beach, California, 101 Size, of sea otters, 7, 13-14
San Juan Island, Washington State, 11 (illust.) Skeleton, adult female sea otter, 6 (illust.)
San Miguel Island, California, 12 Skull
San Nicolas Island, California analysis of, and taxonomic classification, 12
E. l. nereis in, 12 of a juvenile or subadult, 16-17 (illust.)
reintroduction of otters in, 31, 96, SMR. See Standard metabolic rate
101 (illust.), 102 Soberanes Point, California, 14, 19, 45, 48, 59
San Pedro Formation, California, 3 Social organization, of sea otters, 6, 9 (illust.),
San Simeon, California, 48, 55, 56, 59, 101 48-59. See also Behavior
San Simeon Point, California, 87 Soquel Point, California, 56, 77, 79, 101
Santa Cruz, California, 45, 46, 48, 53, 55 South Africa, algae in, 5
Santa Maria River, California, 77, 79, 87, 100 South America, algae in, 5
126 BIOLOGICAL REPORT 90 (14)

Soviet Union, sea otters in Tool use, by sea otters, 5, 33-34, 34 (illust.), 35
diet of, 31, 36, 36-40 (table), 40 Torch Bay, Alaska, 26
effect of, on benthic invertebrates, 25 Torre Canyon, California, 56
skulls of, 12 Toxaphene,92
Spain, fossils in, 3 Tresus nuttallii, 27, 44
Species, otters as a keystone, 25 Tributyltin, 92
Sperrnatogenesis, 61 Turban snail. See Tegula
Squid. See Loligo opalescens Twinning, 65
Standard metabolic rate (SMR), 21, 22. See also
Metabolism Uca (crab), 93
Starvation, otter mortality and, 90 Umiak Island, Alaska, 14,97
Steller's sea cow. See Hydrodamalis gigas Urchin, sea. See Strongylocentrotus
Stillwater Cove, California, 45 Urechis caupo (fat innkeeper worm), 35,41
Strongylocentrotus (sea urchin) spp., 41, 93 Urine, ingestion of, by otters in captivity, 20
barrens, Shemya Island, Alaska, 28 (illust.) Ursus
populations of, and reintroduction of otters, 26 arctos (brown bear), 6,89
predators upon, 31 maritimus (polar bear), 33,94,95
otters as, 28 (illust.), 28-29 Urup Island, U.S.S.R., 41
size of, and otter populations, 30, 73
francisanus (red sea urchin), 26, 31, Valenictus, 4
32 (illust. ), 41
Vancouver Island, British Columbia, 30, 99
polyacanthus (green sea urchin), 26,27 Variability, genetic, reduction in, and otter mortality,
purpuratus (purple sea urchin), 26,36 91
STX. See Saxitoxin
Villa Creek, California, 30
Substrate, rocky-bottom, as a sea otter habitat, 23 Vocalization, 50, 52-53
Sunflower star. See Pycnopodia helianthoides
Surf seater. See Melanitta perspicillata
Surge Bay, Alaska, 26 Walking, 15
Survival, sea otter, rates of, 82 Washington State
Sus scrafa (swine), 93 kelp forest in, 29
Swimming, sea otters' speed of, 15 sea otters in
Swine. See Sus scrafa diet of, 36-40 (table)
growth rates of, 82
Tapetum, development of, in the sea otter, 20 as a "keystone" species, 25
Taxidea taxus (badger), 65 reintroduction of, 73, 96, 99-100
Taxonomy, otter, 7-12, 12 (table) Water Pollution Control Laboratory (CDFG), 91
Teal, common. See Anas crecca Weaning, 64, 66--67, 69-70
Teeth. See Dentition Weather, adverse, and otter mortality, 90
Tegula (turban snail), 35, 41, 93 Weight, of sea otters, 13-14
Tellina spp., 41 Whale, killer. See Orcinus orca
Territoriality Wolf-eel. See Anarrhichthys ocellatus
among male sea otters, 62--64 Worm, fat innkeeper. See Urechis caupo
and kelp beds, 23
Territory. See Habitat Yakutai Bay, Alaska, 98 n.
Tillamook Bay, Oregon, 82 Yankee Point, California, 56
Time budgets Yaokbi Island, Alaska, 98 n.
of females with pups, 68
for sea otters' activities, 45--48 Zalophus californianus (California sea lion),
Timms Point Silt Member. See San Pedro Formation 19-20,93
Tivela stultorum (Pismo clam), 26, 27-28, 41-44 Zinc, 92
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Riedman, Marianne L. and James A. Estes. 1990. The Sea Otter (En- Riedman, Marianne L. and James A. Estes. 1990. The Sea Otter (En-
hydra lutris): Behavior, Ecology, and Natural History. U.S. Fish hydra lutris): Behavior, Ecology, and Natural History. U.S. Fish
Wildl. Serv., Bioi. Rep. 90 (14). 126 pp. Wildl. Serv., Bioi. Rep. 90 (14). 126 pp.

This monograph provides a comprehensive review of the biology of This monograph provides a comprehensive review of the biology of
the sea'otter (Enhydra lutris) and includes a summary and synthesis of the sea otter (Enhydra lutris) and includes a summary and synthesis of
information on the following subjects: phylogeny and evolution, syste- information on the following subjects: phylogeny and evolution, syste-
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This monograph provides a comprehensive review of the biology of the sea This monograph provides a comprehensive review of the biology of the sea
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otter (Enhydra lutris) and includes a summary and synthesis of information on otter (Enhydra lutris) and includes a summary and synthesis of information on
the following subjects: phylogeny and evolution, systematics, morphology, the following subjects: phylogeny and evolution, systematics, morphology,
physiology, habitat, community ecology, foraging behavior, activity, social physiology, habitat, community ecology, foraging behavior, activity, social
organization, movements and home range, reproduction, mortality, population organization, movements and home range, reproduction, mortality, population
dynamics, and reintroductions. dynamics, and reintroductions.

Key words: ecology, evolution, foraging, life history, morphology, physiology, Key words: ecology, evolution, foraging, life history, morphology, physiology,
reintroduction, sea otter, social behavior. reintroduction, sea otter, social behavior.
 TAKE PRIDE
in America l'.S.
FlSI-I &WILllJ.J}'E.
SERVIC:f<:

U.S. DEPARTMENT OF THE INTERIOR

FISH AND WILDLIFE SERVICE

As the Nation's princ1pa1 conservation agency, the Department of the Interior has responsibility for most
of our nationally owned public lands and natural resources. This includes fostering the wisest use of our
land and water resources, protecting our fish and wildlife, preserving the environmental and cultural
values of our national parks and historical places. and providing for the enjoyment of life through outdoor
recreation. The Department assesses our energy ar:d mineral resources and works to assure that their
development is in the best interests of all our people. The Department also has a major responsibility for
American Indian reservation communities and for people who live in island territories under U.S.
administration.