The California, Galapagos, and Japanese sea lions are » closely related species that together comprise the genus – Z/ilophus. They occupy (or occupied, in the case of the presumably extinct Japanese sea lion) widely separated regions of the Pacific, including the temperate western and eastern North Pacific and the tropical Galapagos Archipelago (Fig, 1). The varying environmental conditions experienced throughout this range, along with the corresponding variations in behavior, provide fascinating insights into their behavioral ecology.
I. Taxonomy and Distribution
The California, Galapagos, and Japanese sea lions are now regarded as separate species: Z/iloplws californianus (Lesson, 1828), Z. wollebaeki (Sivertsen, 1953), and Z. japonicus (Peters, 1866), respectively. Previously they were typically considered to be geographically isolated subspecies (Z. californianus californianus, Z. c. wollebaeki, and Z. c. japonicus), but recent discoveries of substantial morphological and behavioral differences among them led to their reclassification. Further studies are needed to delineate the differences among species and to identify any subspecies or stocks. Differences in mitochondrial DNA indicate that the Pacific and Gulf of California populations of California sea lions have long been genetically isolated. However, no differences have been found in the cranial morphology of the two populations, and subadult males appear to migrate between colonies in the southern Gulf of California and those along the Pacific Coast of Mexico. The degree of interchange between Mexican and U.S. populations is not known. The main breeding areas of California sea lions include the Channel Islands in southern California and Mexican islands off the Pacific coast of Baja and in the Gulf of California. Rarely, births may occur as far north as the Farallon Islands off central California. Outside the breeding season, animals (mostly males) are common as far north as Vancouver Island. Vagrants occur as far north as Prince William Sound, Alaska, and as far south as Chiapas, Mexico. Females and immatures may disperse from the breeding islands to forage, but apparently do not migrate as extensively as males.
Galapagos sea lions breed on all the islands of the archipelago. In 1986 a small rookery was established outside of the Galapogas on Isla de La Plata off the coast of Ecuador. Vagrants have been reported along the mainland coast of Ecuador and on Islas del Coco (Costa Rica) and Gorgona (Columbia).
Although historical and archaeological records are incomplete, Japanese sea lions appear to have lived in coastal areas from Kyushu to southern Kamchatka. Their range was likely centered along the west and east coasts of Honshu, off Shikoku and Kyushu, in the Seto Inland Sea, and on islands in the Sea of Japan and the Izu region. Known rookeries include Take-shima and Ullung-do in the southern Sea of Japan, the northwest and also central-eastern coasts of Honshu, and four islands in the Izu region. Vagrants have been noted to southwestern Sakhalin, the Kuril Islands, southern Kamchatka, and the east coast of South Korea.
II. Population Trends and Exploitation
The annual return of pinnipeds to predictable breeding areas makes them particularly vulnerable to exploitation. Subsistence hunting of California sea lions probably occurred for several thousand years without much of an effect on the population. However, commercial harvesting during the 1800s and early 1900s in southern California and Mexico reduced the population to only about 1500 animals by the 1920s. The harvest, which at various times was for hides, blubber, meat, predator control, or the whiskers and bacula sold as aphrodisiacs, probably focused on adult males. A floundering market coupled with protective legislation allowed the population to start increasing by the 1940s, although some killing and live collecting continued until the 1970s. The 1972 U.S. Marine Mammal Protection Act and similar legislation in Canada and Mexico greatly facilitated the population’s recovery. The U.S. population of California sea lions is currently estimated to be 167,000-188,000, with about 34,000 pups produced annually. Overall, the population is increasing at a rate of roughly 5% per year; however, periods of growth are frequently reversed during strong El Nino events. A 1992 census of the Mexican Pacific coast recorded about 10,000 California sea lions, compared to nearly 28,000 counted a decade earlier (Maravilla and Lowry, 1996). Allowing for uncensused animals at sea, the current Mexican Pacific population may be roughly 13,000 to 22,000. Clearly the population fluctuates in this region; its relationship to changes in the U.S. population is not known. A 1992 census of the Gulf of California population recorded about 23,000 animals; correction factors yielded a population estimate of about 31,000 (Aurioles and Zavala, 1994). Thus, the total California sea lion population is about 211,000-241,000.
Figure 1 Ranges of California, Galapagos, and Japanese sea lions.
The Galapagos sea lion has been largely spared the commercial exploitation that depleted the California sea lion population. However, the number of Galapagos sea lions apparently does fluctuate frequently due to El Nino events and epidemics of seal pox. The population was estimated at 20,000-50.000 in 1963. Following the 1997-1998 El Nino, which was accompanied by up to 90% pup mortality and 45% overall mortality, the population was estimated at only about 14,000 individuals (Salazar, 1999).
Between 30,000 and 50,000 Japanese sea lions may have existed in the mid-1800s. Heavy, unregulated hunting depleted the population such that by the 1950s 50 to 60 animals on Take-shima were the only ones reported. The IUCN lists the species as extinct; some scientists believe this status needs to be confirmed by surveys in remote regions.
III. Habitat and Environment
California and Galapagos sea lions breed on sandy beaches and rocky areas on remote islands. Because females must forage at sea during lactation, breeding areas are restricted to regions of high marine productivity. California sea lion rookeries along the Pacific coast are in a very productive upwelling zone, and productivity in the Gulf of California is also very high due to tide- and wind-generated upwelling. The waters of the continental margin adjacent to areas once used by breeding Japanese sea lions are quite productive. While low productivity generally excludes otariids from breeding in the tropics, the islands in the Galapagos Archipelago are bathed in nutrient-rich upwelling currents. This creates an isolated pocket of high productivity, which supports the Galapagos sea lions. The importance of high productivity can be seen in the devastation that occurs during El Nino events, when a plume of warm, nutrient-poor water emanating from the equatorial Pacific decreases the availability of the sea lions’ prey. These frequent, but unpredictable events are most severe in the eastern tropical Pacific where the Galapagos sea lion lives, with lesser impacts at the higher latitudes occupied by California and Japanese sea lions. Sea lions living in the Gulf of California, Mexico, may be largely protected from the effects of El Ninos; strong tidal mixing there should be able to resupply nutrients to surface waters during an El Nino event.
The breeding habitat occupied by Zalophtis ranges from temperate to tropical regions. As a result, breeding animals are often subjected to high temperatures while on land. The affects of these high temperatures and of El Nino events are described in Section VIII.
IV. Description
California sea lions are highly sexually dimorphic: the weight and length for adult males is about 350 kg and 2.4 m compared to about 100 kg and 1.8 m for adult females. Males in the Gulf of California appear to be smaller than their Pacific counterparts. Newborn California sea lion pups weigh 6-9 kg for females and males, respectively. They are dark brown to black until they molt to a tawny brown color at 4-6 months (Fig. 2). Females remain this color throughout adulthood, whereas male coats typically darken as they age. Adult males usually are a dark brown, but can range from light brown to black. All individuals appear darker when wet. It is difficult to distinguish females from young males until the latter begin developing the broad chest, dark color, and sagittal crest of adult males (Fig. 3). The sagittal crest, which is unique to Zalophus, is usually topped by white fur and is quite conspicuous. Galapagos sea lions are smaller than California sea lions and appear to be much less sexually dimorphic. Females weigh about 80 kg. No weights are available for males. Young California and Galapagos sea lions are especially playful, spending much time chasing and mock fighting with each other, playing with objects such as kelp and feathers, and bodysurfing. All age classes are fairly vocal; territorial males are exceedingly so. Little is known about the physical characteristics of the Japanese sea lion.
Figure 2 An adult female California sea lion suckling her pup after returning from a feeding trip at sea. Photo by C. B. Heath.
Figure 3 An adult male California sea lion on his territory. The broad neck and chest are indicative of an adult male; the fat deposits they contain will sustain him tvhile fasting for the duration of his tenure. Note the pups playing in protected shallow waters.
V. Life History and Annual Cycle
In southern California, where California sea lions have been studied extensively, animals can be found on the breeding islands year-round. The number ashore increases rapidly in May with the onset of the breeding season. At this time adult males begin fighting for territories along the shorelines of the rookeries. Most are unsuccessful and retreat to sea or to “bachelor” beaches nearby. Those that establish territories maintain their boundaries with ritualized displays and frequent barking. Territorial males fast throughout their tenure, surviving on fat accumulated during the off-season. Tenure lasts from 1 to 45 days and may end when residents are displaced by another male or when their fat reserves are depleted. Some males maintain territories for multiple breeding seasons. Throughout May and June females give birth to a single pup a few days after coming ashore. Vocal and olfactory imprinting follows birth and is used by mothers and pups to reunite after separations (Fig. 4). Mothers spend the first week postpartum with their pup and then begin alternating feeding trips at sea with suckling bouts on land. The feeding trip length is largely determined by the distance to the foraging grounds and the availability of prey. It averages 2-3 days, but varies with location and year. Stays on land average 1-2 days. This pattern continues until the pup is weaned. Most pups are weaned by 10-12 months of age. The number that continue to suckle as yearlings or even 2 year-olds varies among years (Francis and Heath, 1991). Females mate about 27 days after giving birth, an unusually long interval for otariids. Not all females breed every year. At many rookeries, females form “milling” groups as a prelude to mating (Fig. 5). In these groups of 2-20 females, the females often mount each other and the territorial male. Eventually 1-2 of the females mate and the milling activity ends (Heath, 1989). While ashore, both males and females make regular movements to the water to cool off (Peterson and Bartholomew, 1967).
Figure 4 An adult female California sea lion vocalizes to her newborn pup. Mothers and pups imprint on each others’ calls and smell at birth, which helps them recognize each other and reunite after separations. Note remnants of amniotic sack on pup.
After the breeding season ends in August, most adult and subadult males leave the southern California rookeries and migrate north, where they feed throughout the fall and winter. Females and juveniles appear to disperse to feed in the general vicinity of the breeding islands. Pup mortality is roughly 15-20% for the first 6 months of life. In the southern Gulf of California, at least, it then increases to about 40% for the next 6 months as pups venture into the water (Aurioles and Sinsel, 1988). Sexual maturity occurs at about 4-5 years of age, although males are not large enough to hold breeding territories for several more years. Longevity is estimated at 15-24 years. Sources of mortality include starvation, infection, sharks, killer whales, toxic phy-toplankton blooms, entanglement, shooting, and disease.
California sea lions living in the Gulf of California, Mexico, experience a similar annual cycle with some notable differences. The pupping season lasts 1-2 weeks longer for at least some rookeries in the northern half of the Gulf (Morales, 1990), and the interval between birth and mating appears more variable than in the U.S. population (Heath, 1989). About 40% of the adult males in this region remain around the breeding islands year-round (Zavala, 1990), and the age of weaning appears to be both older and more variable than in southern California (Heath et al., 1996).
The breeding season is very protracted in the Galapagos sea lion, and territorial males are observed most of the year. Births occur from June to March, but the peak pupping period varies among rookeries and years. The interval between birth and mating has been estimated at about 3 weeks. Territorial males sometimes go to sea to feed, thus often losing their territory to another male, but sometimes reclaiming it upon their return. Migration within the archipelago is minimal. Normal pup mortality to age 6 months is about 5%. Most pups are weaned within 1 year, but may continue to suckle as yearlings or 2 year olds if their mother does not have a new pup.
As with all other parameters, we have virtually no information regarding the life history of Japanese sea lions.
VI. Social Relationships
California sea lions are highly intelligent and adaptable animals, capable of learning a simple sign language in captivity (Schusterman and Krieger, 1986). Both California and Galapagos sea lions can recognize individuals in the wild through scent, sound, and probably sight. They are also gregarious animals, with much opportunity for social interaction during the breeding season, at least. These traits would seem to dispose them to sustained relationship with other individuals; however, the only obvious social unit is between mothers and their offspring. Perhaps longer term studies of permanently marked individuals will reveal other types of relationships.
VII. Diet
California sea lions eat a wide variety of prey, which is determined to some degree by its relative availability. The most common prey items in southern California are northern anchovy, Pacific whiting, rockfish, cephalopods, jack and Pacific mackerel, and blacksmith (Lowry et al, 1986). The first three species are also important in the Mexican Pacific and Gulf populations, as are midshipmen. Myctophids, sardines, cutlassfish, alopus, cusk eels, and bass are frequently prey in various areas of the Gulf (Sanchez, 1992). Diet varies greatly among years, seasons, locations, and probably individuals. El Nino events cause shifts in the diet, and species otherwise rarely consumed, such as the pelagic red crab, may become more common in the diet. Feeding can occur at any hour of the day. Dives typically last for about 2 min, but can be as long as 10 min. Dive depth averages 26-98 m, but can be well over 200 m (Feldkamp et al, 1991). The staple of the Galapagos sea lion diet is sardines. During El Nino events, however, partial shifts to green-eyes (1982-1983) and myctophids (1997-1998) have occurred (Trillmich and Dellinger, 1991; Salazar, 1999). Galapagos sea lions forage within a few kilometers of the coast, feeding during the daytime on a near-daily basis. Dive depth averages 37 m, but can reach 186 m. There is no information on what the Japanese sea lions ate.
Figure 5 A “milling” group of California sea lions. These groups form in some areas as a prelude to mating. Females often mount each other or the territorial male while in these groups. Note the male’s saggital crest, which is unique to Zalo-phus.
VIII. Behavioral Ecology
Life is a compromise, and pinnipeds have evolved many adaptations in response to the sometimes conflicting pressures of breeding on land and feeding at sea. Certain environmental conditions can increase the costs or benefits of some of these adaptations and bring about compensatory changes in behavior. Two such conditions—high air temperatures on rookeries and decreased prey availability during El Nino events—play particularly important roles in shaping the breeding and foraging behavior of California and Galapagos sea lions.
A. Temperature and Its Effects on Breeding Behavior
California sea lion females are very particular about male behavior. Boisterous, overly attentive, or aggressive males are typically abandoned and left to sit alone on their territories. Any interference with female movements is simply not tolerated. Should a male attempt to block a female’s path, she needs only to extend her neck out and up, and sway it side to side as she walks. This long-neck display signals males that she requires free passage; the rare male that does not respond to this will likely be subjected to a display of jerky hopping and flipper slapping, which will dissuade him from interfering further. Males seem to have little option but to acquiesce if they are to be successful at breeding.
Why might this situation exist, especially in such apparent contrast to some otariid species where females may be herded, threatened, and even injured by territorial males? The explanation appears to partly lie in the animals’ thermoregulatory needs. The particularly warm climate in which Zalophus breed increases the cost of moving between marine and terrestrial habitats. The blubber, fur, and large size, which insulate against cold ocean waters, can lead to overheating while ashore, thus making necessary regular access to wet substrate or water for cooling. The breeding fat of adult males intensifies their thermal stress, thereby limiting the distribution and number of territories. Successful males have territories containing access to water; others must abandon their territories (and any hopes of mating) during the heat of the day. Breeding females must also have access to cooler shoreline areas on a near-daily basis, and they regularly travel through several males’ territories while moving from resting to cooling areas. Furthering this pattern of female movements is the unusually long interval (about 21-27 days) between birth and mating. During that interval females must also make regular feeding trips to sea to replenish their milk supplies. A male that prevented these premating thermoregulatory and feeding excursions by herding the females would be left with, at best, only severely stressed females, which are not likely to mate. Thus the combination of warm breeding areas and delayed mating together foster a system in which males may control each other, but not the females. Rather, when it is time to mate, many females leave the male’s territory in which they have given birth and mate with another male that they may have encountered in their movements about the rookery. Females show a surprising degree of unity in their selection of mates. As a result, many males holding territories during the breeding season never or rarely mate, while a few males mate with many females (Heath, 1989). This dramatically increases the degree of polygyny in California sea lions: males make the first cut by excluding many of their gender from the rookeries and females make another cut via their selection of mates.
The influence of temperature on behavior can also be seen in the high percentage of copulations that occur in contact with the water. This percentage increases in hotter regions, as does the amount of time females spend cooling off at the shoreline. In the Gulf of California, where air temperatures are very high, nearly all territorial defense and breeding activities are restricted to the water (Garcia, 1992; Heath, 1989).
Galapagos sea lions show a similar response to high air temperatures with their great reliance on shoreline areas for cooling. However, observations of their breeding behavior are inadequate to compare to California sea lions. Environmental conditions in at least part of the former range of the Japanese sea lion are similar to those of its congeners. However, barring the discovery of historical records, we will never know if their behavioral responses were the same as those of the California and Galapagos sea lions.
B. Responses to El Nino
The environmental changes that occur during El Nino events also elicit behavioral responses by Zalophus. However, unlike the fairly constant heat stress experienced on rookeries, the environmental stresses associated with El Nino are unpredictable and only occur every few years. In addition, because the degree of stress varies among events and locations, the sea lions’ responses must be somewhat flexible. El Ninos cause a reduction in prey availability for Zalophus throughout much of its range. The potential consequences of this reduction are mitigated somewhat by adaptations that have evolved over the sea lions’ long history of coexistence with El Ninos. However, the severe impacts of some El Nino events demonstrate the limits of these adaptations. The 1982-1983 El Nino was a particularly strong one, and much is known about its effects on the California sea lions that breed in southern California. Some non-breeding sea lions in this region responded to local prey depletion by migrating north to more productive areas. Many im-matures and some adult females left their normal winter foraging areas and migrated to central California (Huber, 1991). Emigration was thus apparently an option for some individuals to reduce the effects of El Nino. Territorial males in southern California showed no measurable affects from this event, most likely due to their preseason foraging farther north. Adult females, however, appeared to be more tied to the general vicinity of the breeding sites, where prey reduction was more pronounced. The increase in spontaneous abortions during the 1982-1983 winter indicates that some of these females were unable to find adequate prey (Francis and Heath, 1991). Females that did manage to produce full-term pups then faced the greater challenge of nourishing them. Feeding during lactation makes females quite vulnerable to localized decreases in food availability. In southern California they attempted to compensate for decreased prey by increasing their foraging effort while at sea, partially shifting their prey, and by slightly prolonging their feeding trips (Lowry ct al, 1986; Ono ct al, 1987). These efforts, however, were inadequate to compensate for the strength of the 1982-1983 El Nino. Females apparently made less milk: pups suckled less, grew more slowly, and weighed less at age 2 months (Ono et al, 1987). Pup mortality increased, and pup production decreased by 30-71% at various islands. Fewer of the male pups were weaned by age 1 year, and more of them stayed on their birth island and suckled into their second year. Fewer females mated during the El Nino summer, presumably a sign that they were undernourished. As a result, pup production was still low in the following year. Because pup production took several years to return to pre-El Nino levels, it is possible that there may have been some mortality of breeding females and juveniles associated with this event. In Mexico, pup production on at least one Pacific island decreased by 50% during the 1982-1983 El Nino, while effects appeared to be very weak in the Gulf (Aurioles and Le Bouef, 1991). An even stronger El Nino occurred in 1997-1998. While not as widely monitored for its effects on California sea lions, they appear to have been even greater.
The reduction of prey during El Nino events is particularly strong in the eastern tropical Pacific. Because Galapagos sea lions are isolated from alternative feeding areas by vast expanses of unproductive tropical waters, emigration to better feeding areas is not an option for them. Mortality has thus been very high for this species during El Nino events. Between 80 and 95% of the pups born in 1982 did not survive their first year of life. Pup production at various rookeries in 1983 was between 3 and 65% of normal years. Adult female mortality was estimated at 20%, and territorial male mortality was particularly severe (Trillmich and Dellinger, 1991). During the 1997-1998 El Nino, pup mortality was close to 90%, and mortality for the overall population was about 45% (Salazar, 1999).
Oceanic conditions also change in Japan during El Nino events, but what effects this may have had on the Japanese sea lions is not known.
The oceanographic counterpart to El Ninos are Las Ninas, periods of generally cooler ocean temperatures and greater productivity. Little is known of their effects on pinnipeds or any role they might play in the recovery from El Nino events.
IX. Interactions with Humans
Like all marine mammals, California and Galapagos sea lions spend a good portion of their lives in remote areas or underwater, hidden from our view. However, the California sea lion is one of the most familiar marine mammals. This is due in part to their being the most commonly used “seal” performer in animal park shows and also to their habituation to human presence in some areas, especially where there is a comfortable dock or buoy to be acquired by this tolerance. These activities are indicative of their intelligence and flexible nature, which itself can sometimes lead to less positive interactions with humans.
A. Fisheries Interactions
Enviable hunter or lowly thief? The answer to this question is largely a matter of perspective. Certainly, California sea lions are highly skilled at catching their prey of fish and squid, and their growing population consumes many tons of them yearly. As with many predators, they are also flexible and opportunistic in their search for food, as their diet and thus foraging patterns vary with age, location, and environmental changes caused by things such as El Nino and commercial fishing. While this flexibility is partly responsible for the recovery of this species, it at times also brings them into direct competition with human fisheries. Healthy populations of fish, sea lions, and humans have coexisted throughout much of our history; however, the demand for marine resources generated by a rapidly increasing human population, coupled with its increasingly efficient exploitation of those resources, has heightened concerns about competition between humans and other marine predators. This, combined with the highly visible actions of individual sea lions that have learned to exploit the easy take from fishing lines and nets, has led some to view California sea lions as marine pests rather than an integral part of a healthy ecosystem.
B. Habitat Overlap
Another form of competition occurs when sea lions make themselves at home on docks and other man-made resting areas. While this can be quite inconvenient, in areas such as Pier 39 in San Francisco, the situation has been converted into a popular tourist attraction.
C. Pollution
The growing arsenal of toxic chemicals and waste that makes its way into marine mammals’ habitats and prey has generated much concern. This is particularly relevant for the Channel Islands population of California sea lions; their proximity to the major metropolitan areas of southern California exposes them to a great deal of urban and industrial runoff, waste, and debris. Because they are high-level predators, sea lions are vulnerable to compounds such as organochlorines (e.g., DDT and PCBs) that become increasingly concentrated as they move up the food chain. Laboratory studies of such compounds have revealed that they can suppress pinniped immune systems, rendering them more vulnerable to disease. However, establishing such clear cause-and-effect relationships in wild populations exposed to organochlorines is more difficult due to confounding factors. California sea lions were found to have elevated levels of organochlorines associated with increased stillbirths and premature pupping, but the level of contribution of disease to this problem could not be determined. Although the specific links among chemicals, immune system responses, and disease or mortality are incompletely understood, enough indications of problems exist to warrant caution and further research.
D. Entanglement
Entanglement with marine debris is a problem found in all populations of California and Galapagos sea lions. Materials such as packing bands and discarded fishing line or nets can become caught on the animals’ necks or flippers, leading to injury, infection, reduced feeding efficiency, or death. Sea lions are also killed incidentally in some fisheries.
The southern California population of California sea lions is currently thriving and is thus apparently quite able to recover from its interactions with humans. The extinction of the Japanese sea lion, however, reminds us that there can be limits to this recovery. This is especially true for smaller populations, such as those of the Galapagos sea lions or the Mexican population of California sea lions. If harmful human activities were to increase substantially or happened to coincide with natural stresses such as epidemics or El Nino events, recovery might not be so rapid or complete.
