Reproduction

Social Organization and Mating Behavior

Bulls are belligerent when they arrive on the rookery at the start of the breeding season, threatening and fighting with each other in areas where females will settle to give birth. When pregnant females begin arriving, they seek each other out for safety from the sexually aggressive males and gather in groups, or harems. The result of the fierce, bloody encounters between males is a dominance hierarchy at each breeding area (Le Boeuf and Peterson 1969; Le Boeuf 1974; McCann 1981). This social structure effectively reduces access to the grouped females to a few of the highest-ranking males in the area. One male, the alpha or beachmaster, dominates all other males and keeps them away from females with the species-specific threat vocalization delivered with the head and neck elevated, braced up with the foreflippers. The second-ranked male keeps all other males away from females, too, but defers to the top-ranked male, and so it goes with decreasing rank. Social rank is directly associated with access to females; the alpha bull situates himself in the middle of the group of females. Although small harems of 100 females or less may be ruled by one bull, as the female group increases in number, it becomes too time- and energy-consuming for the alpha male to keep all other males out. Other males, next in rank, take up peripheral positions in the harem. In small colonies, the harems are smaller and discrete, each controlled by a single dominant bull, with subordinate bulls positioned around but outside the harem. In very large colonies, like

some beaches at South Georgia, there may be a nearly continuous mass of breeding females stretching for a kilometer or more, without individual harems. Alpha males and subordinate bulls are then positioned at intervals among the females (Laws 1956a ).

Mating Success of Males

The ultimate result of this power structure is that few males mate, and male mating success is directly related to social rank in the dominance hierarchy. At Año Nuevo, as few as 5 out of 180 males were responsible for up to 92% of the copulations observed with up to 470 females during a breeding season; one male held the alpha position in a large harem and dominated mating for four consecutive years, inseminating an estimated 200 females (Le Boeuf 1974). In the southern elephant seal, M. N. Bester and I. S. Wilkinson (this volume) recorded that "dominant bulls controlling the harems achieved over 98% of all matings."

A study of lifetime reproductive success at Año Nuevo confirms that there is great variance in male reproductive success (Le Boeuf and Reiter 1988). In a sample of 91 male pups, only 19 reached breeding age. Three males were extremely successful, inseminating an estimated 121, 97, and 63 females, respectively; 5 other males apparently inseminated 69 females, and the remaining 11 surviving males (as well as the 72 nonsurvivors) failed to mate. The males most successful at mating achieved high ranks in the dominance hierarchies associated with harems.

Although males undergo puberty at about 5 years of age in the northern species and 4 to 5 years of age in the southern species, they do not achieve high rank until they are older, at least eight years of age, and larger (Laws 1956a ; McCann 1985; Clinton, this volume; Deutsch et al., this volume). Prime breeding years for northern males are at age 9 to 12, males are in decline at age 13, and 14 years is the maximum life span (Le Boeuf and Reiter 1988). The majority of breeding bulls in the southern species are also 9 to 12 years old, but the maximum life span is 20 years (Laws 1953a ; McCann 1985). Despite the predominance of adult males in mating and male-male competition, four other categories of subadult males (SAMs) are present during the breeding season: SAM1 = 4 years old, SAM2 = 5 years old, SAM3 = 6 years old, and SAM4 = 7 years old (Le Boeuf 1974; Cox and Le Boeuf 1977; Clinton, this volume).

The Reproductive Cycle of Females

There is strong circumstantial evidence that most females of both species mate for the first time at sea (Laws 1956a , 1956b , this volume; B. J. Le Boeuf, unpubl. observ.). At Año Nuevo, only a few identifiable (marked) virgin females mate on land each year, late in the breeding season; the vast majority must mate at sea because they are not observed elsewhere on land,

either at this time or later in the season. Studies on the southern species demonstrated that in parous females, after copulations and fertilization, development is suspended and the blastocyst remains free in the uterus for about 4½; months; implantation occurs at the end of the summer molt, and active embryonic growth occupies about 7½; months (Laws 1956b ).

Within 6 days after a pregnant northern elephant seal arrives on the rookery during the breeding season, she gives birth to a single pup (this period in the southern elephant seal is 5 days). She keeps it near her and nurses it daily for 27 days (23 days in the southern elephant seal), all the while remaining in the harem and fasting from food and water. During the last 3 to 5 days of nursing, she copulates (about 4 days in the southern elephant seal). Four weeks after giving birth, 34 days after arriving on the rookery (28 days in the southern elephant seal), and on her last day of estrus, the female weans her pup by returning to sea (Le Boeuf, Whiting, and Gantt 1972; Laws 1953b , 1956a , 1956b ).

Age at Primiparity and Natality

In expanding colonies in northern California, females give birth for the first time at age 3 to 6, with 4 years of age being the mean age at primiparity (Reiter, Panken, and Le Boeuf 1981; Huber 1987; Le Boeuf and Reiter 1988). High local density of breeding females is correlated with deferred maturity (Huber et al. 1991). Most females produce a pup annually until they die at a maximum age of about 20 years; however, skipping a year has been observed in some rookeries, especially following first breeding (Huber 1987; Huber et al. 1991).

At South Georgia, M. leonina females also give birth for the first time at age 3 to 6, the majority at age 4. At Macquarie Island, there was deferment of the range and mean by one year (McCann 1980; Carrick et al. 1962). The reason for the difference is not clear, although body growth rates are lower at Macquarie Island. M. A. Hindell and G. J. Little (1988) report two known-age females observed suckling pups on Macquarie Island at age 23.

Female Reproductive Success

Female weaning success increases with age up to at least age 8 (Reiter, Panken, and Le Boeuf 1981; Le Boeuf and Reiter 1988; Huber 1987; Huber et al. 1991; Sydeman et al. 1991; Deutsch et al., this volume). Reproductive experience may have a positive (Reiter, Panken, and Le Boeuf 1981) or a negative effect on subsequent weaning success (Sydeman et al. 1991; Sydeman and Nur, this volume). An important factor in weaning success is female mass, which increases with age (Deutsch, this volume). At Año Nuevo, older, larger females dominate younger, smaller females, displacing them or their pups and preempting areas in the harem that are less prone to nursing disruptions caused by peripheral males or high water (Christenson and Le Boeuf 1978).

Preweaning Pup Mortality

The major cause of pup mortality on the rookery and lack of weaning success is the trauma-starvation syndrome that begins with mother-pup separation and ends with starvation or lethal injury inflicted by adults (Le Boeuf and Briggs 1977). Trauma results from crushing by breeding bulls, or from orphaned pups being bitten while attempting to suckle alien females. Three classes of variables affect motherpup separation and increase pup mortality either directly or indirectly: female aggression; the number; distribution, and density of females; and winter storms that flood the harems at peak season.

An important variable affecting the maximum pup mortality rate is the size of the breeding unit in relation to the topography of the breeding site. At Año Nuevo, if mothers and their pups can move inland to higher ground when surf and high water threatens, such as occurs on large island beaches or mainland breeding sites, the annual pup mortality rate is usually less than 10% of pups born. If, however, there is no fallback position, due to wave cut platforms or high cliffs, the pup mortality rate may rise to 75 to 100% (Le Boeuf and Condit 1983; Stewart and Yochem 1991). On northern elephant seal island colonies, where the pup mortality rate has been monitored closely, the annual rate is usually in the range of 10 to 40% (Le Boeuf and Reiter 1991; Huber, Beckham, and Nisbet 1991). In the southern species, it has been recorded at 2 to 6% on average (Laws 1953b ; Condy 1978). It is higher in unfavorable conditions. Thus, at South Georgia, in some situations on land at the beginning of the season, pups melted deep holes in the snow, which prevented them from sucking and resulted in mortality as high as 30%. Mortality (80%) was associated with ice-breeding colonies at Signy Island due to breakup of the fast ice in storms (Laws 1953b ).

Nursing and Adoption

Most females nurse their own pups exclusively until weaning; however, some females that lose their own pups adopt orphans and raise them as they would their own. In a study by M. L. Riedman and B. J. Le Boeuf (1982) at Año Nuevo, 5% of the orphans reunited with their mothers, 27% were adopted or frequently cared for by foster mothers, and 68% remained orphaned and died. Since young, inexperienced females most often lost their pups, they were the ones most likely to foster an orphan. Usually, they adopted pups that were the same age as those they had lost. Adoption of a single pup was most common, but pupless females also attempted to steal suckling pups, adopted a weaned pup, adopted two pups, or indiscriminately nursed any orphan that approached. Nursing between unrelated cows and pups has been observed in southern elephant seals, but it is unusual. Orphaned pups that attempt to steal milk are usually unsuccessful (McCann 1982).

At Año Nuevo, a few "superweaners" may be produced when pups are

suckled by two "mothers" or are adopted by a pupless female after being weaned by their own mother (Reiter, Stinson, and Le Boeuf 1978; Le Boeuf 1981). These weanlings may attain twice the mass of normal weanlings. In addition, some weanlings attempt to steal milk from nursing females by stealth or perseverance; the majority of these milk thieves are males.

Philopatry and Site Fidelity

Like most other pinnipeds and many terrestrial mammals, most female elephant seals give birth on the rookery where they were born in roughly the same site from year to year. Seventy-one percent of the females born at Año Nuevo during the 1970s returned to give birth there for the first time (Reiter, Panken, and Le Boeuf 1981). The rest moved to adjacent rookeries as their birth site became crowded (Le Boeuf, Ainley, and Lewis 1974). Similarly, 70% of females monitored returned to give birth at the original site the following year. Movement to a new site was associated with failing to wean a pup or high density of breeding females. Similarly, D. G. Nicholls (1970) reported that at Macquarie Island, 77% of branded cows up to 11 years old were found breeding within 4 km of their birth site, and Hindell and Little (1988) reported two 23-year-old cows breeding within 1 km of their birth site.