Fostering behaviour and milk stealing in Antarctic fur seals

N. J. LUNN British Antarctic Survey, Natural Environment Research Council, Madingley Road,

Cambridge CB3 OET, United Kingdom

Received August 16, 1991 Accepted November 6, 1991

LUNN, N. J. 1992. Fostering behaviour and milk stealing in Antarctic fur seals. Can. J. Zool. 70: 837 -839. During the lactation period, female otariid seals alternate trips at sea to feed with visits ashore to nurse their pups. A female

returning ashore must be able to recognize her own pup, and it is generally agreed that this is facilitated by auditory and olfactory cues. Instances of fostering behaviour (females nursing nonfilial pups) and milk stealing are reportedly rare among the otariids. In the austral summer of 1989, I observed eight and two instances of fostering behaviour and milk stealing, respectively, by Antarctic fur seals at Bird Island, South Georgia. The following summer, 26 cases of fostering behaviour and 71 cases of milk stealing were documented. In 1990, females appeared to have difficulty acquiring sufficient resources to feed their pups, so nutritional stress was probably responsible for the increase in milk stealing. The occurrence of fostering behaviour suggests that mothers were unable to recognize their own pups, although in the above cases the cause was not clear; neither human disturbance nor density appeared to be the primary factor. Maternal experience may have been a factor in 1990, as 10 of 1'4 females fostering pups were 5 years of age or less and had given birth to either their first or second pup.

LUNN, N. J. 1992. Fostering behaviour and milk stealing in Antarctic fur seals. Can. J. Zool. 70 : 837-839. Au cours de la pCriode d7allaitement, les otaries femelles alternent leurs excursions en mer pour se nourrir et leurs visites

aux rives pour nourrir leurs petits. Une femelle qui retourne B la rive doit pouvoir reconnaitre son petit et 1,011 croit gCnCrale- ment que ce processus se fait par 17intermCdiaire de l'audition et de l'olfaction. Les cas d'(( adoption n (i.e., allaitement de petits non apparent&) et de vol de lait semblent rares chez les otariidCs. Au cours de 17CtC austral de 1989, j'ai observC 8 cas d'adoption et 2 cas de vol de lait chez des Otaries B fourrure de 1'Antarctique dans l'ile Bird, Georgie du Sud. Au cours de 1'CtC suivant, 26 cas d'adoption et 71 cas de vol de lait ont CtC rapportCs. En 1990, les femelles semblent avoir CprouvC de la difficult6 B acquCrir suffisamment de ressources pour nourrir leurs petits et l'augmentation des cas de vol de lait semble donc attribuable B des stress alimentaires. Les comportements d'adoption indiquent que les mkres Ctaient incapables de recon- naitre leurs propres petits, bien que les cas rapportCs ici restent inexpliquCs; ni l'intervention humaine, ni la densit6 ne semb- lent avoir CtC des facteurs importants. L7expCrience maternelle peut avoir jouC un r61e en 1990, puisque 10 des 14 femelles qui ont (( adopt6 * d'autres petits Ctaient $gees de 5 ans ou moins et n'en Ctaient qu'8 leur premier ou B leur second petit.

[Traduit par la rCdaction]

Introduction Pregnant Antarctic fur seals, Arctocephalus gazella, come

ashore approximately 2 days prior to parturition, give birth, and then remain with their pups for a period of about 7 days (Doidge et al. 1986). For the remainder of the 4-month lacta- tion period, females alternate trips at sea to feed (1 = 4.3 days) with visits ashore to nurse their pups (1 = 2.1 days) (Doidge et al. 1986). Although the duration of these individual events varies between species, this pattern is typical of all otariid seals (Bonner 1984) and requires females returning ashore to locate their own pup among several thousand others. It is generally agreed that among otariids, mother-pup recog- nition is facilitated primarily by auditory and olfactory cues (Bartholomew 1959; Stirling 1970; Trillmich 198 1 ; Roux and Jouventin 1987). Mothers appear to be discriminatory, nor- mally nursing only their own pup (Bartholomew 1959; Bonner 1968; Stirling 197 1 ; Roux and Jouventin 1987), and can inflict serious injuries on nonfilial pups that try to suckle (Doidge et al. 1984). Fostering behaviour (i.e., females nursing non- filial pups) and milk stealing have commonly been observed among some phocids: Mirounga angustirostris (Reiter et al. 1981; Riedman and Le Boeuf 1982), Mirounga leonina (Carrick et al. 1962; McCann 1982), Leptonychotes weddelli (Stirling 1975; Tedman and Bryden 1979), Halichoerus grypus (Fogden 197 I), and Monachus schauinslandi (Boness 1990). However, their occurrence is uncommon among otariids , although isolated cases have been reported for a number of species (Trillmich 1981 ; review in Bowen 1991).

During the austral summers of 1989 and 1990, I observed

10 and 97 instances, respectively, of female Antarctic fur seals with nonfilial pups at Bird Island, South Georgia (540001S, 38O02'W). Observations were made from mid-December through mid-April in both years from a catwalk of steel scaffolding over a 440-m2 beach (Doidge et al. 1984) where 822 and 545 pups were born in 1989 and 1990, respectively. Several hundred females that pup on the study beach were individually known by means of uniquely numbered coloured tags applied to their foreflippers in previous years. On the day of their birth, all pups born to these tagged females were retrieved with the aid of a noosing pole, marked with a serial number by bleaching the fur on their back with peroxide hair dye (Clairol Born BlondeB, Bristol-Myers Company Limited, Swakeleys House, Milton Road, Ickenham, Uxbridge, U.K.), and returned to their mother. A pup was defined as suckling when it nuzzled the fur of a female in the region of her nipples while she lay on her side. Such behaviour is typical of female Antarctic fur seals nursing pups (Bonner 1968). Nonfilial pups were recorded as either suclding or stealing milk. They were scored as suckling when the female was seemingly aware of the pup's presence because she infrequently turned her head towards it yet made no attempt to drive it away. In contrast, they were classified as stealing milk when the female appeared to be unaware of the pup, either because she was sleeping or because, when she turned towards the pup, it was immediately driven away. Only those observations where at least one of the participants was identifiable were recorded.

In 1989 I observed eight and two instances of fostering behaviour and milk stealing, respectively. Two females were

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838 CAN. J. ZOOL. VOL. 70, 1992

seen nursing nonfilial pups on four occasions each; both had previously lost their own pups through starvation (postmortem examination of the pups revealed that subcutaneous fat was absent and there was no food in the gastrointestinal tract). Upon my arrival at the beach, these nonfilial pups were already suckling, although it was not known whether either female was still lactating. These nonfilial pups all appeared smaller and thinner than other pups on the beach, though no measurements were made.

One pup was seen stealing milk twice from the same female. In the first case, the female appeared to be sleeping while both her own pup and the nonfilial pup sucked from anterior and posterior nipples, respectively. The nonfilial pup terminated sucking after approximately 5 min. In the second case, the female and her pup slept while the nonfilial pup sucked from the posterior nipples. After approximately 2 min, the nonfilial pup was driven off when the female awoke. Unlike the other nonfilial pups, this pup looked fat.

The fate of these nonfilial pups is unknown; none was sub- sequently found dead, but the pup that stole milk was seen regularly through mid-January . Their mothers were not iden- tifiable and, as a consequence, I was uncertain whether any regularly fed their pup.

In 1990, 71 of 97 observations were recorded as milk steal- ing, the remainder as cases of females nursing nonfilial pups. Twenty-nine marked pups were involved in all but three of the instances of milk stealing and, despite all being regularly fed by their mothers, 14 (48 %) subsequently died. Fourteen tagged females nursed 26 nonfilial pups; only 2 (14%) successfully weaned their own pup. Tagged females were observed feeding pups on 382 occasions, 29 (7.6%) of which involved non- filial pups.

It is not known whether any nonfilial pup was nursed by a relative in either 1989 or 1990.

The technique used by nonfilial pups to approach females is worth noting, as it was similar in all observed instances. A pup would move around the beach, presumably in search of poten- tial females to steal milk from. To make an attempt, the pup lay down, tucked in its foreflippers, and pushed itself along using only its hind flippers. The approach was always made from the female's posterior and always from an estimated dis- tance of less than 1 m. Whereas most filial pups would tuck in their foreflippers while suckling, all nonfilial pups, regard- less of whether they were stealing or suckling, kept their fore- flippers at right angles to their bodies, presumably to facilitate a rapid retreat.

Accounts of maternal behaviour among otariids suggest that fostering behaviour and milk stealing are very uncommon and isolated occurrences (reviews in Stirling 1975; Bowen 1991). The instances reported here indicate that this is not so for Antarctic fur seals. The increase in fostering behaviour and milk stealing between 1989 and 1990 was not an artifact of changes in sample design or an increase in effort, as both were similar in the two years. In discussing possible explanations it is important to make the distinction between pups stealing milk and females nursing nonfilial pups.

The increase in milk stealing might be due to an increase in pup abandonment. However, as 68 of 71 cases involved 29 known individuals and these pups were all regularly fed by their mothers, this explanation was dismissed.

Nutritional stress is the most probable cause of the increase in observations of milk stealing between years. Females nor- mally spend 4 -5 days feeding at sea between visits ashore to

nurse pups (Doidge et al. 1986; Boyd et al. 1991). This was true in 1989 (x = 4.4 f 0.1 days, n = 1156), but in 1990 these trips were longer (x = 7.9 f 0.2 days, n = 522). The consequences of long foraging trips in 1990 included (i) high pup mortality: 60% (57194) of pups born to tagged females died, 79% (31139) of these mortalities (where cause of death was determined) being due to starvation; and (ii) reduced pup growth (males: 74 g/day in 1989, 60 g/day in 1990, 41 ,3641 = 9.88, P < 0.01; females: 67 g/day in 1989, 61 g/day in 1990, F~1,6101 = 2.85, P < 0. I). It is clear that females had a diffi- cult time acquiring sufficient resources to feed pups; at Bird Island, it has been shown that seabirds and fur seals feeding extensively on krill (Euphausia superba) all periodically expe- rience a season of particularly poor reproductive performance (Croxall et al. 1988). It does not seem unreasonable to expect that more pups would be nutritionally stressed in such years. Despite the potential for serious injury resulting from bites by females, it would seem advantageous for nutritionally stressed pups to attempt to steal milk, compared with the alternative, starvation.

Fostering of pups implies that mothers made mistakes in recognition. Human disturbance has been considered a major cause of such behaviour (Fogden 197 1 ; Stirling 1975). I dis- counted this possibility because (i) my activities each year were similar, yet there was more than a threefold difference in the numbers of these observations; (ii) nonfilial pups were already suckling, in a number of instances,, upon my arrival; and (iii) I was stationary, quiet, and unobtrusive during my observations. In addition, Antarctic fur seals give birth in dense colonies, where natural disruptive events such as terri- torial disputes between males, movement of females in and out of the colony, and interactions between pups are frequent. They must, therefore, already be adapted to some degree of disturbance.

The density of animals in breeding colonies has also been suggested as an important cause of fostering behaviour (e.g., H. grypus, Fogden 1971; M. angustirostris, Riedman and Le Boeuf 1982). However, despite an approximate 35 % decrease in pup density on the study beach from 1989 ( 1.9 pups/m2) to 1990 (1.2 pups/m2), the observed incidence of females nursing nonfilial pups increased by over 300%. This contradicts the hypothesis of density dependence, which predicts an increase in such observations in years when pup density is higher, but agrees with Boness (1990), who con- cluded that density was not necessarily a primary cause of fostering in all pinnipeds in which this behaviour has been observed.

Maternal experience may have influenced fostering, as 10 of 14 tagged females observed nursing nonfilial pups in 1990 were young (5 years of age or less) and had given birth to either their first or second pup. Perhaps under conditions in which there is a high incidence of pups stealing milk, less experienced mothers have more difficulty recognizing their pups than experienced mothers.

Fostering behaviour and milk stealing does occur among Antarctic fur seals and may be more prevalent when pups are nutritionally stressed. These observations are of interest not only because such behaviour is reportedly rare in otariids, but also, and perhaps more importantly, because of the implica- tions with regard to maternal investment and reproductive success. Do these pups get sufficient milk to increase their probability of survival? If so, their mothers may realize an increase in reproductive success without necessarily increas-

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