TABLE The pupping. sites

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1 MOTHER-YOUNG INTERACTIONS IN THE COMMON SEAL, PHOCA VITULINA VITULINA by SUSAN WILSON 1) 2) (Department of Zoology, Glasgow University Scotland, U.K.) (With 1 Figure) (Rec. 3-XI-1972) INTRODIJCTION For no species of seal (Phocidae) have the interactions between mother and pup been studied to ascertain the range of behaviour and its change over the lactation period. The grey seal, Halichoerus grypus, has been studied the most, starting with several general descriptions of the mother and pup (DARLING, 1939; DAVIES, 1949; LOCKLEY, 1954, 1966; MATTHEWS, 1950, 1952; CAMERON, 1967, 1969). In particular, DAVIES reported that there was no apparent decline in the frequency of nursing bouts as the 3-week lactation period progressed. More recently, the tendency of grey seal mothers to nurse pups other than their own in crowded or disturbed conditions has been studied by SMITH (1966, 1968) and FO(;DEN 1971). In her most recent and detailed report, FOGDEN (1971) concludes that there is no evidence for pup recognition of its own mother, that pups usually initiate suckling by first calling to the mother and then nuzzling her nipple area when she approaches, and that mothers can distinguish their own pups by their scent and call. She 1) I would like to thank Professor A. A. BARNETT for his support and advice throughout this study. The final part of my work was made possible through the guidance of the late Dr YVETTE SPENCER-BOOTH, to whom I am indebted. I am grateful also to Professor R. A. HINDE for valuable discussion, to Dr H. H. ROBINSON and Dr D. G. KLEIMAN for criticising the manuscript, and to Dr B. A. BROWN for his helpful discussion on the analysis. Grateful acknowledgement is due to Queens University Zoology Department and Mr A. IRVINE for facilities at Strangford Lough. I would also like to thank formally the Mouat and Leslie families of Noss, Shetland, for their hospitality. I would also like to thank Professor D. R. NEWTH for his support and for facilities in the Department of Zoology, Glasgow University between 1967,-68. Some of this paper formed part of a thesis submitted in 1969 for an M. Sc. degree at Glasgow University, and that part of the study was financed by a grant from the Glasgow University Faculty of Science. 2) Present address : Scientific Research Division, National Zool. Park, Smithonian Institution, Washington D.C , U.S.A.

2 24 suggests that, since the lactation period during which the pup must treble its birth weight in order to survive is so brief, the most must be made of this limited time by nursing at the maximum rate until weaning with no increase in nursing intervals. Although this may well be the case, changes must nevertheless occur in the relationship which result ultimately in weaning. Such behavioural changes are difficult to detect in the grey seal, since most mothers and pups are together only on the beach, where they are rather inactive when not nursing. Occasionally a grey seal pup is reared partly or mostly in the water (pers. obs., ) where more activity occurs, such as exploration, approaching and leaving mother, contact with mother and play. Some of this behaviour may change as the pup develops; however, such animals are too rare to be studied satisfactorily. The closely related common seal, Phoca vitulina vitulina, is more suitable for such a study, since the young are reared in the water as a rule rather than as an exception, and several kinds of behaviour of the mother and pup may be observed. Since the length of the common seal lactation period is about the same as the grey seal, one would expect suckling intervals likewise to show no obvious change as weaning approaches. General characteristics of the mother-pup behaviour of the common seal in Shetland were reported by VENABLES & VENABLES (1955). The only other study is by FINCH ( ig66), who observed a captive mother and pup. In view of the widespread intensive hunting of nursing common seal pups in Europe, and consequent problems of management and conservation (U.F.A.W., y68; TnCKELL, 1970), a study of the mother-pup relationship is of practical as well as theoretical interest. This study was a preliminary attempt to describe common seal mother- young interactions and measure any changes as the lactation period progressed. The observation sites, the seals observed at each, and the relevant dates are given in Table i. Grid references are not included, but are available from the author. Length of the mother-pup relationship. The maximum number of mothers with pups observed at the Strangford Lough pupping site was 12 in 1968 and i5 in The pups were born between 20 and 30 June in 1968 and between 25 June and 4 July in In both years the number of pups secn accompanied by their mothers declined after io July. In 1970 some pups (maximum 5 on 16/7) were always observed without their mothers for the entire observation period from 14 July onwards, although the number of pups with mothers always exceeded

3 25 those without. When observations finished in both years (Table i), only three mothers were still attending their pups at the observation site. TABLE The pupping I sites These counts suggest that the mother-pup relationship at Strangford Lough lasts about three weeks. This is less than the 4-6 week suckling period suggested for other populations in Britain and on the Dutch coast (VENABLES VENABLES, SERGEANT, 1951; HAV'INGA, 1933). MOTHER-PUP CHARACTERISTIC BEHAVIOUR METHODS Notes were taken on paper until T1K8. At Strangford in IQÓ8. a continuous commentary on the behaviour was tape-recorded and subsequently transcribed. Most observations were of the activity occurring after high water until the haul-out. In order to obtain a description which was representative of all the pairs in each day, the pair observed was changed frequently; it was not possible to identify individuals or pup ages by sight. From this general commentary it was possible to distinguish between the behaviour characteristics of all the mother and pup pairs and rare or individually variable behaviour, such as feeding or avoiding alien pups, searching for lost pups, hostility or tolerance towards nearby mothers with pups, and isolated incidents of a mother teaching her pup. The following description is concerned only with regularly occurring behaviour which could be traced throughout the suckling period. Individual differences in maternal behaviour are important, but not yet substantiated. In order to obtain a preliminary picture of the change in the relationship as the

4 26 lactation period progresses, the beliaviour characteristic of all the pairs was categorized, as shown in Table 2. The tape-recorded commentary was transposed into figures by scoring a unit each time an activity changed, or the pair disappeared under water. The figures so obtained were then totalled for each week of observation. Since the 12 pups were born over the first 1-2 weeks, the figures for weeks 1-3 include all the behaviour of the pups in their first week, weeks 2-4 pups in their 2nd week, and weeks 3-5 pups their 3rd week. In order to compare the weeks, a standard for observation time was necessary, since observation time was not equivalent to time spent at the observation site. Therefore, the number of units of 'close together' (mother and pup together at the surface) was taken as a rough guide to the effective observation time in each week, since this behaviour seemed to occur consistently throughout the five weeks. TABLE 2 TVeekly totals of behœviour rccorded for 12 lilother-pup pairs in Strangford Lough, 1968 The behaviour underlined seems to show a change in frequency of occurrence over the weeks. 'Close together' is taken as all indicator of the number of ohscrvations. OBSERVATIONS (This description refers to the Strangford Lough herd except when specified otherwise.) Pups followed their mothers in the water. Each mother swam slowly, thus guiding her pup. She continually swam back to it, or turned around to it. This is illustrated by the following extract from field notes: M surfaces, swimming in. She looks back. P surfaces. M swims away from seaweed, and P surfaces several metres behind her, M immediately turns round and goes over to P... M surfaces, swimming out. P surfaces several metres behind her. M inunediately swims back, makes muzzle contact with P and dives, followed by P... M swims in, P just behind her. P submerges, M surfaces, splash from P a few metres behind. M swims on. More splashing from P. M looks round and swims on. M stretches back and submerges...

5 27 Pups rarely failed to follow the mother when she moved away. However, the mother encouraged the pup to follow her by making muzzle contact with it, or by splashing. At Fitful Head, splashing took the form of a definite 'beckon' with the flipper. Before diving in front of the pup, the mother would raise herself slightly out of the water with her back to her pup, and smack her flipper on the surface sending the spray towards the pup. On each of six occasions when the pups did not follow such a beckon, the mother returned to the pup and repeated the signal until either the pup followed, or the mother took it away in her flippers. At Fiunary Island the splashing took this form on only a single occasion when the mother had just previously discouraged the pup from following her by using another unusual variant of the flipper splash. Her next signal, the 'beckon', provided a marked contrast. Mothers at Fiunary Island also attracted the pup's attention by jerking the head, raising a flipper, or by a soft snort. Pups occasionally attracted the mother either with a short, sharp call or a soft, low noise, inaudible to any but a very closely placed observer. At Fiunary Island, 16 of 18 times before pups mounted their mothers' back, the mother first either made muzzle contact with the pup or touched it with her flipper, and then she lay horizontal at the surface while the pup mounted. This behaviour was seen once at Fitful Head, but riding was not seen at all at Strangford. Sometimes the pup slept at the surface. The mother either rested close beside it, or left it while she dived by herself for periods of up to several minutes. Mothers at Fitful Head left their pups in this way more often than Strangford mothers. When the mother eventually wanted the pup to follow her, she used a variety of methods to waken it, such as splashing vigorously round it, circling it and making muzzle contact, and climbing on top of it. When the pup took initiative in swimming and diving away from its mother, the mother usually lay horizontally at the surface with her head under water, following its movements closely. The leading behaviour by the mother eventually resulted in the mother taking the initiative in hauling out, nursing following immediately. When the pup took the initiative in hauling out, the mother never followed, but remained in the water beneath the pup, and then the pup returned to her. Thus mothers always controlled the onset of suckling, although it was almost always the pup who terminated a suckling bout (Table 3). There were seldom any preliminaries to suckling other than occasional muzzle contact or stroking with the foreflipper by the mother. It was very rare for a mother to refuse her pup when it tried to suckle. ny contrast with the Strangford

6 28 seals, the Fitful seals nursed in the water (cf. VENABLES & VENABLES, 1955). Here suckling was usually preceded by muzzle contact, followed by the pup climbing on the mother's back, tumbling off again, and starting to suckle with its head under water. TABLE 3 Nursing behaviour: Strangford, 197. Start of suckling seen 44 times Play between mother and pup occurred frequcntly in bouts of a few seconds, and less often was prolonged. Sometimes the pup frolicked round the mother while she watched without participating. This frolicking consisted largely of splashing, porpoising, streaking under the surface, and diving on top of the mother. The pup often approached the mother, and she always followed the pup closely. When the mother played with the pup, they often turned over each other, heads to tails, leaping backwards out of the water as they did so. At other times their muzzles touched, and they splashed continuously while twisting round each other. All this behaviour was termed 'rolling' (see VENABLES & VENABLES, 1957; 1959, for origin of terminology). Both porpoised as well. Sometimes the mother approached the pup, and sometimes she dived on top of it. It was clear that mothers encouraged their pups to play. All the play activities were qualitatively similar to juvenile play (?W Lsorr, 1973). Table 2 indicates those activities which seemed to change as the suckling period progressed. Effective observation time was small in week i, since few pups had been born. There were more observations in weeks 3 and 5 (which were roughly comparable) than in weeks 2 and 4 (which were also roughly comparable). While close contact between mother and pup did not seem to change, there was a progressive increase in time spent at a distance from each other, and consequently an increase in the frequency of approaching one another. There was a slight progressive decrease in the mother leading the pup ('pup follows mother'). An increase in the pup sleeping at the surface and in giving the 'distress' call was seen as the pups entered their third week. These changes in the relationship as the suckling period progresses are discussed further in the next section.

7 29 PROGRESSIVE CHANGES IN THE MOTHER-PUP RELATIONSHIP METHOD The progressive changes in the relationship were measured at Strangford in ig7o by a method similar to that of HINDE & ATKINSON (Io70) and HINDE & SPENCER-BO?OTH (I97l). Their method, developed for studying interactions between captive rhesus monkeys and their infants as the lactation period progresses, analysed both the time spent in close contact and at a distance, and which animal was responsible for making and breaking contact. This approach allows the changing relationship which gradually results in behavioural independence and weaning of the young to be better understood. Since preliminary observations of common seals (described in the previous section) and grey seals (described by the authors cited in the Introduction) suggest a lack of continuity between maternal behaviour before and at the time of weaning, a modification suitable for seals of the method used by HINDE and his colleagues was adopted through the advice and guidance of the late YVETTE SPENCER-BoOTH. A check sheet was designed to record the number of half-minutes in which behaviour items occurred during a ten-minute observation period, The seals were observed during the two hours following high water. A pair was selected for observation if the mother and pup were close by in the water, and not attempting to haul out, at the start of each observation period. Although it was impossible to select the pairs either at random or in turn, each daily record represented as many pairs as possible. The ten-minute periods were often curtailed by bad visibility or by the pair disappearing, but the period was included if it was more than half complete. The intervals between observation periods were often prolonged either by rain or by the absence of seals in the water. The activities recorded are shown in Fig. I. The seals spent an increasing amount of time hauled out as the tide ebbed, and consequently the amount of each aquatic activity in successive ten-minute periods of each day decreased accordingly. Therefore, haul-out time had to be discarded from each ten-minute period to obtain behaviour indices meaningful for a day-byday comparison. However, with haul-out time discarded, the effective length of the original ten-minute periods was often too short to be useful. Therefore, the scores for each behaviour item were calculated collectively as the % half-minutes per time spent in the water for all the half-minute records for one day. Approach and leave were scored for both the mother and pup each time either crossed an imaginary 'near' boundary (about one adult body length from the animal not moving) or 'far' boundary (about six adult body lengths from the 'near' boundary). In order to assess progressive changes in this behaviour, each category of approachings and leavings was totalled over each of five 6-day periods. The frequency of leaving was too small for these measures to be considered separately for each pair. Time spent in the water. Before hauling out time could be discarded from the behaviour records, it was necessary to make sure that time spent in the water was not itself a factor inherent in the mother-pup relationship, possibly undergoing progressive change. Physical factors affecting time spent in the water before hauling out on the ebb include (i) the depth of water available surrounding the hauling out rocks (which varies a lot at Strangford with spring and neap tides) and the time after high water; (ii) the weather, and (iii) the time of day. Plotting the percentage of mother-pup pairs hauled out each day at three different times and three different water levels during the observation period indicated that of these factors only the time of high water was im-

8 30 portant period indicated that of these factors only the time of high water was important to a day-by-day comparison of haul-out numbers of months with pups. The percentage of pairs which hauled out early in the observation period was high when high water occurred between early morning and late afternoon, but dropped dramatically when high water occurred in the early evening. Therefore, there is possibly a combination of tidal and diurnal rhythms. Since no other daily trend in haul-out time was observc<l, discarding haul-out timl? form the behaviour records was deemed justifiable. RESULTS Fig. I indicates a slight decrease in the time spent by the mother in leading the pup (c). This might reflect an increasing reluctance to haul out and nurse. Time spent playing together did not change, but pup frolicking round the mother was not observed until the eldest pups were about io days old (g). Time spent slightly apart ('near': between about 1-7 adult body lengths from each other) did not change (b). Pup sleeping at the surface was not observed until the eldest pups were in their third week (e). These results confirm the same behaviour changes implied in Table 2. Time spent close together, which was assumed to be unchanging in Table 2, actually increased slightly according to Fig. Ia. There is an apparent discrepancy between the two sets of observations concerning time spent at a distance ('far': more than about 7 body lengths from each other, and apparently behaving independently of one another). According to Table 2 this clearly increased, but Fig. mi indicates no obvious change. However, Fig. I describes the behaviour of selected pairs who were close by at the start of a io-minute observation period. The 1968 observations were not biased thus, and hence, the indicated progressive increase in time spent at a distance is probably real. Responsibility for breaking and re-establishing contact (Tables 4 and 5). Throughout the lactation period the mother was usually responsible for re-establishing contact. Table 5 expresses this by showing the percentage of approaches due to the mother minus the percentage of leavings due to the mother across both the 'near' and 'far' boundaries during each of five 6-day observation periods in This figure was always positive. However, during the first part of the lactation period, it was usually the pup who broke contact with the mother, crossing either the 'near' or the 'far' boundary. In its third week (the last two of the 6-day periods), it was still the pup who crossed the 'near' boundary most often, but it was the mother who was most often breaking contact completely (Table 4).

9 The mother succeeded in severing contact with her pup on these occasions by swimming too fast for it to keep up. Her departure in this manner sometimes terminated a vigorous play bout, the mother porpoising rapidly away in an apparently playful manner. Some, though not all, mothers were 31 Fig. i. Number of half minutes in which various activities occurred (expressed as a percentage of time spent in the water) : - (a) close together; (b) at a distance (apart: 'near') ; (c) mother leads pup; (d) at a distance (apart: `far') ; (e) pup asleep at surface; (f) pup leads mother; (g) play together: 0 pup frolics: o. - The vertical broken line at July 4 marks the date after which no pups were born.

10 32 seen later in the same observation period to return to their pups, again porpoising at the reunion. TABLE 4 Approaching and leavings during each of five 6-day observation periods As the mother vanished, the pup sometimes gave the 'distress' call, which was always ignored. Calling may have been more likely when play did not precede the mother's departure, but this has yet to be confirmed. The small total number of times this behaviour was seen suggests that weaning is rather sudden. TABLE 5 % Approaches minus 7o Leavings due to niother during each of five 6- day observation periods

11 33 Separation and reunion. DISCUSSION EVANS & BASTIAN ( I96g) state that when mother and pup common seals are separated the pup gives a distinctive call. The mother approaches the calling pup, they rub muzzles, and then the pup follows the mother. In Strangford Lough the only lone pups which called were those which had just been left by the mother, who paid no attention to the calling. This may be because mother and pup were rarely separated by accident in the sheltered lough waters. A. FRASER (personal communication) described a sequence observed in East Anglia, in which a pup was experimentally removed from its mother and placed a short distance away round the corner of a creek. The subsequent behaviour corresponded to EVANS and BASTIAN's description except that the pup did not call. The importance of muzzle contact as a greeting ceremony for all Pinnipedia has been commented on by PETERSON & BARTHOLOMEW (I969) and EVANS & BASTIAN (I969). The latter authors also stress the importance of flipper touching and rubbing and body rubbing. Responsibilty for changes in the relationship. FINCH ( I966) studied a captive mother and pup of the common seal for six weeks in an enclosed pen containing a pool and gravel area. She concluded that, since the pup spent more and more time swimming independently from its mother, changes in the pup's behaviour were responsible for changes in the relationschip. However, this interpretation would be wrongly applied to the behaviour of the Strangford seals. HINDE & SPENCER-BOOTH (I97I) emphasise that `... the more fundamental aspects of the relationship may not be those that are the more immediately obvious.' For example, the time the infant monkey spends off its mother and at a distance from her depends on the frequency with which both mother and infant make and break contact. This seems to be true also for common seals. My observations showed that throughout the relationship the mother was usually responsible for re-establishing contact. Also, she always controlled the time of haul-out and hence the subsequent nursing. This suggests she was always in complete command of the pair's combined behaviour, and that her interest in the pup was not subject to a gradual waning. Indeed, the amount of time spent close together actually increased. Furthermore, the mother spent progressively less time in guiding the pup, and the mother began to break contact in the third week. The only obvious changes in the pup's behaviour, which are the onset of frolicking round the

12 34 mother and sleeping at the surface, might, however, contribute indirectly to the changing relationship by somehow affecting the mother. The mother never avoided or punished her pup's approach. This is in contrast not only to monkeys but to many other mammals. HINDE, and SPENCER-BooTH found that rejection by the mother is more important than her initiative in making contact in determining the time the pup spends away from her. Ascertaining whether the absolute reverse of this is true of seals (which my observations suggest) or whether there are more subtle factors functionally equivalent to 'rejection' will require observations on identifiable individuals in their natural habitat. This study has underlined the importance of space and the tidal rhythm for understanding normal mother-pup interactions: observations on captive seals would probably be misleading. It seems paradoxical that the pair were sometimes playing vigorously just before the mother took her leave of her pup, and that the porpoising manner in which the mother left and returned suggested a playfulness on the part of the mother. Possibly this play between mother and pup, which is initiated by the mother, reduces the stress on the pup caused by its mother's disappearance. The question arises whether this unusual relationship between mother and young is (i) peculiar to the Strangford Lough population, (ii) characteristic of Phoca vitulina only, or (iii) behaviour common to all the Phocidae. The parameters of overt behaviour certainly vary from common seal population to population (cf. VENABLES & VENABLES, 1955), and sub-species to subspecies, and even more so from species to species. The great and obvious differences between common and grey seal maternal care is a case in point. Such differences, however, may only conceal underlying similarities in the nature of the mother-young relationship. SUMMARY The mother-young relationship of the common seal Phoca vitulina in Strangford Lough, N.E. Ireland, lasted about three weeks. Mothers with young were most active during the first two hours of the ebb, and also they spent more time in the water when the ebb occurred towards evening than in the morning. Characteristic behaviour in the water included (i) the mother guiding the pup and maintaining close contact with it (ii) playing, and (iii) the pup sleeping at the surface with the mother close by. Progressive changes in the relationship included a slight decrease in time spent by the mother in guiding the pup, a slight increase in time spent close together, an increase in time spent at a considerable distance apart, and an increase in time spent by the pup sleeping at the surface. Throughout the suckling period the mother controlled the onset of suckling, but rarely terminated it. Throughout, also, the pup broke contact the most, while the mother re-established contact the most. Just before weaning, mothers left their pups for long periods, the separation sometimes terminating a play bout.

13 REFERENCES CAMERON, A. W. (1967). Breeding behaviour in a colony of western Atlantic gray seals. Can. J. Zool. 45, p (1969). The behaviour of adult gray seals (Halichoerus grypus) in the early stages of the breeding season. --- Can. J. Zool. 47, p DARLING, F. F. (1939). A naturalist on Rona. - Oxford: Clarendon Press. - (1947). Natural history of the Highlands and Islands. - London: Collins. DAVIES, J. L. (1949). Observations on the grey seal Halichooerus grypus at Ramsey Island, Pembs. - Proc. Zool. Soc. Lond. 119, 3, p EVANS, W. E. & BASTIAN, J. (1969). Marine mammals communication: social and ecological factors. - The Biology of Marine Mammals, ed. H. T. ANDERSEN. New York and London: Academic Press. FINCH, V. A. (1966). Maternal behavior in thc harbor seal. - Proc. 3rd Ann. Conf. on Biol. Sonar and Diving Mammals. FOGDEN, S. L. C. (1968). Suckling behaviour in the grey seal Halichoerus grypus and the northern elephant seal Mirounga angustirostris. - J. Zool. Lond. 154, p (1971). Mother-young behaviour at grey seal breeding beaches. J. Zool. Lond. 164, p HAVINGA, B. (1933). Der Sechund (Phoca vitulina) in den Holländischen Gewässern. - Tijdschr. Ned. Dierkundige Ver. (Leiden) 3, p HINDE, R. A. & ATKINSON, S. (1970). Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys. - Anim. Behav. 18, p & SPENCER-BOOTH, Y. (1971). Towards understanding individual differences in rhesus mother-infant interactions. - Anim. Behav. 19, p LOCKLEY, R. M. (1954). The seals and the Curragh. - London: J. M. Dent & Sons. (1966). Grey seal, common seal. - London : André Deutsch Limited. MATTHEWS, L. H. (1950). The natural history of the grey seal, including lactation. - Proc. Zool. Soc. Lond p (1952). British Mammals. - London: Collins. PETERSON, R. S. & BARTHOLOMEW, G. A. (1969). Airborne vocal communication in the California sea lion Zalophus californianus. - Anim. Behav. 17, p SERGEANT. D. E. (1951). The status of the common seal Phoca vitulina on the East Anglian coast. - J. Marine Biol. Assoc. U. K. 29, p SMITH, E. A. (1966). Mother-young relations in the grey seal. - Mamm. Soc. Bull. 26, p (1968). Adoptive feeding in the grey seal. - Nature 217, p TICKELL, W. L. N. (1970). The exploitation and status of the common seal Phoca vitulina in Shetland. - Biol. Conserv. 2, p U.F.A.W. (1968). Sealing in U.K. and Canadian waters. - London: U.F.A.W. VENABLES, U. M. & VENABLES, L. S. V. (1955). Observations on a breeding colony of the seal Phoca vitulina in Shetland. - Proc. Zool. Soc. Lond p WILSON, S. C. (1973). Juvenile play of the common seal Phoca vitulina vitulina, with comparative notes on the grey seal Halichoerus grypus. - Behaviour 48, p RÉSUMÉ Le rapport entre la mère du phoque Phoca vitulina et son enfant à Strangford Lough, N.E. Irlande, durait vers trois semaines. Les mères avec leur enfant étaient le plus actives pendant les deux heures premières de la baisse. D'ailleurs, elles passaient plus de temps dans l'eau si la baisse s'est passée vers le soir que si elle s'est passée le matin. Le comportement characteristique dans l'eau embrassait (i) la mère en dirigeant son 35