mother–pup reunions in harp seals, phoca groenlandica : cues for the...
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Mother - pup reunions in harp seals, Phoca groenlandica: cues for the relocation of pups
Kit M. Kovacs
Abstract: This study was designed to examine how female harp seals (Phoca groenlandica) solve the orientation problems they face when returning to their pups from the water in a pack-ice environment. Data were collected during the breeding seasons of 1992 and 1993 in the Gulf of St. Lawrence, Canada. During 31 h of observations, 73 returns of females were documented. Most return paths of females from the water originated at the access point closest to their pup (88%), indicating good underwater orientation capabilities. The mean path length was 1.3 f 2.2 times the length of a direct line between the water access point and the pup, and most females were clearly oriented toward their pup upon leaving the water. Most return paths (84%) terminated in a nursing session with the pup. Prior to nursing, naso-naso contact was made by the mother -pup pair. Only 26% of return paths were directed toward a calling pup, the rest were spontaneously performed to a silent, unmoving pup. The mean duration of calling prior to the appearance of the female was 7.3 f 7.2 min (N = 18). Mothers returning to a vocalizing pup did not have more direct return paths than those returning to a silent pup (Mann-Whitney U test, U = 422, P = 0.19). Although pups were remarkably sedentary in the absence of their mothers, approximately half of females returning to their pup (32173) were approached by it. Only 7% of paths (5173) of females involved contact with a foreign pup. Likewise, pups rarely approached females other than their mother. Females were able to return directly to sleeping, silent (or dead) pups that were not visible from the origin of the path and were able to return to locations where they had last left the pup without the pup itself acting as a stimulus. Thus, it appears that harp seal mothers use multimodal sensory cues to return to their pups in the pack-ice environment. At long distances spatial information appears to be of primary importance and can be used exclusively by females to return to specific positions on the ice. Visual and auditory cues emitted by pups may ease the task of relocation, although they must be considered of secondary importance. Pups appear to recognise their mothers at a distance. At close range, olfactory cues provide the definitive means of individual identification within mother -pup pairs.
RCsumC : Cette Ctude a CtC entreprise pour tenter de dCterminer comment les femelles du Phoque du Groenland (Phoca groenlandica) rCussissent A s'orienter dans L'eau lorsqu'elles cherchent h retrouver leurs petits au milieu des glaces fixes. Les donnCes ont CtC recueillies au cours des saisons de reproduction de 1992 et 1993 dans le Golfe du Saint-Laurent, Canada. Au cours de 31 h de surveillance, 73 cas de retrouvailles mkre-petit ont CtC observCs. La plupart des trajets suivis par les femelles partaient du point d'accks le plus proche du petit (88%), ce qui reflkte une haute capacitC d'orientation sous l'eau. La longueur moyenne du trajet suivi par les femelles Ctait de 1,3 f 2,2 fois la longueur de la ligne directe entre le point d'accks h l'eau et le petit, et la plupart des femelles Ctaient dCjA clairement orientCes en direction de leur petit au moment de quitter l'eau. La plupart des trajets observCs (84%) se terminaient par une session d'allaitement. Avant l'attaitement, il y avait contact museau-museau entre la mkre et son petit. Dans seulement 26% des cas les femelles se dirigeaient vers un petit qui criait; les autres trajets ont CtC entrepris spontankment, vers des petits silencieux et immobiles. La durCe moyenne des appels avant l'apparition des femelles a CtC CvaluCe h 7,3 f 7,2 min (N = 18). Les femelles qui se dirigeaient vers un petit qui criait n'empruntaient pas une route plus directe que les mkres qui cherchaient h retrouver un petit silencieux (test de Mann-Whitney, U = 422, P = 0,19). La plupart des petits Ctaient remarquablement sCdentaires en l'absence de leur mkre, mais environ la moitiC des femelles (32173) ont vu leur petit venir h leur rencontre au cours de leur trajet. Dans seulement 7% des cas (5/73), les femelles ont rencontrk un petit Ctranger au cours de leur trajet. De la meme f a~on , les petits cherchaient rarement h s'approcher de femelles autres que leur mkre. Les femelles se sont avCrCes capables de retourner directement h leur petit endormi, silencieux (ou mort),
I Received June 22, 1994. Accepted February 10, 1995.
K.M. Kovacs. Department of Biology, University of Waterloo, ON N2L 3G1, Canada.
Can. J . Zool. 73: 843-849 (1995). Printed in Canada 1 ImprimC au Canada
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mkme quand celui-ci n'Ctait pas visible du point d'origine du trajet hors de l'eau et elles pouvaient retrouver le lieu ou elles avaient laissC leur petit sans que celui-ci ne serve de stimulus. I1 semble donc que les femelles nourricikres du Phoque du Groenland utilisent des signaux sensoriels multimodaux pour retrouver leur petit au milieu des glaces fixes. Sur de longues distances, les signaux spatiaux semblent &re d'importance capitale et peuvent &re utilisks exclusivement par les femelles qui cherchent B retrouver des points spkcifiques sur la glace. Les signaux visuels et auditifs Cmis par les petits rendent la tiche plus facile, mais ils n'ont qu'une importance secondaire. Les petits semblent capables de reconnaitre leur mkre B distance. A faible distance, les signaux olfactifs constituent un moyen ultime de reconnaissance entre mkre et petit. [Traduit par la RCdaction]
Introduction
In mammalian species where females leave their young between nursing sessions, the ability to repeatedly locate the offspring again and recognise it is of vital importance to the survival of neonates. The bonds between mothers and their pups appear to be established during the first few hours following birth in most pinniped species (e . g . , Fogden 197 1 ; Le Boeuf et al. 1972; Trillmich 1981 ; Kovacs 1987; Lawson and Renouf 1987; Stewart 1987). Subsequent identification, in those species that recognise their young, is usually attributed to olfaction at close range and to a combination of visual, acoustic, and perhaps spatial cues at greater ranges (for a review see Bowen 1991). Specific testing of factors involved in long-distance relocation have been conducted on relatively few species of pinnipeds and most of this work has concentrated on otariid species (e.g., Arctocephalus galapago- ensis, Trillmich 198 1 ; A. tropicalis, Roux and Jouventin 1987; Zalophus californianus, Hanggi and Schusterman 1990; Gisiner and Schusterman 1991). These studies have demonstrated that acoustic signalling is the primary mechan- ism for successful reunion of mother-pup pairs, both the female and the pup being active participants, each able to identify the call of the other. This mutual vocal recognition has obvious selective value for all otariids. Throughout lacta- tion, which lasts from 4 months to several years depending on the species and prevailing environmental conditions, fur seals and sea lions alternate nursing sessions with several days of foraging at sea (e.g., Bonner 1984; Gentry and Kooyman 1986; Oftedal et al. 1987). During their mother's absences, pups of most species do not remain sedentary; they group into mobile pods (e.g., Trillmich 1981), which may prevent the use of spatial cues for relocation. However, pups of at least three otariid species do show a distinct preference for a relatively small area, which may facilitate the use of spatial cues by females when they begin the searching process (A. australis and Callorhinus ursinus, see Riedman 1990; Neophoca cinerea, Higgins and Gass 1993).
The lactation strategy of phocids, and for many species their breeding habitat also, is quite different from that of otariids (see Stirling 1983; Kovacs and Lavigne 1986, 1992a; Oftedal et al. 1987). Phocid seals are characterized by short lactation periods that last from 4 days to a maximum of about 2 months. Parturition habitats include pack ice, land-fast ice, and land. Attendance patterns are highly vari- able, ranging from the female remaining with her pup through- out lactation (e.g., Mirounga angustirostris, Le Boeuf et al. 1972; Halichoerus grypus on Sable Island, Boness and James 1979) to the female routinely spending periods of several
hours in the water between nursing sessions (e.g., beach- breeding grey seals in the United Kingdom, Fogden 197 1; Phoca groenlandica, Kovacs 1987). During lactation, phocid females produce extremely rich milk (for a review see Oftedal et al. 1987), principally or solely from their body reserves, which ensures rapid transfer of energy to their off- spring (e.g . , Fedak and Anderson 1982; Kovacs et al. 199 1). Misdirection of resources through suckling of foreign pups can have serious consequences for the survival of a female's offspring. It is not surprising, therefore, that female phocids usually show strict discrimination in their choice of suckling partner, and foreign suckling is a relatively rare event (for a review see Bowen 1991).
In the northwest Atlantic, harp seals congregate in large herds during late February and early March to give birth on the pack ice. During the first 24 h, postpartum females attend their single pup continuously. For the remainder of the 10- to 14-day nursing period (Stewart and Lavigne 1980; Kovacs and Lavigne 1985), females usually return to the water between nursing sessions, which take place every few hours (Kovacs 1987; Stewart 1987). While in the water they spend 44% of their time at or near the surface and 56% actively diving (Lydersen and Kovacs 1993). To return to their pup after a bout of diving, a female harp seal must locate it in a crowded nursery patch on a breeding substrate that can change dramatically in both location and form in a relatively short period of time. Terhune et al. (1979) suggested that harp seal mothers used visual, auditory, and olfactory clues to locate and identify their pups and that pups were approached from a distance in a random manner because the instability of the ice prevented the use of spatial memory. During subsequent studies of maternal behaviour and pup development in harp seals (Kovacs 1987; Stewart 1987), most of these suggestions have been confirmed. However, the paths taken by returning females did not appear to be ran- dom. This study was designed to further examine how female harp seals solve the orientation problems they face when returning to their pups.
Methods
Data were collected from direct observations during the breeding seasons of 1992 and 1993 in the Gulf of St. Lawrence, Canada. Each year the harp seal herd was located via a helicopter survey flown out of the Magdalen Islands. An observation area was chosen that contained very young pups. A spatial grid was established for behavioural obser- vations by placing small coloured ice screws every 5 m along three axes. Two short axes (30 m in length) were constructed
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perpendicularly to a longer one (50 m in length), thus form- ing an H shape on the ice. The marks allowed the observer to mentally subdivide the observation areas into grids (25 m2) and to draw reasonably accurate area maps depict- ing the positions of points of access to water (holes or leads), the general topography of the ice (ice piling, rafting, etc.), and the position and movements of the seals. Maps were adjusted, as required, when the observation areas changed structurally. To facilitate relocation of observation areas, VHF radio-transmitter stations that could be tracked from the helicopter were set up on the ice about 50 m from the obser- vation grids.
All pups within grid areas were dye marked with unique colour patterns and tagged with numbered Jumbo Roto-tags through the webbing of a hind flipper. At the start of each year's observation period, all of the pups within each obser- vation area were less than 3 days of age (see Kovacs and Lavigne 1985). Adult females were marked with paint applied in pellet form using a C02-powered pistol if they were not easily identifiable from their coat pattern.
Observations commenced each day with a survey of the area, conducted from the edge of the grid, during which the position of each seal was plotted. The observer sat on an ele- vated ridge of rafted ice and recorded the activity taking place on or very near to the grid; for reasons of comfort, the location of the observer depended on the direction of the wind. During behavioural sampling, the movements of each animal (female or pup) were drawn on acetate overlays superimposed on a scaled schematic map that depicted the spatial grid and structural features of the observation area. A new overhead was used as necessary to avoid superimposi- tion of information. Path lengths, measured in millimetres, were directly comparable among observation areas and between years. Particular attention was paid to the time at which pups started vocalizing or moving and the time that the mother hauled out. The orientation of the female with respect to the pup was noted upon her return to the ice surface. Addi- tionally, notes were taken on any foreign contacts or unusual incidents that occurred along the return paths of females. At the end of each day's observation period the identity of all pups was confirmed. The duration of observation sessions varied between 3 and 5 h. The period was set a priori each day, and was usually from 14:OO until 17:00, which coin- cides with a peak nursing period (see Kovacs 1987).
In 1992 a grid containing 23 pups was established on 2 March. A storm that night completely destroyed the grid and the marked pups in the area dispersed broadly. Because of the instability of the region a new grid was set up in a different area approximately 15 km away on the morning of 4 March. Fifty-one pups were tagged and colour marked. Observations were conducted that afternoon and during the afternoon on the next 2 days. In total, 8 h of data were col- lected before another, more severe storm struck the Gulf region. The observation patch was relocated via a fixed-wing aircraft survey on 12 March, 30 km from its position on 6 March. Forty-nine of the 51 colour-coded pups remained on the grid, but virtually all of them had been weaned.
During 1993 a grid containing 29 pups was established on 27 February. During the night of the 28 February, ice move- ments resulted in major structural changes to the observation area, including the opening of a lead, which produced
several new haul-out holes and a ridge. Nine pups had moved out of sight, but the other 20 were still in view and the grid remained intact throughout the following 2 weeks. The patch was successfully relocated each day on which the weather permitted helicopter flights to be made. Observations were conducted until 13 March, when most of the females had weaned their pups. In total, 23 h of data were recorded during 1993. During the first few days of the 1993 season a female attended a stillborn pup. Although her behaviour was documented, her return paths are not included in the analyses.
Results
All of the females observed during this study spent time in the water and hence had to return to their young for nursing sessions. Pups in the grid areas were all located within 20 m (range 2 -20 m) of a point of access to open water, through either a lead in the ice or a hole. The structure of the ice defined arena areas consisting of flat areas of ice surrounded by rafted ice pieces that build up when ice pieces are forced together by the action of winds and currents. Access points to water were concentrated in the areas of ice breakage, where piling and ice rafting were common. In addition to proximity to maternal return sites, these rafted areas pro- vided shelter from the wind for pups. Hence, pups were also concentrated in or near these areas of rough ice.
During the 31 h of observations conducted during the 2 study years, 73 returns were documented (mean -2.4 return pathslh) for 41 females. The number of paths per female in the sample ranged from 1 to 3, so although paths are not completely independent, the autocorrelation due to repeat sampling of individual females is minimal.
Most return paths of females (87.5 % ; N = 72) originated from the water through the access point closest to their pup. Individual females used the same hole for sequential haul- outs as long as the pup remained in the same location. If their pup's resting spot changed, mothers adjusted their haulout hole to the hole nearest the new location. A single haulout hole or lead was used by several females.
Females' paths to their young were remarkably direct, with a mean path length of only 1.3 + 2.2 times the length of the direct line between the water access point and the pup (N = 72). This is remarkable, given that females had to alter their paths to avoid adult conspecifics and irregularities in the ice surface. Females showed almost no hesitation during their trips from the water to their pup. Only 14% (10173) of paths involved a turn of 90" or greater, and most females were clearly oriented toward their pup upon leaving the water (Fig. 1).
Most return paths terminated with a nursing session upon contact with the pup (84%; N = 73). Those paths that did not result in nursing involved disruption due to interactions with other animals or failure of a sleeping pup to wake upon the return of the mother. Prior to nursing, females made naso - naso contact with their offspring. Only one nursing session was observed to take place without such prior con- tact. In 62% (38161) of nursing sessions, females led the pup for some distance prior to the commencement of feed- ing. This was done by the female presenting her nipples and allowing the pup to make contact, then moving away before
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Fig. 1. Orientation of female harp seals with respect to their pup upon haulout from the water. Females that were oriented directly toward their pup immediately upon haulout were registered in the zero class. Deviations on either side of the direct line are registered in classes that represent = 30" groupings.
4 9
Haulout orientation
presenting again. Pups followed their mothers readily in such situations. Pups occasionally remained in the new location (8 % ; 5/61), but if the distance moved was only a few metres, they returned to their previous resting spot upon termination of nursing or the departure of the female.
Few females checked foreign pups prior to contacting their own. Only 5 of the 73 (7%) paths observed involved a foreign contact. In 4 of these cases the pup was the nearest neighbour to the returning female's own pup. In the fifth case, multiple contacts were made by a searching female whose complete path was not observed because she moved out of the observation area. This female's pup was on the study grid but had moved 2 m in the absence of the female. The female passed her sleeping pup and went directly to its usual location before commencing an elaborate search throughout which she emitted a quiet, warbling vocalization. After 30 min of searching inside and outside the observation area, she found her sleeping pup and nosed it, waking it up. The pair then moved to the pup's normal resting place, where the female nursed it. During 1993, the paths of two additional females involved multiple contacts with pups in the observation area. These females were unknown and their pups were not in the study area, so the outcome of their searches is unknown. These females emitted the same soft, warbling vocalization during their searches. All encounters between unrelated animals were of short duration. After naso - naso contact the animals simply parted or one or both participants in the interaction performed low-threat behav- iours (see Kovacs 1987).
Pups were remarkably sedentary during the nursing period in areas where the ice remained more or less intact. The majority of pups marked on the second grid in 1992 and those on the grid in 1993 remained within or very close to the grid until weaning (86%; 69/80). In fact, many pups remained in the exact locations where they were first mapped, leaving only in response to their mother's appearance for
feedings. Most movements of any significant distance were conducted in the presence of the mother and were actively induced by her enticing the pup to follow her to a new loca- tion as described above. The largest displacement measured during the study was a movement of 300 m from the pup's initial position until weaning. Twenty-one occurrences were documented of pups moving more than 1 m, in the absence of their mother, in a direction other than toward the hole that she used. The average displacement from commencement to termination of the movement was 4.6 + 4.3 m. The total dis- tance travelled was considerably longer in many cases (52 % ; 1 112 l ) , but pups tended to circle around their resting spot. Only two extensive movements by solitary pups were observed. Both of these pups were vocalizing and were therefore presumably hungry. Unfortunately, neither mother - pup reunion was observed, as both occurred after the end of the day's observations. Both pups were back on the grid in their usual resting spots at the commencement of the next day's observations.
Most return paths of females were spontaneous, but some pups did commence calling in the absence of their mother (26% ; 19/73). Half these pups also began moving out of their resting spot while calling (1 5 % ; 1 1/73). The time between a pup commencing vocalization and its mother returning was 7.3 + 7.2 min (range 0.1-23 min; N = 18; one case of extremely long duration (125 min) was removed as an out- lier). Mothers returning to vocalizing pups did not follow significantly more direct paths than those returning to silent pups (Mann - Whitney U test, U = 422, P = 0.19). Previ- ously silent, stationary pups often commenced vocalizing and moving toward their mother when she hauled out onto the ice. Forty-four percent of returning females were approached by their offspring (32173). During all of the observations only two instances of pups approaching a strange female were observed.
In 1993 a female gave birth to a stillborn pup in the obser- vation area. The mother remained with the corpse continu- ously during the day of its birth and the following day, often attempting to induce suckling. During the third and fourth days after delivery the female went to the water and returned to the dead pup at intervals. She was not seen thereafter. Her return paths were extremely direct even though the body was not readily visible from the hole and provided no other cues, unless they were olfactory.
Discussion
Few studies have addressed the orientation capabilities of seals. It is clear that many seal species have a good homing ability (e.g . , Boness and James 1979; Ridgway and Robison 1985). Additionally, good under-ice navigation skills have been demonstrated for Weddell seals (Leptonychotes weddel- lii; for a review see Wartzok 1991) and ringed seals (Phoca hispida ; Wartzok et al. 1992). However, the fine resolution required by some phocid seals to relocate pups in nursery areas has received little attention. Female phocids face a broad range of orientation needs with respect to maintaining the mother-pup bond. Concomitant with differences in par- turition habitat and attendance patterns, the problems faced by females in relocating pups differ among species. For spe- cies or populations in which attendance on ice or land is con- tinuous, the problem of relocation is almost nonexistent. This
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is the case for species such as the hooded seal (Cystophora cristata) in which mothers do not leave their pups prior to weaning. In this species, mothers appear to have no ability to recognise their offspring (Kovacs and Lavigne 19926) if they do become separated. In harbour seals (P. vitulina), although mothers and pups stay together throughout much of the lactation period, the pairs do not remain at a fixed loca- tion and separations do occur (Boness et al. 1992). It has been suggested that pup vocalizations (Renouf 1984; Perry and Renouf 1988) play an important role in keeping pairs together in this species and that both the pup and the mother play a role in maintaining their close proximity (Renouf et al. 1983). Godsell (1988) suggested that the observed fidelity shown by harbour seal mother-pup pairs to specific loca- tions within haulout sites may facilitate reunions of separated pairs. Among phocids on the fast-ice that use lairs for breed- ing (ringed and Baikal seals (P. caspica); McLaren 1958; Pastukhov 1969; Smith and Stirling 1975)' the fixed spatial positions of the lairs, their widely separated distribution, and the relative stability of the ice clearly allow for spatial orien- tation to relocate pups (see Wartzok et al. 1992).
For gregarious phocid species, or populations, where females return to the water at intervals during lactation, relo- cation of the pup is complex, particularly in the pack ice, which is mobile and subject to structural change. Although the density of harp seals in whelping patches is low compared with that of breeding colonies of most otariid seals and land- breeding phocids, pups do aggregate close to common access points to water and there is potential for confusion among pairs. Despite these complexities, harp seal mother-pup reunions are usually simple and the mortality rate due to star- vation during the first few weeks of life is extremely low (Kovacs et al. 1985). No starving pups were observed in the grid areas during this study.
Females also displayed good navigation skills beneath the ice, routinely returning to the hole closest to their pup, and they adjusted their choice of haulout hole when the pup had been moved. Most surfacing females were oriented toward their pup and followed a remarkably direct return path in most instances.
Pups' behaviour patterns aided their mother's relocation task in at least three ways: (1) pups are quite sedentary, (2) they frequently provide visual cues for their mother through starting to move toward her, and (3) some pups vocalize, providing acoustic cues. The sedentary nature of pups means that their spatial location is quite predictable. Some hungry pups did become mobile but tended to loop around their resting spot, hence their actual change in loca- tion was relatively small. During more than half of the returns the pups moved in the direction of their approaching mother, providing visual cues facilitating relocation. The low proportion of pups approaching foreign females suggests that harp seal pups are able to recognise their mother from a distance, as has been observed for harbour seals (Perry and Renouf 1988).
Most females' returns to the ice appeared to be spontane- ous and most encounters between mothers and pups leading to a nursing session were initiated by the female without any vocal identification cues from either member of the pair. However, approximately one-third of pups had commenced calling prior to the female's return to the ice surface, gener- ating auditory cues that may have aided in localization of the
pup. Additionally, previously silent pups occasionally com- menced vocalizing when their mother was approaching them. Individual variation among harp seal pup calls has been established (Miller 199 l), which suggests the possibil- ity of individual recognition. However, females approaching calling pups did not follow more direct paths than those returning to silent pups. Additionally, in two of the five paths involving females contacting foreign pups, those pups were calling. In both cases they were the nearest neighbour to the pup of the mother that checked them. Thus, the degree of dis- crimination of which females are capable on the basis of acoustic cues is unclear. Calls alone do not appear to be suffi- cient for females to unambiguously identify their own pup, but a pup calling in a particular area may induce mothers whose pups are in the vicinity to return to the ice surface. Similar conditions governing vocal recognition of pups by female elephant seals have been reported (Klopfer and Gilbert 1967). Pup calls play a relatively minor role in relocation of pups in harp seals compared with otariid seals and harbour seals (Trillmich 1981; Roux and Jouventin 1987; Perry and Renouf 1988; Gisiner and Schusterman 1991).
The quiet, warbling vocalizations emitted by females that were engaged in prolonged searches for their pups may be homologous with the otariid pup attraction call, but they were heard so infrequently that it is not possible to character- ize this call type or its use in any detail.
Final identification using olfactory cues via nosing behav- iour by mother-pup pairs has been described for a variety of pinniped species (e. g . , Bartholomew 1959; Fogden 197 1 ; Lawson and Renouf 1987), including harp seals (e.g., Terhune et al. 1979; Kovacs 1987). In this study, only one nursing session was observed that was not preceded by naso - naso contact. The almost immediate identification of a strange pup by a female when she nosed it was in contrast to the lack of definitive identification through visual appear- ance, acoustic cues, or odour at a distance. There was no indication of the use of olfactory cues for long-distance orientation during this study, nor has this been reported for other pinnipeds. Females were not seen sniffing the air or the ice surface when hauling out or carrying out any scent- marking behaviour either near the pup or along the return path from the water to the pup. Nor did they appear to orient their paths according to wind direction.
The precision of the paths taken by females to return to their pups on the ice provides significant evidence of the abil- ity of females to memorize spatial location. The orientation of females upon surfacing from the water and the directness of their return paths indicate that they anticipate their destina- tion. Successful, direct relocations of silent, nonmobile pups that were hidden behind ice indicate that females do not require direct cues from their pup to orient themselves on the ice, although these cues may simplify the task of relocation. Additionally, the fact that a female was able to repeatedly relocate a stillborn pup that was not visible from her haulout hole suggests that cues provided by pups are secondary to spatial location in the searching process.
The ability of harp seal females to use spatial cues to relo- cate their pups on the pack ice is not unexpected. Many animals have special spatial orientation capabilities that are adaptations to specific environments (see Berry 1971). A random search pattern was observed only in exceptional cir-
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cumstances, once by a female whose pup was not in its nor- mal resting spot and was asleep upon the return of the mother and twice by unknown females whose pups were definitely not in the observation area. It appears that females that have lost their pups search extensively, checking numerous pups while trying to locate their own. Displacement experiments could be used to investigate how females search for lost pups. Additionally, mothers could be rendered temporarily anosmic to test the impact of olfactory cues on both their return paths and their responses to their pups.
A female's selection of a haulout hole close to her pup and the relatively short distance between the pup and the water, in addition to the sedentary nature of pups, further eases the task of relocation. Repeated use of the same hole, even when there were other holes close by, suggests the possible use of kinaesthetic information to memorize return paths.
In conclusion, harp seal mothers use multimodal sensory cues to return to their pups from the water in the pack-ice environment. Spatial information appears to be of primary importance despite the fact that the pack ice is considered to be a highly variable environment. Although the pack-ice landscape changes from day to day, female harp seals return to their pups every 3 or 4 h to nurse, and mothers also check their pup intermittently from the water between nursing ses- sesions (Kovacs 1987; Stewart 1987). Thus, females can regularly update their perceptions of the environment. How- ever, they do not remain in proximity to their pups at all times, as was suggested by Terhune et al. (1979). Female harp seals spend 45% of their time in the water during the breeding period and dive for periods of up to 13 min and to depths of at least 90 m while they are lactating (Lydersen and Kovacs 1993). It is likely that spatial information can be used exclusively by females to return to a specific position on the ice. The sedentary nature of pups means that they are usually found where their mothers last left them, so spatial relocation alone is usually sufficient for a successful reunion. Visual and auditory cues emitted by pups may ease the task of relo- cation, although they can be considered of secondary impor- tance. At close range, olfaction is the definitive means of individual identification of pups by their mothers.
Acknowledgements
I thank Christian Lydersen, Graham Nancekivell, Anita Schenk, and Tim Tinker for their help in the field. Richard Folk's (Cougar Helicopters) skill as our pilot was instru- mental in the successful completion of this research. This study was funded by the Brian Davies Foundation (via a research grant to K.M.K. and D.M. Lavigne, University of Guelph) and by research grants from the Natural Sciences and Engineering Council of Canada to K.M.K. I thank Dave Lavigne for his cooperation. I also thank Ron Schusterman and Beth Perry for their editorial comments. The design of the study benefited from discussions with Marie Claude Gr6bety.
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