Mother Vocal Recognition in Antarctic Fur Seal Arctocephalus gazella Pups: A Two-Step Process

In otariids, mother’s recognition by pups is essential to their survival since females nurse exclusively their own young and can be very aggressive towards non-kin. Antarctic fur seal, Arctocephalus gazella, come ashore to breed and form dense colonies. During the 4-month lactation period, females alternate foraging trips at sea with suckling period ashore. On each return to the colony, females and pups first use vocalizations to find each other among several hundred conspecifics and olfaction is used as a final check. Such vocal identification has to be highly efficient. In this present study, we investigated the components of the individual vocal signature used by pups to identify their mothers by performing playback experiments on pups with synthetic signals. We thus tested the efficiency of this individual vocal signature by performing propagation tests and by testing pups at different playback distances. Pups use both amplitude and frequency modulations to identify their mother’s voice, as well as the energy spectrum. Propagation tests showed that frequency modulations propagated reliably up to 64m, whereas amplitude modulations and spectral content greatly were highly degraded for distances over 8m. Playback on pups at different distances suggested that the individual identification is a two-step process: at long range, pups identified first the frequency modulation pattern of their mother’s calls, and other components of the vocal signature at closer range. The individual vocal recognition system developed by Antarctic fur seals is well adapted to face the main constraint of finding kin in a crowd.     

Vocal signature recognition of mothers by fur seal pups

Subantarctic fur seals, Arctocephalus tropicalis, come ashore to breed in dense colonies and lactating females have to alternate foraging trips at sea with periods ashore during which they suckle their pups. The effectiveness of vocal recognition between mothers and pups, has been shown experimentally. To see whether the recognition abilities of females differ from those of their offspring, we investigated how pups recognize their mother's calls. We used artificially modified signals in playback experiments to determine which acoustic parameters support the recognition process. Pups used both the energy spectrum and the ascending frequency modulation occurring at the beginning of each call. However, they seemed to rely mainly on spectral analyses. The vocal identification process at a perceptual level is therefore asymmetrical, as mothers mainly use temporal structures to recognize their pup's calls. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Individual variation in pup vocalizations and absence of behavioral signs of maternal vocal recognition in Weddell seals (Leptonychotes weddellii)

Individually stereotyped vocalizations often play an important role in relocation of offspring in gregarious breeders. In phocids, mothers often alternate between foraging at sea and attending their pup. Pup calls are individually distinctive in various phocid species. However, experimental evidence for maternal recognition is rare. In this study, we recorded Weddell seal (Leptonychotes weddellii) pup vocalizations at two whelping patches in Atka Bay, Antarctica, and explored individual vocal variation based on eight vocal parameters. Overall, 58% of calls were correctly classified according to individual. For males (n= 12) and females (n= 9), respectively, nine and seven individuals were correctly identified based on vocal parameters. To investigate whether mothers respond differently to calls of familiar vs. unfamiliar pups, we conducted playback experiments with 21 mothers. Maternal responses did not differ between playbacks of own, familiar, and unfamiliar pup calls. We suggest that Weddell seal pup calls may need to contain only a critical amount of individually distinct information because mothers and pups use a combination of sensory modalities for identification. However, it cannot be excluded that pup developmental factors and differing environmental factors between colonies affect pup acoustic behavior and the role of acoustic cues in the relocation process.     

VOCAL INDIVIDUALITY IN MOTHER AND PUP SOUTH AMERICAN FUR SEALS, ARCTOCEPHALUS AUSTRALIS

South American fur seals breeding in Peru are subjected to levels of maternal aggression, and subsequent pup mortality, that are higher than has been reported for any other otariid species. For mothers and pups to maintain contact with each other, a mutual recognition system should exist to facilitate reunion and avoid misdirection of maternal effort. We recorded vocalizations of mothers and pups at Punta San Juan, Peru, during the 1994 and 1995 breeding seasons. Sixteen acoustic variables were measured from a total of 560 calls from 15 mothers and 13 pups. Multivariate analysis showed that calls were variable in several acoustic dimensions. While calls of both mothers and pups showed low variability within and high variability among individuals, mothers' calls were more individualistic. On average, discriminant-function analysis correctly assigned 60% of pup calls and 70% of mother calls to the individual that produced them. Characteristics of the fundamental frequency were most important for distinguishing among mothers, while pup calls, which typically contained less harmonic structure, could be differentiated by formant-like frequency ranges. Thus, calls of mother and pup South American fur seals appear to exhibit sufficient stereotypy to allow for recognition and discrimination among individuals.     

Rapid Onset of Maternal Vocal Recognition in a Colonially Breeding Mammal,the Australian Sea Lion

Background

In many gregarious mammals, mothers and offspring have developed the abilities to recognise each other using acoustic signals. Such capacity may develop at different rates after birth/parturition, varying between species and between the participants, i.e., mothers and young. Differences in selective pressures between species, and between mothers and offspring, are likely to drive the timing of the onset of mother-young recognition. We tested the ability of Australian sea lion mothers to identify their offspring by vocalisation, and examined the onset of this behaviour in these females. We hypothesise that a rapid onset of recognition may reflect an adaptation to a colonial lifestyle.

Principal Findings

In a playback study maternal responses to own pup and non-filial vocalisations were compared at 12, 24 and every subsequent 24 hours until the females'' first departure post-partum. Mothers showed a clear ability to recognise their pup''s voice by 48 hours of age. At 24 hours mothers called more, at 48 hours they called sooner and at 72 hours they looked sooner in response to their own pup''s vocalisations compared to those of non-filial pups.

Conclusions

We demonstrate that Australian sea lion females can vocally identify offspring within two days of birth and before mothers leave to forage post-partum. We suggest that this rapid onset is a result of selection pressures imposed by a colonial lifestyle and may be seen in other colonial vertebrates. This is the first demonstration of the timing of the onset of maternal vocal recognition in a pinniped species.     

How mothers find their pups in a colony of Antarctic fur seals

In Antarctic fur seals, Arctocephalus gazella, mothers must identify their own young among hundreds or even thousands of pups, if they are to invest in their own offspring and avoid misdirecting their parental care. When returning to their breeding colony from a foraging trip of several days at sea, mothers have to find and identify their young before suckling can occur. There appears to be little confusion about which pup belongs to a mother, and adoption is absent or rare. Using behavioral observations, we investigated the means by which female Antarctic fur seals identified their pups in a breeding colony of about 750 mother-pup pairs on Kerguelen Island. We evaluated the importance of vision, scent communication, vocalizations, and rendezvous locations as possible explanations of how mothers find their pups. Every pup that a mother examined, whether her own or not, exchanged naso-nasal inspection with her, suggesting a strong role for olfactory communication in individual recognition. Both mothers and pups called to each other, and mothers that searched for pups over a longer period gave more calls and encountered more pups. Thus, vocalizations may have been used to attract pups that might be offspring. Nursing usually occurred in the same place from the end of one maternal visit to the colony and the arrival at the beginning of the next visit, suggesting that nursing locations may serve as a meeting place, or rendezvous, for mothers and pups. These results suggest that finding pups is a two-stage process for females, in which pups for sampling are attracted by calls or examined at the previous nursing location, and then individual identification is made by olfactory cues.     

The influence of behavioural context on Weddell seal (Leptonychotes weddellii) airborne mother-pup vocalisation

Previous mammalian studies have demonstrated that varying levels of signaller arousal are frequently expressed through vocal behaviour. The potential for callers to convey their motivational state may ensure that recipient responses are appropriate to their needs. The current study investigated the influence of behavioural context on Weddell seal mother-pup vocalisation. Mother and pup call rates were calculated within five and seven behavioural contexts, respectively, and the acoustic characteristics of 69 pup calls were measured within four contexts (total calls = 276). Context significantly influenced the temporal patterning of calls, with reuniting mothers and pups and lone active pups emitting more calls than during mother-pup contact periods. Reuniting and lone pup calls were also characterised by longer durations, higher fundamental frequencies, and increased energy in upper harmonics. Results suggest that reunion events and lone pup searching are characterised by calls reflective of heightened arousal, compared with mother-pup contact periods.     

Energetic costs and thermoregulation in northern fur seal (Callorhinus ursinus) pups: the importance of behavioral strategies for thermal balance in furred marine mammals

Behavioral thermoregulation represents an important strategy for reducing energetic costs in thermally challenging environments, particularly among terrestrial vertebrates. Because of the cryptic lifestyle of aquatic species, the energetic benefits of such behaviors in marine endotherms have been much more difficult to demonstrate. In this study, I examined the importance of behavioral thermoregulation in the northern fur seal (Callorhinus ursinus) pup, a small-bodied endotherm that spends prolonged periods at sea. The thermal neutral zones of three weaned male northern fur seal pups (body mass range = 11.8-12.8 kg) were determined by measuring resting metabolic rate using open-flow respirometry at water temperatures ranging from 2.5° to 25.0°C. Metabolic rate averaged 10.03 ± 2.26 mL O?kg?1 min?1 for pups resting within their thermal neutral zone; lower critical temperature was 8.3° ± 2.5°C , approximately 8°C higher than the coldest sea surface temperatures encountered in northern Pacific waters. To determine whether behavioral strategies could mitigate this potential thermal limitation, I measured metabolic rate during grooming activities and the unique jughandling behavior of fur seals. Both sedentary grooming and active grooming resulted in significant increases in metabolic rate relative to rest (P = 0.001), and percent time spent grooming increased significantly at colder water temperatures (P < 0.001). Jughandling metabolic rate (12.71 ± 2.73 mL O?kg?1 min ?1) was significantly greater than resting rates at water temperatures within the thermal neutral zone (P < 0.05) but less than resting metabolism at colder water temperatures. These data indicate that behavioral strategies may help to mitigate thermal challenges faced by northern fur seal pups while resting at sea.     

Prevalence of allosuckling behaviour in Subantarctic fur seal pups

Non-offspring maternal care should be rare due to the high costs of raising offspring, particularly lactation, but nonetheless occurs in a variety of taxa. Misguided parental care, associated with recognition errors and/or inattentiveness by lactating females, has been hypothesized as an explanation for allolactation in mammals. In an extension of this hypothesis, we suggest that milk-stealing is parasitism instigated by non-filial offspring, and that maternal behaviour is of secondary interest in an evolutionary context if she is unaware of the interaction. We provide evidence for frequent milk-stealing attempts by Subantarctic fur seal (Arctocephalus tropicalis) pups, including an example of sustained non-maternal care (> three months) for one pup during the confirmed absence of his mother, leading to a weaning mass equal to the population mean. We also present only the second account of fostering/twins in the species at this locality. We suggest that rather than the hitherto suggested rare and anomalous behaviour, milk-stealing behaviour (while not always successful) is common.     

INDIVIDUAL VARIATION OF THE FEMALE ATTRACTION CALL PRODUCED BY AUSTRALIAN FUR SEAL PUPS THROUGHOUT THE MATERNAL DEPENDENCE PERIOD

ABSTRACT

Australian fur seals are colonial breeding animals that give birth on crowded rookeries. Females leave their pups unattended for extended periods while they forage at sea. On return to the colony, a mother must relocate her pup amongst the hundreds of other pups. Vocal recognition is thought to play a vital role in maintaining the mother-pup bond. In the present study, four sets of 7 different pups were recorded once each at different times throughout the maternal dependence period. The Female Attraction Call was used to determine whether Australian fur seal pups produce individually distinct calls which could be used as a basis for vocal recognition. Results from three different analyses (PIC, DFA and CART) indicated that the fundamental frequency, number of parts per call, duration, quavering and peak frequency changes at the start, mid-point and end of the call (i.e., along PEAK Fl) were important to recognition. In 75% of cases using DFA, the Female Attraction Call was classified to the correct caller, suggesting that there is sufficient stereotypy within individual calls, and sufficient variation between them, to enable vocal recognition by females.     

Biased estimates of fur seal pup mass: origins and implications

The mass of fur seal pups weighed in different years can be used to estimate growth rates or compared with one another to make inferences about the relative condition of a population. However, unless appropriate precautions are taken, many factors can bias estimates of pup mass and lead to incorrect conclusions. Using data collected from tagged and untagged northern fur seal pups ( Callorhinus ursinus ) at the Pribilof Islands, Alaska, I assess how milk consumption, the timing of sampling, and the effects of growth and sample size influence the size of pups captured for weighing. Evidence is presented suggesting that pup mass may increase in a sigmoid fashion, with the most rapid rate of growth occurring when about two months old. This phenomenon can confound efforts to compare the masses of pups weighed on different days in different years, particularly if pups are weighed over the period of rapid growth. Variability in pup mass increases with time because growth rates of individuals vary and because the amount of milk pups consume increases with body size. Thus sample sizes must be increased as the pups grow older in order to detect statistically significant differences in mean body mass. There is also evidence that pups of different ages and sizes are not randomly distributed on the breeding beaches and are not randomly selected for weighing. It appears that the first pups captured for weighing are smaller and younger than subsequent captures, possibly because smaller pups are easier to handle and are segregated to the peripheral rookery regions where sampling begins. These hidden biases, related to sampling error and fur seal biology, must be considered and controlled for when weighing fur seal pups.     

Factors affecting weaning weight in Antarctic fur seals Arctocephalus gazella at South Georgia

Summary Relationships between size, body condition, age and feeding-attendance patterns during pup rearing of female Antacrtic fur seals Arctocephalus gazella and their effects on the timing of birth and weaning, pup weight, growth and condition were studied at South Georgia in 1981–1982. Twenty-seven (6 male, 21 female) mother-pup pairs were followed from birth to weaning. The analysis of maternal effects was limited to female pups because of the small sample size of male weaners. High weaning weight was associated with those female pups whose mothers spent more time ashore attending their offspring. Weaning weight showed no relationship with perinatal duration, number of feeding trips to sea, days at sea or date of weaning. A further 63 mother-pup pairs were analysed for the effects of maternal body condition (weight/length), age and timing of birth on offspring body weight and condition. Pup weight and condition were weakly correlated with maternal age in female pups. Male pups born earlier in the season were heavier and in better condition. Maternal and offspring body weight and condition were unrelated. For the Antarctic fur seal population at South Georgia where the food supply was apparently not limiting in summer, maternal condition and foraging time were subordinate to maternal care on land (as expressed by attendance duration) in determining offspring weight at weaning.     

Observations on the infectivity of parasitic third-stage larvae of Uncinaria lucasi Stiles 1901 (Nematoda: Ancylostomatidae) of Northern fur seals, Callorhinus ursinus Linn., on St. Paul Island, Alaska.

Twelve fur seal pups, which had not nursed their mothers, were used in an infectivity experiment. Pups were exposed to parasitic 3rd-stage larvae of Uncinaria lucasi from belly tissues of fur seal bulls, bachelors, and pregnant cows, to determine maturation capability of the larvae. Hookworms were not recovered from the intestines of 3 pups receiving larvae from belly blubber of bulls, 6 pups receiving larvae from belly blubber of bachelors, and 1 nonexposed pup. Maturation of hookworms did occur in 2 pups exposed to larvae from a mixture of belly blubber, mammary tissue, and milk of pregnant cows. Parasitic 3rd-stage hookworm larvae from belly tissues of pregnant and "non-pregnant" fur seal cows averaged 938.1 and 802.1 micron long, and 34.1 and 31.5 micron wide, respectively; however, larvae from belly tissues of a fur seal bull, bachelors, 2-year-old males, male and female yearlings and pups, and Steller Sea Lion subadults averaged 640.5-732.0 micron long and 20.9-24.9 micron wide.     

Holocene changes in the ecology of northern fur seals: insights from stable isotopes and archaeofauna

The remains of northern fur seals (Callorhinus ursinus) are among the most abundant of pinniped elements recovered from mainland coastal archaeological sites in both California and Oregon. This is surprising as all contemporary northern fur seals breed exclusively on offshore islands, primarily at high latitudes, and the species is otherwise pelagic. The vulnerability of these animals to human predation suggests that either humans were foraging much further offshore than has been presumed or alternatively that the ecology of these animals has shifted during the late Holocene. We used isotopic and archaeofaunal analysis of the remains of pinnipeds from the middle to late Holocene of central and northern California to clarify the breeding and foraging behavior, and migration patterns of these ancient animals. The carbon and nitrogen isotope compositions of ancient northern fur seals reveal that these animals fed as far offshore as they do today, and that they remained at middle latitudes throughout the year. From an archaeological site at Moss Landing, California, we identified 16 skeletal elements from at least 12 very small northern fur seal pups. From another site near Mendocino, California, we identified the remains of at least 6 pups. We estimate the size and age of 5 of the young animals using sex-specific regressions of body length on the short dentary length derived from measurements of modern specimens. Our estimates indicate these ancient pups were substantially smaller, and therefore younger, than modern 3-month-old northern fur seal pups from similar latitudes and their nitrogen isotope compositions suggest they had not been weaned. As present-day northern fur seals do not leave their rookeries until they are at least 4 months old, we consider it highly unlikely that these ancient pups swam to these mainland locations from some distant island rookery. While there are numerous nearshore rocky outcrops along the Mendocino Coast, which may have supported small breeding colonies, the Moss Landing site is centered on a 40-km-long sandy beach, and is more than 120 km from what at the time were the nearest offshore islands. We conclude that northern fur seal adult females, subadults, and pups whose remains were recovered at the Moss Landing archaeological site must have been taken at a mainland rookery. Evidence that northern fur seals once bred on the mainland at this central California location suggests that the abundant remains of these animals at numerous other archaeological sites along the California coast also reflect the presence of nearby mainland rookeries. Based on the relative abundance of their remains in ancient human occupation sites and the widespread distribution of sites where their remains have been found, it appears that northern fur seals were once the predominant pinniped throughout a region where they now only rarely occur. Furthermore, their presence along the central and northern California coasts appears to have once severely limited the distribution of other pinnipeds, which are now common to the region.     

Maternal buffering of stress response in free‐ranging Pacific harbor seal pups in Alaska

We examined the effects of maternal buffering in free‐ranging Pacific harbor seal pups during capture and handling research procedures. We predicted that pups held with their mother would benefit from social buffering and exhibit lower cortisol concentrations resulting from capture and handling than dependent pups caught without their mothers and weaned pups. We expected that pups captured with their mother that experienced a short separation would exhibit increased stress‐induced vocal behavior and activity level compared to dependent weaned pups caught alone. The results showed that the presence of the mother significantly buffered the stress response, as measured by reduced serum cortisol concentrations, in pups captured with their mothers as compared to dependent pups captured alone. Cortisol concentrations of mothers with pups initially were higher than nonlactating females, then diminished. Pups showed a significantly higher rate of vocalization soon after maternal separation compared to single pups separated for a longer period of time. Newly separated pups, especially males, showed a high level of activity compared to the other pups. The results provide unique quantitative evidence of the physiology underlying the maternal‐pup bond in a marine mammal, and the role that maternal buffering may play on the stress response of the offspring.     

Individual recognition in wild bottlenose dolphins: a field test using playback experiments

We conducted playback experiments with wild bottlenose dolphins, Tursiops truncatus, to determine whether there is sufficient information in their individually distinctive signature whistles for individual recognition. We conducted experiments with members of a resident community of dolphins in waters near Sarasota, Florida, during temporary capture-release projects. We used a paired playback design, wherein the same two whistle sequences were predicted to evoke opposite responses from two different target animals. This design controlled for any unknown cues that may have been present in the playback stimuli. We predicted that mothers would respond more strongly to the whistles of their own independent offspring than to the whistles of a familiar, similar-aged nonoffspring. Similarly, we predicted that independent offspring would respond more strongly to the whistles of their own mother than to the whistles of a familiar, similar-aged female. Target animals were significantly (P<0.02) more likely to respond to the predicted stimuli, with responses measured by the number of head turns towards the playback speaker. In bottlenose dolphin societies, stable, individual-specific relationships are intermixed with fluid patterns of association between individuals. In primate species that live in similar 'fission-fusion' type societies, individual recognition is commonplace. Thus, when taken in the context of what is known about the social structure and behaviour of bottlenose dolphins, these playback experiments suggest that signature whistles are used for individual recognition. Copyright 1999 The Association for the Study of Animal Behaviour.     

Lactating Females Do Not Discriminate Between Their Own Young and Unrelated Pups in the Communally Breeding Rodent, Octodon degus

Females in numerous rodent species engage in communal nesting and breeding, in which they share one or more nests to rear their young. A potential cost of communal nesting and breeding is that mothers divert resources to unrelated offspring. One way mothers could avoid this cost is to recognize and favour their own young over unrelated offspring when allocating maternal effort. We assessed whether female degus (Octodon degus), a communally nesting and breeding caviomorph rodent, discriminate between their own and unrelated offspring during lactation. Female degus previously have been shown to distinguish between their own and unrelated pups when exposed to odours from both. We measured pup discrimination based on differences in the retrieval behaviour of females that were in early or intermediate lactation directed towards their own and unrelated offspring; offspring presented were of similar or different age. Before any event of pup retrieval, lactating females spent similar amounts of time and interacted to a similar extent with their own and unrelated pups. During pup retrieval, all lactating females transported both pups to the nest. Neither relatedness to pups, nor pup‐age differences, influenced the order in which pups were retrieved to the nest. Dams waited similar amounts of time before retrieving the first pup when the first transported young was their own or unrelated. Likewise, females waited similar amounts of time before retrieving the second pup when the pup transported first was their own or unrelated. The time between first and second pup transport events was longer when dams were in early when compared with intermediate lactation, but only when pups were of similar age. All experimental subjects nursed unrelated pups after they were retrieved. Collectively, our results do not support the hypothesis that communally breeding female degus use their recognition ability to discriminate against unrelated offspring in favour of their own young.     

Patterns of paternal relatedness in British grey seal colonies

Previous studies of breeding behaviour in the grey seal, Halichoerus grypus, have painted conflicting pictures. Behavioural observations suggest a classical polygynous system with a small number of dominant males fathering most of the offspring. However, genetic analysis suggests that many potential fathers spend little time ashore, that some pairs of seals show partner fidelity and that the dominant males are not as successful as their behaviour would suggest. Here we used paternal relatedness between pups with known mothers, sampled over an 11-year period, to show that behavioural dominance leading to enhanced fitness is a feature of only a handful of males located near the centre of the breeding colony. The vast majority of pups are fathered by any of a large number of males who all share approximately equal success, including virtually all those males who have previously escaped our best sampling efforts. As expected, the frequency of full-sibs is reduced in this longer time series relative to the original study. However, absolute estimates of the frequency of full-sibs seem to be confounded by a tendency for females who produce paternally unrelated pups to have conceived to males who are more genetically dissimilar from each other than expected by chance alone. Together, these elements of breeding behaviour would help to maintain maximum genetic diversity and to minimize the effects of inbreeding.     

Offspring kidnapping with subsequent shared nursing in Antarctic fur seals

Non-offspring maternal care should be common in phocids, but their occurrence would be uncommon among otariids due to the high costs of raising offspring, particularly lactation, and an efficient recognition system that allow for accurate recognition during the frequent mother–pup re-associations. However, non-offspring maternal care has been documented in some otariid species. While the phenomenon in general is not novel among the colonially breeding seals, the exclusive care to a single pup by two lactating females for an extended time is a behavior scarcely documented in natural population. In an extension of this allonursing care, we document the first case of the kidnapping of a pup with subsequent shared nursing in Antarctic fur seal including data on the effect of this interaction on the pup’s growth. While all other lactating females nursed exclusively their own pups, the shared nursing was advantageous for the pup because he grew noticeably larger (in weight and axillary girth) than other of his cohort, particularly after 50 days. This advantage would have been influenced by the asynchrony of the foraging cycle of the biological and foster mother, which resulted in a higher attendance on shore than any other male pups. Although several explanations have been hypothesized for allolactation in mammals, our observations suggest a misguided parental care, associated with recognition errors by the foster mother whose pup was stillborn.     

Maternal discrimination of offspring vocalizations in Barbary macaques (Macaca sylvanus)

The response of Barbary macaque (Macaca sylvanus) females to vocalizations of their offspring was studied in a semi-free ranging population. The results of both facal observations and playback experiments demonstrated that mothers preferentially turned to their offspring's vocalizations over those of other young, providing evidence that mothers are able to recognize their offspring by acoustic signals alone. We assume that they may use this ability to monitor their infants' activities.