Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2003? 2003 802 305312 Original Article VOCAL MEMORY IN FUR SEALS I. CHARRIER

Biological Journal of the Linnean Society, 2003, 80, 305–312. With 2 figures

Fur seal mothers memorize subsequent versions of developing pups’ calls: adaptation to long-term recognition or evolutionary by-product? ISABELLE CHARRIER1,2*, NICOLAS MATHEVON1,3 and PIERRE JOUVENTIN2 1

Laboratoire de Biologie Animale, Université Jean Monnet, St Etienne, France. CEFE-CNRS UPR 9056, Equipe d’Ecologie Comportementale, Montpellier, France. 3 NAMC-CNRS UMR 8620, The BioAcoustics Team, Université Paris-Sud, Orsay, France 2

Received 18 December 2002; accepted for publication 31 March 2003

In pinnipeds and especially in otariids, mothers and pups develop the capacity to recognize each other’s voices. Pups become able to discriminate their mother’s voice a few days after birth. For females, this discrimination seems to occur earlier, probably during the few hours after parturition. However, during lactation, mothers are confronted with a major problem: the change of the characteristics of their pup’s calls. To investigate this problem, we first performed an acoustic analysis of pups’ calls from birth to weaning to identity the successive different versions of these calls. Secondly, we performed playback experiments just before weaning to test if females retain these different versions over a long time period. The acoustic analysis of pups’ calls reveals that several characteristics of their vocalizations change with age. Playback experiments demonstrate that females still recognize all the successive immature and mature versions of their pup’s calls. In our opinion, this long-term memorization seems to be a by-product of the permanent pups’ voice learning from birth to weaning since no apparent adaptive benefit seems to arise from this capacity. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 305–312.

ADDITIONAL KEYWORDS: learning – memory – mother–pup interactions – vocal recognition.

INTRODUCTION In pinnipeds, mother–pup recognition is essential for enabling reunion when mothers return from the ocean or whenever mothers and pups are separated within the colony. Olfaction, vision and audition have been shown to be involved in this identification process (Bartholomew, 1959; Peterson & Bartholomew, 1969). Since pinnipeds are myopic in air (Wartzok & Ketten, 1999), vision is unlikely to be used for individual identification. Olfaction is well developed in pinnipeds (Rand, 1955; Bartholomew, 1959); however, olfactory signals seem to be used only in a final check when mothers and pups are at close range (Bonner, 1968; Stirling, 1971). In contrast, acoustic signals are efficient over long and short distances, and appear to be a ET AL.

*Corresponding author. E-mail: [email protected]. Present address: Songbird Neuroethology Laboratory, P450 Biological Sciences Building, Department of Psychology, University of Alberta, Edmonton, T6G 2E9, Canada.

key factor for mother–pup identification (Trivers, 1972; Falls, 1982; Gould, 1983). Vocal recognition of mothers by pups has been experimentally shown in several otariid species (Trillmich, 1981; Insley, 2000, 2001; Charrier, Mathevon & Jouventin, 2001, 2003), but mutual recognition has been reported in two species only (in Callorhinus ursinus: Insley, 2000, 2001; in Arctocephalus tropicalis : Charrier et al., 2001, 2003). Pups are able to discriminate their mother’s voice a few days after birth (2–5 days after birth in Arctocephalus tropicalis, Charrier et al., 2001). Although this has not been experimentally tested, mothers must learn to recognize their pup’s calls and this seems to occur within a few hours after parturition (Bartholomew, 1959). Mother–pup recognition lasts for up to several years after weaning (in C. ursinus: Insley, 2001). Changes in the acoustic structure of bird and mammal vocalizations have been shown to occur throughout ontogeny, due to growth-induced modifications in the vocal tract and brain maturation (Beecher,

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Beecher & Hahn, 1981; Jones, Falls & Gaston, 1987; Mountjoy & Lemon, 1995; Jorgensen & French, 1998). It is likely that the vocal characteristics of fur seal pups also change during the period of lactation (Insley, 2000). Given that mother–pup recognition remains efficient throughout lactation (Charrier, Mathevon & Jouventin, 2002), mothers may therefore be confronted with changes in the acoustic characteristics of their pup’s call. In this paper, we study mother–pup recognition in the Subantarctic fur seal Arctocephalus tropicalis . Like most pinnipeds, this species breeds ashore in large and dense colonies. At the beginning of the austral summer, each female gives birth to a single pup which is dependent on her for 10 months (from December to October: Bester et al., 1987). Like most otariid species, maternal care is exclusive, A. tropicalis females suckling only their offspring (Stirling, 1975; Boness, 1990; Georges, Sevot & Guinet, 1999). During the lactation period, females alternate suckling periods with foraging trips at sea, and periodically leave their pup alone in the colony for 2–3 weeks (Georges & Guinet, 2000). The great distances mothers have to cover in the ocean to find appropriate resources explain the long duration of these foraging trips (Georges & Guinet, 2000). This constitutes a strong ecological constraint for the pups since they are then subjected to long fasting periods, which may be difficult to support for growing animals (Guinet & Georges, 2000). Mother–pup vocal recognition has been demonstrated in this species, and the acoustic features supporting this identification process are known (Charrier et al., 2002, 2003). This vocal recognition system is particularly effective since, in spite of the high risk of confusion due to the great density of individuals in the colony, mother–pup pairs have been shown to meet in less than 11 min when the mothers returned from foraging trips at sea (Charrier et al., 2001). Vocal recognition of pups by mothers occurs from birth to weaning. We first studied the ontogeny of pups’ vocalizations to detect changes of vocal characteristics during growth by performing an acoustic analysis of calls at different ages. Next, we used playback experiments at the end of the rearing period to test whether mothers retain the changing vocal versions of their pups.

MATERIAL AND METHODS STUDY

LOCATION AND ANIMALS

This study was carried out on an A. tropicalis colony located on Amsterdam Island (37 °55′S, 77°30′E) in the Indian Ocean, from December 1999 to August 2000. At the end of November, females returned to the colony after 2 months at sea. They give birth to a single pup

a few days after their arrival. The 10-month rearing period consists of suckling periods ashore (4–5 days) alternating with foraging trips at sea (10–20 days) (Bester, 1987; Georges & Guinet, 2000). The study colony named ‘La Mare aux Elephants’ comprised 500–550 adult females. Females have been tagged for several years, and their respective pups are marked shortly after birth using temporary labels glued onto their fur. At approximately 1 month old, each pup is double-tagged in the web of the fore flippers with an individually numbered plastic tag.

RECORDING

AND SIGNAL ACQUISITION

This study was restricted to ‘female attraction calls’ emitted by pups (Fig. 1) which have been shown to support recognition of pups by mothers (Bartholomew, 1959; Paulian, 1964; Bonner, 1968; Peterson et al., 1968; Stirling, 1971; Trillmich, 1981). Recordings were performed with an omnidirectional Revox M 3500 microphone (frequency bandwidth 150– 18 000 Hz, ±1dB) mounted on a boom (2 m long) and connected to a Sony TC-D5M audiotape recorder. Calls were recorded when a pup and its mother were separated and trying to find each other, for example when a mother returned from a feeding trip or a short swim. The distance between the emitting pup and the microphone was approximately 0.5 m. This relatively short distance never disturbed the behaviour of calling pups. Calls were digitized with a 16-bit acquisition card at a sample rate of 22 050 Hz, using acquisition software (Cool Edit, Johnston, 1996). Recordings were performed throughout the breeding period at different ages (1, 2, 4, 6, 15, 30, 60, 90, 150, 180 and 210 days old). We primarily chose to follow 26 mother–pup pairs. However, the high mortality of pups during the first month of life meant that we lost a high number of pups and thus we were only able to follow nine mother–pup pairs throughout the whole breeding period, from birth to 7 months old. Moreover, we were not able to record each pup at all ages because of field constraints (e.g. pups are highly mobile and sometimes very difficult to find in the colony; bad weather conditions often impaired recordings). Our data set therefore comprised acoustic signals of five to eight individuals at each age (except for 150 days old for which only three individuals were recorded) with four to seven calls per individual, giving a total of 345 calls. To perform the acoustic analysis, we pooled the ages into four age groups: <1 week old (1, 2 and 4 days old), 1–2 weeks old (6 and 15 days old), 1–3 months old (30, 60 and 90 days old) and 5–7 months old (150, 180 and 210 days old). As we did not have enough recordings for two individuals, we could not include either of these pups in our study. The analysis was therefore

© 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 305–312

VOCAL MEMORY IN FUR SEALS Frequency (kHz)

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B

0.8 Frequency (kHz) dQuavering 7

FMrange

A

0.4 Autocorrelation

0.5

Time(s)

1

3.5

0.5

1

dtot

Times (s)

FFT Fmaxl (2)

FunFreq

C

Amplitude

Fmaxl (3)

0

1

2

Fmax3 (6)

3

4

5

6 7 Frequency (kHz)

Figure 1. Parameters of pups’ calls measured for the acoustic analysis. (A) Oscillogram and spectrogram of pup from which the total duration of the call (dtot) and the duration of the quavering (dQuavering) were measured. (B) Range of the frequency modulation (FMrange) on the fundamental frequency was measured using autocorrelation. (C) On the FFT spectrum, we identified the value of the fundamental frequency (FundFreq) and the rank of the first three frequencies with peak amplitude (Fmax1–3).

made on seven pups (four age groups) and a total of 281 calls.

ACOUSTIC

ANALYSIS OF PUPS’ CALLS

To study the change in pups’ call structure during the breeding period, we analysed several acoustic parameters at each age group. Our methods of analysis were similar to those employed in a previous study, in which we described the individual acoustic signature in calls of 7–8-month-old pups (for details, see Charrier et al., 2002). In this study, we focused on the call parameters known to encode the acoustic individual signature of pups and to be used by mothers to identify their offspring: females pay particular attention to the spectral energy distribution and the frequency modulation, whereas amplitude modulation is not used in the recognition process (Charrier et al., 2002). The following seven parameters were therefore measured to characterize the acoustic structure of the pups’ calls (Fig. 1). We measured the value of the fundamental frequency (FundFreq, Hz), and the harmonic values corresponding to the first, second and third peak amplitudes (respectively Fmax1, Fmax2 and Fmax3). As the value of the fundamental is likely to change with age, the numerical values of the associated harmonics are also likely to vary. To be able to

compare the energy distribution in the spectrum between calls of different ages (e.g. we wanted to know which harmonics were energetically reinforced), the eventual developmental effects needed to be controlled. Then, to create a picture of the energy distribution within the frequency spectrum for each considered call, the harmonic values corresponding to the first, second and third peak amplitudes were coded by their position in the spectrum rather than their absolute numerical value. For example, if Fmax1 was the second harmonic in a given call, Fmax2 the fundamental and Fmax3 the first harmonic, then Fmax1 = 3, Fmax2 = 1 and Fmax3 = 2. To study the frequency modulation of the call, we measured the range of the frequency modulation (FMrange, Hz). A visual inspection of spectrograms showed that a fast frequency modulation, named quavering, is typically present over the majority of each call (see Fig. 1), so to describe the frequency modulation of the call, we had to take into account this parameter. We therefore measured the duration of the quavering part and the total duration (dtot) of the call to assess the percentage of quavering (%Quavering = dQuavering/dtot). To compare a given parameter among individuals and among different age groups we performed Friedman’s test, a non-parametric test allowing comparisons of repeated measures (Sokal & Rohlf, 1995). For

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coded data (Fmax1, Fmax2 and Fmax3), we used the chi-square test for independency between two parameters (Fmax1–3 and age groups) (Sokal & Rohlf, 1995).

PLAYBACK

RESULTS

PROCEDURE

Playback tests on females were performed when their pups were 7 months old. All nine mothers were challenged except female C (who was not present at the time of testing). Experimental signals were broadcast to mothers using a Sony TC-D5M tape recorder connected to an Audax unidirectional loudspeaker via a customised amplifier (10 W; frequency response 1–9 kHz, ± 4 dB). The loudspeaker was placed 3–4 m from the female being tested. Tests were carried out when mothers and pups were separated in the colony. During a playback session, we broadcast to a given female an experimental tape containing five consecutive experimental series, each series being composed of a repetition of four pups’ calls, as follows: one series consisted of four calls of the test female’s own pup recorded when the pup was 1–2 days old (‘age1 series’); one series constituted of four calls of the tested female’s own pup recorded when the pup was 1 month old (‘age2 series’); one series constituted of four calls of the tested female’s own pup recorded when the pup was 3–5 months old (‘age3 series); one series constituted of four calls from a strange (non-offspring) pup (‘stranger series’); and the ‘control series’ constituted four calls of the tested female’s own pup recorded a few hours before the playback experiment (i.e. when the pup was 7 months old). The order of presentation of the series was randomized for each mother. Calls were emitted at natural rates (1 call per 3 s, I. Charrier, pers. observ.) and were played at a natural sound pressure level (SPL = 75 ± 7 dB measured at 1 m, using a Bruël & Kjaer sound level meter type 2235). Between the broadcasting of each experimental series, we waited until the mother’s behaviour was calm (motionless and silent). In addition, there was always a minimum of 10 min between each series.

CRITERIA

with age1, age2 and age3 series with those elicited by the control series and those elicited by the stranger series.

OF RESPONSE

Under natural conditions, a mother responds to her own pup’s calls by calling and orienting towards her calling offspring. Prior to the broadcasting of an experimental series, we observed the test mother for 2 min. During the playback test, the female’s behaviour was scored with two simple dichotomous parameters: first, whether or not females called in response to the playback (‘calling response’); second, whether or not females orientated towards the speaker (‘orientation response’). We then used the McNemar test (Sokal & Rohlf, 1995) to compare the behavioural responses obtained

DEVELOPMENTAL CHANGES IN

PUPS’ CALL STRUCTURE

Regardless of the pups’ age, the female attraction call was a complex, tonal sound composed of a fundamental frequency and its associated harmonics (up to 15) and was modulated in frequency. However, the fine acoustic characteristics of this call varied considerably through the pup’s early development (Fig. 2). Table 1 presents the results of the analysis of calls for each individual. To simplify the table, only the oldest call version (i.e. when the pup was <1 week old) and the youngest call version (i.e. when the pup was 5–7 months old) have been presented. However, as mentioned above in the Material and Methods, the statistical comparison was performed on the four age groups (Friedman’s test). The value of the fundamental frequency and the percentage of quavering changed significantly with the pups’ age. The most conspicuous trait was that quavering was only produced during the first 15 days of life. The range of frequency modulation (FMrange) changed for some pups; however, these differences were not significant with pups’ age (Table 1). Table 2 presents the results of the chi-square test of independence between Fmax1–3 and the age groups. Considering spectral cues, the three parameters Fmax1–3 were strongly dependent on age group (P < 0.001, Table 2). The energy distribution among the spectra appeared to be characterized by instability over time. For instance, as pups matured, the spectral energy tended to concentrate over the first harmonics (Fig. 2) whereas some higher-pitched frequencies were reinforced when pups were very young.

PLAYBACK

EXPERIMENTS ON MOTHERS

Results of the playback experiments are summarized in Table 3. Females never reacted to calls of strange (non-offspring) individuals: they did not call in response (χ20.05 (1) = 5.14, P < 0.05), and did not show orienting movements towards the emitting source. In contrast, the behavioural response (calls and orienting movements) obtained by calls of different ages from their own pup did not differ statistically from the behavioural response elicited by the control calls (χ20.05 (1) = 1.33 (NS)).

DISCUSSION We investigated the variability of A. tropicalis pups’ calls throughout the breeding period and the ability of

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Frequency (kHz) 7

7d

1d

15d

3.5

Frequency (kHz) 7

1m

7m

3m

3.5

300 ms

Figure 2. An example of one pup’s calls at different ages (1 day, 7 days, 15 days, 1 month, 3 months and 7 months). The general structure of the call changed with the pup’s age: quavering occurred only during the first 2 weeks of life, and the distribution of energy among frequencies tended to be more concentrated in the higher pitched frequencies when pups were very young. d = day; m = month. Table 1. Mean ± SD values of each parameter for the oldest (<1 week old) and youngest (5–7 months old) call version, and results of the statistical analysis on the acoustic parameters with comparisons between different age groups ( n = 7)

Individual pup

frequency (Hz)

Fundamental Fmax 1-2-3*

FM range (Hz)

%Quavering

A

443 ± 22 483 ± 68 487 ± 74 619 ± 37 497 ± 47 596 ± 21 529 ± 23 562 ± 66 467 ± 12 471 ± 24 487 ± 29 654 ± 52 641 ± 35 568 ± 21 <0.01

2-6-3 2-1-3 3-5-4 1-3-2 1-2-3 1-2-5 2-5-9 2-1-3 3-4-2 2-3-5 2-1-5 1-2-3 1-5-6 1-2-4 –

268 ± 32 265 ± 56 280 ± 83 201 ± 82 268 ± 61 327 ± 67 284 ± 38 335 ± 84 285 ± 65 286 ± 41 310 ± 79 243 ± 12 279 ± 98 448 ± 105 >0.05, NS

68 ± 25 0 91 ± 19 0 89 ± 19 0 34 ± 28 0 62 ± 37 0 53 ± 37 0 41 ± 31 0 <0.01

Oldest Youngest B Oldest Youngest C Oldest Youngest D Oldest Youngest E Oldest Youngest O ldest Youngest G Oldest Youngest Friedman’s test (P)†

*For these three parameters, the mode is presented for scoring data (1: fundamental frequency, 2: first harmonic, 3: second harmonic, etc.…). †Friedman’s test for repeated measures.

mothers to recognize older versions of their own offspring’s vocalizations. The acoustic analysis revealed that pup calls changed gradually over the rearing period. In particular, some acoustic parameters known

to support individual recognition of their offspring by mothers, i.e. the pup’s vocal individual signature, varied from the first days after birth to weaning. Indeed, we found that the energy spectrum and the quavering

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(a characteristic of frequency modulation) varied significantly with age whereas the other frequency modulation characteristic, the FMrange, seemed to be stable over time (the variation was not significant). Recently, we found that the essential parameters used in the recognition process by mothers are the frequency modulation and the spectral energy distribution of pups’ calls (Charrier et al., 2002). Playback experiments showed that A. tropicalis females consistently responded to their own pups’ calls, regardless of the age at which the test call was recorded. This suggests that mothers retain all of the successive versions of their pups’ calls even if features of their acoustic structure vary throughout the rearing period. Thus, Table 2. Results of the chi-square test of independence between Fmax1–3 and the age groups (d.f. = 50)

χ2measured

χ2α = 0.005

Fmax1/age groups

Fmax2/age groups

Fmax3/age groups

110.315 79.49

186.625 79.49

166.964 79.49

Each of the three spectral characteristics of pups’ calls was highly significantly dependent on age group (P < 0.005).

mothers must be capable of permanently learning their pup’s vocal characteristics.

A

STRONG MEMORIZATION PROCESS

In numerous species of mammals, mothers develop a strong attachment and ability to recognize their offspring by auditory, olfactory and/or visual cues, a process analogous to the ‘filial imprinting phenomenon’ (Chalmers, 1983). Filial imprinting has been widely studied, especially in precocial birds, such as ducks, domestic chicks and goslings (Lorenz, 1937; Sucklin, 1972; Bolhuis, 1991; Bolhuis & Honey, 1998; Shettleworth, 1998), and in ungulate mammals (Smith, 1965; Shillito & Alexander, 1975; Shillito-Walser & Alexander, 1980; Nowak, 1989). The filial imprinting phenomenon occurs shortly after birth and is unalterable. However, the imprinting process may not be restricted to newborn animals: ‘maternal imprinting’ also exists, for example in ungulates (Klopfer, Adams & Klopfer, 1964; Klopfer, 1971; Gubernick, Jones & Klopfer, 1979; Gubernick, 1980; Porter et al., 1991) and in primates (Maestripieri, 2001). Maternal imprinting occurs during a brief period after parturition in which mothers learn to recognize the voice and/or odour of their young (Lawson & Renouf, 1987; Terrazas et al., 1999;

Table 3. Mothers’ behavioural responses to playback experiments Individual mother

Age1

Age2

Age3

Strange

Control

Response to calls A B D E F G H I Difference with control

1 0 0 1 0 1 0 1 No

1 0 1 0 0 1 1 0 No

1 0 0 1 0 1 0 1 No

0 0 0 0 0 0 0 0 Yes

1 0 1 1 1 1 1 1 –

Response to orientation movements A B D E F G H I Difference with control

1 1 1 1 1 1 1 1 No

1 1 1 1 1 1 1 1 No

1 1 1 1 1 1 1 1 No

0 0 0 0 0 0 0 0 Yes

1 1 1 1 1 1 1 1 –

We used a dichotomous ethological scale where 0 represents a negative response (no call or no orientation movements were observed) and 1 represents a positive response (calls or orientation movements were observed). Comparisons between the behavioural responses obtained with the control and those obtained with the different experimental series were made using the McNemar test (alpha level used for the analysis: P < 0.05). © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 305–312

VOCAL MEMORY IN FUR SEALS Addae et al., 2000; Ferreira et al., 2000). Early maternal learning is also observed in A. tropicalis: mothers are able to recognize their young a few minutes after birth using acoustic cues (I. Charrier, pers. observ.; Charrier et al., 2002) and possibly olfactory cues. Our results show that this memorization is long-lasting: mothers still responded to calls of their newborns when heard 7 months after birth, even though the acoustic individual signature of their pups had changed in that time.

LONG-TERM

RECOGNITION: ADAPTATION OR

EVOLUTIONARY BY-PRODUCT?

The vocal recognition process during the breeding period is very important for both pups and mothers, and therefore can be considered as an adaptation to the severe ecological constraints imposed on this species. In the northern fur seal Callorhinus ursinus, another otariid species with a similar pattern of maternal attendance, mothers and pups are able to mutually retain their calls for at least four years (Insley, 2000). This result is somewhat surprising from an evolutionary point of view since there is no apparent adaptive benefit for this long-term memory. Some hypotheses have been proposed to explain this longterm recognition ability, suggesting that fitness benefits may arise from cooperation or mate choice (Insley, 2000). Such traits have been found in a number of social and cooperative species living in permanent groups, for example in birds (McGregor & Avery, 1986; Godard, 1991) and in elephants (McComb et al., 2000). Even if, in our opinion, this explanation is not fully satisfying with regard to the social context of fur seals, more investigations on cooperation between related individuals and on mate choice have to be performed to conclude on the ‘non-adaptiveness’ of this long-term recognition. In conclusion, we suggest that the vocal recognition after weaning or the mothers’ ability to retain each version of their pup’s developing call are by-products of the strong ‘permanent and unalterable learning’ experienced by mothers when rearing their young.

ACKNOWLEDGEMENTS We thank the members of the 50th and the 51st scientific missions on Amsterdam Island for their help in the field, and particularly Gwenaël Beauplet, Murielle Ghestem, Rémy Andrada, Catherine Baur, Yann François, Arnaud Jeulin, Florence Patural, Sébastien Ricaud and Vincent Rouvreau. This research was supported in the field by the ‘Institut Français pour la Recherche et Technologie Polaires (IFRTP)’. These experiments comply with French legislation and were submitted to the ethics committee of the IFRTP.

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I.C. was supported financially by the Ministère de l’Education Nationale, de Recherche et de la Technologie (MENRT). We warmly thank Alana Phillips for her kind advice on the manuscript. Special thanks to Joel Attia and Mohamed Rehailia for their assistance with statistics, and two anonymous referees for helpful comments.

REFERENCES Addae PC, Awotwi EK, Oppong-Anane K, Oddoye EOK. 2000. Behavioural interactions between West African dwarf nanny goats and their single-born kids during the first 48 hours post-partum. Applied Animal Behavioural Science 65: 53–61. Bartholomew GA. 1959. Mother-young relations and the maturation of pup behaviour in the Alaska fur seal. Animal Behaviour 7: 63–171. Beecher MD, Beecher IM, Hahn S. 1981. Parent-offspring recognition in bank swallows (Riparia riparia): II development and acoustic basis. Animal Behaviour 29: 95–101. Bester MN. 1987. Subantarctic fur seal, Arctocephalus tropicalis. In: Croxall J, Gentry RL, eds. Status, biology, and ecology of fur seals. NOAA Technical Report NMFS 51: 57–60. Bolhuis JJ. 1991. Mechanisms of avian imprinting: a review. Biological Review 66: 303–345. Bolhuis J, Honey RC. 1998. Imprinting, learning and development: from behaviour to brain and back. Trends in Neurosciences 21: 306–311. Boness DJ. 1990. Fostering behavior in Hawaiian monk seals: is there a reproductive cost? Behavioural Ecology and Sociobiology 27: 113–122. Bonner WN. 1968. The fur seal of South Georgia. Britannic Antarctical Survey Scientific Report 56: 1–81. Chalmers N. 1983. The development of social relationships. In: Halliday TR, Slater PJB, eds. Animal behaviour, Vol. 3. Genes, development and learning. London: Blackwell Scientific Publications, 114–148. Charrier I, Mathevon N, Jouventin P. 2001. Mother’s voice recognition by seal pups. Nature 412: 873. Charrier I, Mathevon N, Jouventin P. 2002. How does a fur seal mother recognize the voice of her pup? An experimental study of Arctocephalus tropicalis. Journal of Experimental Biology 205: 603–612. Charrier I, Mathevon N, Jouventin P. 2003. Vocal signature recognition of mother by fur seal pups. Animal Behaviour 65: 543–550. Falls JB. 1982. Individual recognition by sounds in birds. In: Kroodsma DE, Miller EH, eds. Acoustic communication in birds, Vol. 2. New York: Academic Press, 237–278. Ferreira G, Terrazas A, Poindron P, Nowak R, Orgeur P, Levy F. 2000. Learning of olfactory cues is not necessary for early lamb recognition by the mother. Physiology and Behaviour 69: 405–412. Georges J-Y, Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam island. Ecology 81: 295–308. Georges J-Y, Sevot X, Guinet C. 1999. Fostering in a subantarctic fur seal. Mammalia 63: 384–388.

© 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 305–312

312

I. CHARRIER ET AL.

Godard R. 1991. Long-term memory of individual neighbours in a migratory songbird. Nature 350: 228–229. Gould E. 1983. Mechanisms of mammalian auditory communication. Advances in the Study of Mammalian Behaviour 7: 265–342. Gubernick DJ. 1980. Maternal ‘imprinting’ or maternal ‘labelling’ in goats? Animal Behaviour 28: 124–129. Gubernick DJ, Jones KC, Klopfer PH. 1979. Maternal ‘imprinting’ in goats. Animal Behaviour 27: 314–315. Guinet C, Georges J-Y. 2000. Growth in pups of the subantarctic fur seal (A. tropicalis) on Amsterdam Island. Journal of Zoology, London 251: 289–296. Insley SJ. 2000. Long term vocal recognition in the northern fur seal. Nature 406: 404–405. Insley SJ. 2001. Mother-offspring vocal recognition in northern fur seals is mutual but asymmetrical. Animal Behaviour 61: 129–137. Johnston D. 1996. Cool edit. Phoenix, AZ. Syntrillium Software. Jones IL, Falls JB, Gaston AJ. 1987. Vocal recognition between parents and young of ancient murrelets, Synthliboramphus antiquus (Aves: Alcidae). Animal Behaviour 35: 1405–1415. Jorgensen DD, French JA. 1998. Individuality but not stability in marmoset long calls. Ethology 104: 729–742. Klopfer PH. 1971. Mother love: what turns it on? American Scientist 59: 404–407. Klopfer PH, Adams DK, Klopfer MS. 1964. Maternal ‘imprinting’ in goats. Proceedings of the National Academy of Sciences, USA 52: 911–914. Lawson JW, Renouf D. 1987. Bonding and weaning in harbor seals, Phoca vitulina. Journal of Mammalogy 68: 445– 449. Lorenz C. 1937. The companion in the bird’s world. Auk 54: 245–273. Maestripieri D. 2001. Is there mother-infant bonding in primates? Developmental Review 21: 93–120. McComb K, Moss C, Sayailel S, Baker L. 2000. Unusually extensive networks of vocal recognition in African elephants. Animal Behaviour 59: 716–723. McGregor PK, Avery MI. 1986. The unsung songs of great tits (Parus major): learning neighbours’ songs for discrimination. Behavioral Ecology and Sociobiology 18: 311–316. Mountjoy DJ, Lemon RE. 1995. Extended song learning in wild European starlings. Animal Behaviour 49: 357–366. Nowak R. 1989. Early recognition of the mother by the newborn lamb: effect of breed and litter size. Unpublished PhD Thesis, University of Western Australia.

Paulian P. 1964. Contribution à l’étude de l’otarie de l’île d’Amsterdam. Mammalia 28: 1–146. Peterson RS. 1968. Social behaviour in pinnipeds. In: Harrison RJ, Hubbard RC, Peterson RS, Rice CE, Schusterman RJ, eds. The behaviour and physiology of pinnipeds. New York: Appelton Century-Crofts, 3–53. Peterson RS, Bartholomew GA. 1969. Airborne vocal communication in the california sea lion, Zalophus californianus. Animal Behaviour 17: 17–24. Porter RH, Lévy F, Poindron P, Litterio M, Schaal B, Beyer C. 1991. Individual olfactory signatures as major determinants of early maternal discrimination in sheep. Development and Psychobiology 24: 151–158. Rand RW. 1955. Reproduction in Cape Fur seal, Arctocephalus pusillus. Proceedings of the Zoological Society, London 124: 717–740. Shettleworth SJ. 1998. Cognition, evolution, behaviour. Oxford: Oxford University Press. Shillito E, Alexander G. 1975. Mutual recognition amongst ewes and lambs of four breeds of sheep (Ovis aries). Applied Animal Ethology 1: 151–165. Shillito-Walser E, Alexander G. 1980. Mutual recognition between ewes and lambs. Reproduction, Nutrition and Development 20: 807–816. Smith FV. 1965. Instinct and learning in the attachment of lamb and ewe. Animal Behaviour 13: 84–86. Sokal RR, Rohlf FJ. 1995. Biometry. New York: Freeman. Stirling I. 1971. Studies on the behaviour of the south Australian fur seal, Arctocephalus forsteri. Australian Journal of Zoology 19: 246–267. Stirling I. 1975. Adoptive suckling in pinnipeds. Journal of the Australian Mammal Society 1: 389–391. Sucklin W. 1972. Imprinting and early learning. London: Methuen. Terrazas A, Ferreira G, Lévy F, Nowak R, Serafin N, Orgeur P, Soto R, Poindron P. 1999. Do ewes recognize their lambs within the first day postpartum without the help of olfactory cues? Behavioural Processes 47: 19–29. Trillmich F. 1981. Mutual mother-pup recognition in Galapagos fur seals and sea lions: cues used and functional significance. Behaviour 78: 21–42. Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B, ed. Sexual selection and descent of man. Chicago: Aldine, 136–179. Wartzok D, Ketten DR. 1999. Marine mammals sensory systems. In: Reynolds III JR, Rommel SA, eds. Biology of marine mammals. Washington & London: Smithsonian Institution Press, 117–175.

© 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 305–312

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