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A demonstration of the ability of the harbour seal PhocaVitulina (L.) to discriminate among pup vocalizations
41
J. Exp. Mar. Biol. Ecol., 1985, Vol. 87, pp. 41-46
Elsevier
JEM 440
A DEMONSTRATION
OF THE ABILITY OF THE HARBOUR SEAL PHOCA
VZTULZNA (L.) TO DISCRIMINATE
AMONG PUP VOCALIZATIONS’
DEANE RENOUF Department of Psychology and Marine Sciences Research Laboratory, Memorial University of Newfoundland, St. John’s, Newfoundland, Canada Al C 3X9
(Received 17 September 1984; revision received 28 December 1984; accepted 3 January 1985)
Abstract: A captive adult harbour seal demonstrated that it could distinguish between vocalizations recorded from different pups. This supports the implication of an earlier study which showed that the pup’s call is individually characteristic and might therefore provide one means by which the mother could recognize her offspring and monitor its location. This remote monitoring would be especially important when the pair are in the water where the risk of separation is high. Key words: seal; pup; vocalization; discrimination; Phoca vitulina
INTRODUCTION
Harbour seals Phoca vitdina (L.) give birth to unusually precocial young. In some regions of their habitat, the pups are born on sand exposed at ebb tide, and go to sea with their mothers a few hours later when the rising tide floods their birth site. There are instances in which a pup is forced to swim within minutes of being born, having been flushed into the water by tourists (Lawson & Renouf, 1985). Throughout the nursing season, the pup follows its mother on daily excursions to the sea. This is not the case with most pinnipeds whose offspring normally stay ashore until weaned, and if the mother goes to sea, she does so by herself. The harbour seal mother and pup face various difficulties keeping contact at sea such as poor visibility in the turbid water typical of their vernal pupping habitat, strong currents in the immediate vicinity of their hauling grounds, and relatively loud ambient noise (Renouf, 1980). In earlier work with a breeding population of harbour seals on the French island of Miquelon, we discovered that one of the ways in which the pair maintains contact is through an imprinting-like mechanism evident shortly after the birth of the pup which results in the youngster following its mother’s movements. This makes it appear as if the pup were entirely responsible for ensuring that it does not become separated from its mother. Her overriding control becomes obvious, however, ’ Marine Sciences Research Laboratory Contribution No. 545. 0022-0981/85/$03.30 0 1985 Elsevier Science Publishers B.V. (Biomedical Division)
42
DEANERENOUF
when the pair are in serious danger of being separated, as in the event of a human disturbance (Renoufet al., 1983). In this ease the mother becomes vigilant of her pup, making sure that it stays close by_ One of the ways the female might monitor the following response of her pup is through the latter’s calling. The pup vocalizes almost constantly, especially when it is in the water swimming behind its mother. Since this vocalization disappears from the animal’s repertoire shortly after weaning, it may serve some function in the nurturant relationship. The calls range in duration from 50 to 750 ms, and a pup might emit a series of them separated by as little as 500 ms, or as a single bleat. The cry is of relatively low frequency, most harmonics being below 4000 Hz. Detailed sonagraphic analyses of the calls revealed that they mer among pups in fundamental frequency and harmonic distribution (Renouf, 1984). The fact that the calls are individually distinct with respect to certain physical parameters suggests that the mother may be able to recognize the call of her own pup. The existence of these physical differences, however, does not necessarily mean that the seal can perceive them. The female’s ability to recognize the vocalization of her offspring has been suggested for grey seals, Walichoerus grypus, (Fogden, 1971) and elephant seals, Mrounga angustirostis, (Klopfer & Gilbert, 1966) and discounted in harp seals, ~~go~h~i~ g~~~~a~dic~, (Terhune et al., 1979). The only direct investigation of this hypothesis was u~de~~~n with elephant seals by Petrinovich (1974) who used playback techniques to show that females emit the pup attraction call in response to tape recordings of their own pups, significantly more often than to those of alien young. Although this method has been used effectively to demonstrate call recognition in various species of animals (Espmark, 1971; Petrinovich & Peeke, 1973; T~llmich, 1981), it proved to be ~appropriate for harbour seals. It was virtually impossible to position equipment close enough to the animals in the field. Unlike the elephant seal which stays on the beach for the duration of the nursing period (LeBoeuf et al., 1972), harbour seals are extremely wary and flush to the water with the slightest disturbance. But even if it were possible to locate speakers effectively, the mother does not make a clear response to her pup’s call. When the pair are in water and the pup begins to cry, the female is more IikeIy to reduce the distance separating her from her youngster, than to maintain or increase this distance. When they are on the beach together the mother, however, makes no obvious response to the cry (Renouf, 1984). For this reason I used the only adult female in our colony of captive ha&our seals to test the hypothesis that the seal can discriminate among pup vocalizations.
MATERIALANDMETHODS
The subject was a 7-yr-old female harbour seal which had been living in captivity since it was captured as a weaned pup on Sable Island, Nova Scotia, It was maintained on a diet of herring and vitamins (Geraci, 1975).
HARBOUR SEAL PUP CALL DISCRIMINATION
43
The pup vocalizations were broadcast over one Realistic 40-1009 50-W speaker which had a flat frequency response between 50 and 5000 Hz. Pup vocalizations collected during the breeding season at Miquelon (Renouf, 1984) were played on a Sony Model TCD5 stereo cassette recorder, the same device which had been used to record the calls. The cassette output was amplified by a 50-W per channel SanKen Sl-1050G stereo amplifier. The playback intensity of the calls was measured with a General Radio model 1551C precision sound level meter. Since ambient noise in the outdoor facility was quite high, the calls were broadcast at 94 dB re:20 PPa (20-kHz filter) at 50 cm. During training sessions the seal was required to discriminate between the vocalization of two different pups, each repeated at l-s intervals on a separate channel of a continuous loop cassette tape. On any trial, either the first or the second channel was switched to the speaker. Two feeder boxes, each measuring 10 x 10 x 15 cm, were mounted one over the other on the edge of a 75 x 35 cm platform suspended 20 cm from the water surface. Small pieces of herring could be placed in the back of a feeder box behind a clear Plexiglas sliding door so that the seal could not get access to the herring until the experimenter moved this door aside. The speaker was positioned directly under the feeder boxes. The seal was trained using standard shaping techniques to haul out on the platform and extract pieces of herring from the feeder boxes. Once familiar with the way in which food was to be dispensed throughout the study, the seal was trained to open one feeder after hearing one pup vocalization, and to use the second feeder if the other call were broadcast. On each trial, the animal was not permitted to open a feeder until the call used on that trial was played twice. If the appropriate feeder were chosen, the seal was given access to the herring positioned behind the Plexiglas door at the back of the box. If the incorrect feeder were opened, this door remained closed so that the seal could not reach the herring. The seal was trained to perform three different discriminations. The first was between calls A and B, the second between calls C and D and the third between calls E and F, as shown in Fig. 1. On each trial, a call was repeated at l-s intervals until the seal chose one of the two feeders. Twenty trials were administered in each training session, with each call being presented on half of the trials, in randomized order. When the seal could make the correct response on 80% of the twenty trials in a session for three consecutive days, the discrimination was considered learned.
RESULTS
The seal was able to discriminate between calIs A and B, C and D, and E and F. The animal took 21 training sessions to reach criterion in the first instance, 6 sessions in the second and 10 in the third (Fig. 2).
4
Fig. 1. Calls
a
A and If presented in the first discrimination (a), calls C and D presented in the second discrimination (b), and calls E and F presented in the third discrimination (c).
DISCUSSION 'I%ofact that there are physical distinctions among the calls af difkrent pups does not in itselfdemonstrate that the seals can detect that the vocalizations differ. Since the animal in the present study, however, showed no difficulty in learning to discriminate in three different cases between calls from di&z-ent pups, at Ieast some voices are
45
HARBOUR SEAL PUP CALL DISCRIMINATION looFlRS
DlSCRlMiNATlON
T
*
so.
.
.
. .
80-
./\
.
.
. .
70-
. .
.
.
.
.
.
.
60.
* 50-P
100-w THIRD
DISCRIMINATION
so-
80-
l
l -.-.
l
. 70-
l
.
l
.
60-
SESSION
NUMBER
Fig. 2. The seal’s learning curves for the first (cab A vs. B), second (calls C vs. D), and third (calls E vs. F) discriminations.
individually distinct to the adult seal. If this is true, then it seems reasonable to suggest that the mother can tell the cry of her own offspring from that of others. Even if this were not always the case, if for example, there were some pups whose voices were not suffkiently different to be recognized as such, the fact that the pup is predisposed to stay close to its mother helps to reduce the likelihood that pups with similar calls would be vocalizing from the same location.
46
DEANE RENOUF
The mother does not appear to rely fully upon her offspring’s following tendency, since she makes sure that the pup stays close by when there is any serious threat to their security. She is less vigilant when the two are on the beach where the pup is far less mobile. Once in water, however, the probability of separation is increased by the pup’s enhanced mobility in often treacherous water in which visual cues are limited and ambient noise could be problematical. Calculations using the 25-dB critical ratio of harbour seals, a 70-dB pup call and noise levels of 25 dB (spectrum) indicated that the mother should not be able to hear her pup’s cry once the pair are separated by more than 8 m (Renouf, 1980); the pup’s following tendency ensures that the two are always closer to one another than this. In water, the pup becomes more vocal as it swims behind its mother. Since the call is propagated simultaneously in air and underwater (Renouf, 1984) the mother could effectively monitor the pup’s position from moment to moment without having to turn around to ascertain if her own offspring is following as it should.
REFERENCES ESPMARK,Y., 1971. Individual recognition by voice in reindeer mother-young relationship. Field observation and playback experiments. Behaviour, Vol. 40, pp. 295-301. FOGDEN, S., 1971. Mother young behaviour at grey seal breeding beaches. J. Zool., Vol. 164, pp. 61-92. GERACI, J., 1975. Pinmped nutrition. Rapp. P.-V. R&n. Cons. Int. Explor. Mer, Vol. 169, pp. 3 12-323. KLOPFER, P. & B. GILBERT, 1966. A note on retrieval and recognition of young in the elephant seal, Mirounga angustirostris. Z. Tierpsychol., Vol. 23, pp. 757-760. LAWSON,J. & D. RENOUF, 1985. Parturition in the Atlantic harbour seal. J. Mammalogy, in press. LEBOEUF, B., R. WHITING& R. GANT~, 1972. Perinatal behavior of northern elephant seal females and their young. Behaviour, Vol. 43, pp. 121-156. PETRINOVICH,L., 1974. Individual recognition of pup vocalizations by northern elephant seal mothers. Z. Tierpsychol., Vol. 34, pp. 308-312. PETRINOVICH,L. & H. PEEKE, 1973. Habituation to territorial song in the white-crowned sparrow (Zonotrichia leucophyrs). Behav. Biol., Vol. 8, pp. 743-748. RENOUF, D., 1980. Masked auditory thresholds in harbour seals. J. And. Res., Vol. 20, pp. 263-269. RENOUF,D., 1984. The vocalization of the harbour seal pup, and its role in the maintenance of contact with the mother. J. Zool., Vol. 202, pp. 583-590. RENOUF,D., J. LAWSON& L. GABORKO,1983. Attachment between harbour seal (Phoca vitulina)mothers and pups. J. Zool., Vol. 199, pp. 179-187. TERHUNE,J., M. TERHUNE& K. RONALD,1979. Location and recognition of pups by adult female harp seals. Appl. Anim. Ethol., Vol. 5, pp. 375-380. TRILLMICH,F., 1981. Mutual mother-pup recognition in Galapagos fur seals and sea lions: cues used and functional significance. Behaviour, Vol. 78, pp. 21-42.
J. Exp. Mar. Biol. Ecol., 1985, Vol. 87, pp. 41-46
Elsevier
JEM 440
A DEMONSTRATION
OF THE ABILITY OF THE HARBOUR SEAL PHOCA
VZTULZNA (L.) TO DISCRIMINATE
AMONG PUP VOCALIZATIONS’
DEANE RENOUF Department of Psychology and Marine Sciences Research Laboratory, Memorial University of Newfoundland, St. John’s, Newfoundland, Canada Al C 3X9
(Received 17 September 1984; revision received 28 December 1984; accepted 3 January 1985)
Abstract: A captive adult harbour seal demonstrated that it could distinguish between vocalizations recorded from different pups. This supports the implication of an earlier study which showed that the pup’s call is individually characteristic and might therefore provide one means by which the mother could recognize her offspring and monitor its location. This remote monitoring would be especially important when the pair are in the water where the risk of separation is high. Key words: seal; pup; vocalization; discrimination; Phoca vitulina
INTRODUCTION
Harbour seals Phoca vitdina (L.) give birth to unusually precocial young. In some regions of their habitat, the pups are born on sand exposed at ebb tide, and go to sea with their mothers a few hours later when the rising tide floods their birth site. There are instances in which a pup is forced to swim within minutes of being born, having been flushed into the water by tourists (Lawson & Renouf, 1985). Throughout the nursing season, the pup follows its mother on daily excursions to the sea. This is not the case with most pinnipeds whose offspring normally stay ashore until weaned, and if the mother goes to sea, she does so by herself. The harbour seal mother and pup face various difficulties keeping contact at sea such as poor visibility in the turbid water typical of their vernal pupping habitat, strong currents in the immediate vicinity of their hauling grounds, and relatively loud ambient noise (Renouf, 1980). In earlier work with a breeding population of harbour seals on the French island of Miquelon, we discovered that one of the ways in which the pair maintains contact is through an imprinting-like mechanism evident shortly after the birth of the pup which results in the youngster following its mother’s movements. This makes it appear as if the pup were entirely responsible for ensuring that it does not become separated from its mother. Her overriding control becomes obvious, however, ’ Marine Sciences Research Laboratory Contribution No. 545. 0022-0981/85/$03.30 0 1985 Elsevier Science Publishers B.V. (Biomedical Division)
42
DEANERENOUF
when the pair are in serious danger of being separated, as in the event of a human disturbance (Renoufet al., 1983). In this ease the mother becomes vigilant of her pup, making sure that it stays close by_ One of the ways the female might monitor the following response of her pup is through the latter’s calling. The pup vocalizes almost constantly, especially when it is in the water swimming behind its mother. Since this vocalization disappears from the animal’s repertoire shortly after weaning, it may serve some function in the nurturant relationship. The calls range in duration from 50 to 750 ms, and a pup might emit a series of them separated by as little as 500 ms, or as a single bleat. The cry is of relatively low frequency, most harmonics being below 4000 Hz. Detailed sonagraphic analyses of the calls revealed that they mer among pups in fundamental frequency and harmonic distribution (Renouf, 1984). The fact that the calls are individually distinct with respect to certain physical parameters suggests that the mother may be able to recognize the call of her own pup. The existence of these physical differences, however, does not necessarily mean that the seal can perceive them. The female’s ability to recognize the vocalization of her offspring has been suggested for grey seals, Walichoerus grypus, (Fogden, 1971) and elephant seals, Mrounga angustirostis, (Klopfer & Gilbert, 1966) and discounted in harp seals, ~~go~h~i~ g~~~~a~dic~, (Terhune et al., 1979). The only direct investigation of this hypothesis was u~de~~~n with elephant seals by Petrinovich (1974) who used playback techniques to show that females emit the pup attraction call in response to tape recordings of their own pups, significantly more often than to those of alien young. Although this method has been used effectively to demonstrate call recognition in various species of animals (Espmark, 1971; Petrinovich & Peeke, 1973; T~llmich, 1981), it proved to be ~appropriate for harbour seals. It was virtually impossible to position equipment close enough to the animals in the field. Unlike the elephant seal which stays on the beach for the duration of the nursing period (LeBoeuf et al., 1972), harbour seals are extremely wary and flush to the water with the slightest disturbance. But even if it were possible to locate speakers effectively, the mother does not make a clear response to her pup’s call. When the pair are in water and the pup begins to cry, the female is more IikeIy to reduce the distance separating her from her youngster, than to maintain or increase this distance. When they are on the beach together the mother, however, makes no obvious response to the cry (Renouf, 1984). For this reason I used the only adult female in our colony of captive ha&our seals to test the hypothesis that the seal can discriminate among pup vocalizations.
MATERIALANDMETHODS
The subject was a 7-yr-old female harbour seal which had been living in captivity since it was captured as a weaned pup on Sable Island, Nova Scotia, It was maintained on a diet of herring and vitamins (Geraci, 1975).
HARBOUR SEAL PUP CALL DISCRIMINATION
43
The pup vocalizations were broadcast over one Realistic 40-1009 50-W speaker which had a flat frequency response between 50 and 5000 Hz. Pup vocalizations collected during the breeding season at Miquelon (Renouf, 1984) were played on a Sony Model TCD5 stereo cassette recorder, the same device which had been used to record the calls. The cassette output was amplified by a 50-W per channel SanKen Sl-1050G stereo amplifier. The playback intensity of the calls was measured with a General Radio model 1551C precision sound level meter. Since ambient noise in the outdoor facility was quite high, the calls were broadcast at 94 dB re:20 PPa (20-kHz filter) at 50 cm. During training sessions the seal was required to discriminate between the vocalization of two different pups, each repeated at l-s intervals on a separate channel of a continuous loop cassette tape. On any trial, either the first or the second channel was switched to the speaker. Two feeder boxes, each measuring 10 x 10 x 15 cm, were mounted one over the other on the edge of a 75 x 35 cm platform suspended 20 cm from the water surface. Small pieces of herring could be placed in the back of a feeder box behind a clear Plexiglas sliding door so that the seal could not get access to the herring until the experimenter moved this door aside. The speaker was positioned directly under the feeder boxes. The seal was trained using standard shaping techniques to haul out on the platform and extract pieces of herring from the feeder boxes. Once familiar with the way in which food was to be dispensed throughout the study, the seal was trained to open one feeder after hearing one pup vocalization, and to use the second feeder if the other call were broadcast. On each trial, the animal was not permitted to open a feeder until the call used on that trial was played twice. If the appropriate feeder were chosen, the seal was given access to the herring positioned behind the Plexiglas door at the back of the box. If the incorrect feeder were opened, this door remained closed so that the seal could not reach the herring. The seal was trained to perform three different discriminations. The first was between calls A and B, the second between calls C and D and the third between calls E and F, as shown in Fig. 1. On each trial, a call was repeated at l-s intervals until the seal chose one of the two feeders. Twenty trials were administered in each training session, with each call being presented on half of the trials, in randomized order. When the seal could make the correct response on 80% of the twenty trials in a session for three consecutive days, the discrimination was considered learned.
RESULTS
The seal was able to discriminate between calIs A and B, C and D, and E and F. The animal took 21 training sessions to reach criterion in the first instance, 6 sessions in the second and 10 in the third (Fig. 2).
4
Fig. 1. Calls
a
A and If presented in the first discrimination (a), calls C and D presented in the second discrimination (b), and calls E and F presented in the third discrimination (c).
DISCUSSION 'I%ofact that there are physical distinctions among the calls af difkrent pups does not in itselfdemonstrate that the seals can detect that the vocalizations differ. Since the animal in the present study, however, showed no difficulty in learning to discriminate in three different cases between calls from di&z-ent pups, at Ieast some voices are
45
HARBOUR SEAL PUP CALL DISCRIMINATION looFlRS
DlSCRlMiNATlON
T
*
so.
.
.
. .
80-
./\
.
.
. .
70-
. .
.
.
.
.
.
.
60.
* 50-P
100-w THIRD
DISCRIMINATION
so-
80-
l
l -.-.
l
. 70-
l
.
l
.
60-
SESSION
NUMBER
Fig. 2. The seal’s learning curves for the first (cab A vs. B), second (calls C vs. D), and third (calls E vs. F) discriminations.
individually distinct to the adult seal. If this is true, then it seems reasonable to suggest that the mother can tell the cry of her own offspring from that of others. Even if this were not always the case, if for example, there were some pups whose voices were not suffkiently different to be recognized as such, the fact that the pup is predisposed to stay close to its mother helps to reduce the likelihood that pups with similar calls would be vocalizing from the same location.
46
DEANE RENOUF
The mother does not appear to rely fully upon her offspring’s following tendency, since she makes sure that the pup stays close by when there is any serious threat to their security. She is less vigilant when the two are on the beach where the pup is far less mobile. Once in water, however, the probability of separation is increased by the pup’s enhanced mobility in often treacherous water in which visual cues are limited and ambient noise could be problematical. Calculations using the 25-dB critical ratio of harbour seals, a 70-dB pup call and noise levels of 25 dB (spectrum) indicated that the mother should not be able to hear her pup’s cry once the pair are separated by more than 8 m (Renouf, 1980); the pup’s following tendency ensures that the two are always closer to one another than this. In water, the pup becomes more vocal as it swims behind its mother. Since the call is propagated simultaneously in air and underwater (Renouf, 1984) the mother could effectively monitor the pup’s position from moment to moment without having to turn around to ascertain if her own offspring is following as it should.
REFERENCES ESPMARK,Y., 1971. Individual recognition by voice in reindeer mother-young relationship. Field observation and playback experiments. Behaviour, Vol. 40, pp. 295-301. FOGDEN, S., 1971. Mother young behaviour at grey seal breeding beaches. J. Zool., Vol. 164, pp. 61-92. GERACI, J., 1975. Pinmped nutrition. Rapp. P.-V. R&n. Cons. Int. Explor. Mer, Vol. 169, pp. 3 12-323. KLOPFER, P. & B. GILBERT, 1966. A note on retrieval and recognition of young in the elephant seal, Mirounga angustirostris. Z. Tierpsychol., Vol. 23, pp. 757-760. LAWSON,J. & D. RENOUF, 1985. Parturition in the Atlantic harbour seal. J. Mammalogy, in press. LEBOEUF, B., R. WHITING& R. GANT~, 1972. Perinatal behavior of northern elephant seal females and their young. Behaviour, Vol. 43, pp. 121-156. PETRINOVICH,L., 1974. Individual recognition of pup vocalizations by northern elephant seal mothers. Z. Tierpsychol., Vol. 34, pp. 308-312. PETRINOVICH,L. & H. PEEKE, 1973. Habituation to territorial song in the white-crowned sparrow (Zonotrichia leucophyrs). Behav. Biol., Vol. 8, pp. 743-748. RENOUF, D., 1980. Masked auditory thresholds in harbour seals. J. And. Res., Vol. 20, pp. 263-269. RENOUF,D., 1984. The vocalization of the harbour seal pup, and its role in the maintenance of contact with the mother. J. Zool., Vol. 202, pp. 583-590. RENOUF,D., J. LAWSON& L. GABORKO,1983. Attachment between harbour seal (Phoca vitulina)mothers and pups. J. Zool., Vol. 199, pp. 179-187. TERHUNE,J., M. TERHUNE& K. RONALD,1979. Location and recognition of pups by adult female harp seals. Appl. Anim. Ethol., Vol. 5, pp. 375-380. TRILLMICH,F., 1981. Mutual mother-pup recognition in Galapagos fur seals and sea lions: cues used and functional significance. Behaviour, Vol. 78, pp. 21-42.