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Prenatal experience of parental calls and pecking in the laughing gull (Larus atricilla L.)
Anita. Behav., 1970, 19, 475-480
PRENATAL EXPERIENCE OF PARENTAL CALLS AND PECKING IN THE LAUGHING GULL (LARUSATRICILLA L.) BY MONICA IMPEKOVEN
Institute of Animal Behavior, Rutgers University, Newark, New Jersey, U.S.A. Abstract. Laughing gulls emit a call referred to as 'crooning' with increasing frequency shortly before the hatching of their young. Uttered to newly hatched chicks this call appears to enhance pecking for food. The adult birds 'kow' call in response to disturbances near the nest. Incubator raised chicks respond differentially to these two calls, both pre- and post-natally. An experiment was designed to discover whether the hearing of such vocalizations prenatally would have any bearing on their postnatal effectiveness in eliciting pecking. With respect to 'crooning' an effect was found but it would not be clearly demonstrated that 'crooning' heard prenatally enhances pecking. Chicks pecked less often when hearing 'kow' calls regardless of prenatal experience with this call. Visual stimuli eliciting pecking in gulls have been studied extensively (e.g. Hailman 1967) but auditory aspects of the stimulus situation have received little attention. The adult laughing gull utters a smooth, long-drawn, low-pitched call referred to as 'crooning' or 'mew' call (Fig. 1) with increasing frequency shortly before the hatching of its young. Under the same labels functionally and structurally similar calls have been described for other gull species (reviewed by Evans 1970). Mate reliefs for incubation become more frequent as hatching approaches and the oncoming mate 'croons' besides giving other types of calls (according to my impressions on several nests): Also when alone the incubating bird may give a shorter version of this call after rising and before resettling or even while sitting on its pipping eggs (Impekoven, in preparation). After hatching, some parents 'croon' in the context of feeding the young. On the first and second day after hatching the chicks usually do not locomote but snuggle or sit nestled against the parent's plumage. Before feeding, the parent adopts a stooping posture so that its beak is presented directly in front of the chicks' eyes. According to Beer (1970) and personal observations, the adult then 'croons! if the chicks do not peck immediately. At the beginning of a feeding sequence the call may stimulate the chicks to peck at the parent's bill which in turn seems to promote regurgitation of food by the parent. At the end of the sequence the parent may 'croon' again if the chicks have not eaten all the food presented to them. Chicks of a clutch of eggs may hatch on successive days, thus late comers are exposed to 'crooning' uttered during such feedings whilst still in the egg.
From the 2nd day on when the young become more mobile, 'crooning' may function to attract them to the source of food from a distance also (Beer 1970).
Experiment 1 An experiment was designed to discover whether 'crooning' enhances pecking in incubator hatched chicks and whether the fact that the chicks hear this call prior to hatching has any bearing on the call's postnatal effectiveness. Effects of prenatal auditory experience on approach and following have been demonstrated in young guillemots (Tschanz 1968), domestic chicks (Grier, Counter & Shearer 1967) and ducklings (Gottlieb 1971) but the pecking response was not investigated quantitatively in these studies. Methods Approximately seventy gull chicks were tested in the Department of Zoology, University of Maryland and in the field-station of the Institute of Animal Behavior, situated near a large laughing gull colony in the Brigantine National Wildlife refuge, New Jersey. Subjects, Eggs collected from the gullery were hatched communally in an incubator at approximately 38 ~ to 39-4~ and around 70 per cent R.H. They were turned four to eight times per day till they started to pip. Such eggs were taken at various stages of the incubation cycle up to 3 days before hatching, thus some of them probably had some experience of adult gulls' calls prior to my treatments, others not. It is known that chick embryos respond to auditory stimuli electrophysiologically as early as 7 to 8 days before hatching (Vanzulli & Garcia- Austt 1963) 475
476
ANIMAL
BEHAVIOUR,
and behaviourally as early as 3 to 4 days (Sedlacek 1964). The incubation period of chickens is approximately 21 days, that of laughing gulls 23 days. Apparatus. Calls were recorded from nest-sites of gulls with 0 to 2 day old chicks by means of a Uher-4000-L Report tape-recorder and an omnidirectional microphone (M515). The same tape-recorder was used for playing calls to pipping eggs and incubator hatched chicks. Sound level measurements were made on scale B of a calibrated General Radio soundlevel meter. Eggs were hatched in a force-draft 'Gooser' (Humidaire Co.) or a still-air kerosene incubator (make unknown). The above mentioned incubation temperature refers to the latter. Procedure. A few days before hatching, a starshaped crack appears near the pole of the large blunt end of the shell. This was thought of as being the first stage of pipping and thus was referred to as P1. Yet recent investigations showed that this crack is produced by the rightlifting movements of head and beak during tucking (Oppenheim, personal communication). In the second stage (P2) cracks become visible over an enlarged area. In the third stage (P3) a small hole appears. This pipping hole is enlarged and after it reaches a certain size the actual hatching process starts. In field-observations using microphones placed in nests, calls from the egg did not become audible until late P2 which corresponds with the time when the bill penetrates into the air-space (Oppenheim, personal communication and own observation). Often in response to these calls the parent may call during late P2 and more so during P3 (Impekoven, in preparation). Accordingly one group containing 28 eggs was repeatedly exposed to 'crooning' during the P3-stage till they began to hatch. 'Crooning was played at 76 to 84 db measured near the egg, with a background noiselevel of 50 db or less. Each egg was exposed to the sound individually; it was taken from the incubator, carried to another room where 'crooning' calls were played to it in four bursts of 15-s duration separated by 15-s periods of no sound. The recording consisted of a natural sequence of nine 'croons' of a parent gull towards its day-old chick. The sequence contained only one chick-call. The median interval between 'croons' was 0.7 s. This treatment was repeated every 13 or 2 hr except for an interval of several hours over night. It was given between one and eight times depending
19,
3
on how fast pipping proceeded which was very variable from egg to egg. This treatment differs from the situation in the wild where the incubating bird may call only once or twice in close succession but does so quite frequently. Intervals between nest-reliefs and the number of 'croons' given by the oncoming mate are very variable. Another group of twenty-one eggs was not exposed to 'crooning'. Eight of these eggs were never taken from the incubator; thirteen of them were exposed to 'no sound' for times roughly comparable with those of eggs exposed to 'crooning', in order to control for the possibility that the handling and light-exposure rather than the sound itself would affect the subsequent test-response. The two groups of chicks were tested for pecking between 43 and 12 hr after hatching (i.e. at an age when they stand and peck but when they do not walk). Wild chicks view the parent's dark red beak in a more or less vertical position against the green grass surrounding the nest. Accordingly pecking experiments were carried out in a black box with a vertical red dowel rod placed in front of a green cloth wall. The rod was kept stationary and its tip at the chick's eye level; from behind the green wall 'crooning' calls were played. These calls were the same as those presented in the prenatal exposures except for the intensity near the chick which now was 84 to 90 db. Each chick was tested first for 89min with two 15-s sequences of sound, i.e. eighteen calls and then 3 rain with no sound or vice versa. The two tests were separated from one another by 3 rain or 13 min during which periods the chick was kept under a translucent container in front of the pecking stimulus. Recorded were the number of pecks directed at the red stimulus rod during the sound and no sound condition. In order to see whether and in what way the embryos would respond to the calls during the prenatal exposures thirty-eight eggs were observed as soon as the beak was visible through the enlarged pipping hole. Only twenty-nine of these e g g s were retested after hatching, sixteen of the 'crooning' experienced group and thirteen of the 'no sound' experienced group. When the pipping hole is enlarged bill-movements like bill-clapping, yawning, grinding and back-thrusts against the shell can be recognized. I recorded whether such bill-activities occurred during the 15-s sound and no sound periods in the 'crooning' exposed birds and comparable 15-s no sound periods in birds not exposed to 'crooning'.
IMPEKOVEN: PRENATAL EXPERIENCE IN LAUGHING GULL CHICKS
477
Table I. Chicks: Median Number of Peeks Towards a Red Stimulus Rod
Test-condition No.
Sound
No sound 4"5 10
14.5 16
<0.01 NS
7 13
9 17
<0.05 <0.001
'Crooning' Prenatal condition*
Sound No sound
28 21
10 6
'Kow' Prenatal conditiont
Sound No Sound
12 12
2 4
Total
P
*Difference between prenatally sound and no-sound experienced chicks P<0.01 tDifference between prenatally 'crooning' experienced and 'kow' experienced chicks P<0-002 Results
Experiment 2
'Crooning' experienced chicks pecked more often when hearing the sound than when not. 'No sound' experienced chicks tended to peck more in the no sound than in the sound condition (Table I). The total pecking scores were not different under the two treatments. The relative pecking scores of the 'no sound' experienced chicks under the two testing conditions were the same regardless of whether the eggs were taken from the incubator or not. The total pecking scores were higher in the thirteen 'exposed' chicks than in the eight 'unexposed' ones suggesting that the prenatal handling and or light exposure affected the activity level after hatching. Similarly 'crooning' exposed embryos showed a higher number of 15-s activity periods in the sound than in the no sound situation but the total number of such periods was not higher than that of 'no sound' experienced birds (Table II). Table II. Embryos: Median Number of 15-s Bill-Activity Periods per Minute Exposure
No.
Exposure Sound No sound Total
P
'Crooning'
19
1.3
0.5
1.8
<0.01
'Kow'
17
0.6
0.75
1.35
iS
19
No sound 1.0
1.0
2.0
'No sound'
Statistical tests: Wilcoxon two-tailed for comparison between different test-conditions, Mann-Whitney U two-tailed for comparison between groups with different prenatal experience.
From the result of the first experiment the question arose whether the described effect of 'crooning' was stimulus specific or not. I approached this problem by comparing some of the 'crooning' experienced birds with others raised and tested with 'kow' calls. 'Kow' calls differ from 'crooning' in their sudden onset, shorter duration, higher pitch and harshness (Fig. 1). Single birds 'kow' call at the nest-site in response to minor disturbances of various kinds, and many b i r d s 'kow' call in flight in response to ground predators during incubation and hatching. Functionally this call could be described as an 'alarm' call. Methods
The methods were essentially the same as the ones used in the first experiment. In temporal alternation with some of the eggs exposed to 'crooning' or 'no sound', seventeen other eggs were exposed to 'kow' calls, made by a single bird played at similar intensity levels as 'crooning' and with a comparable number of exposures during the P3-stage. The training tape consisted of three natural sequences of six 'kows' each, the test tape of six such sequences. The median interval between such calls was 0.5 s. Twelve of these chicks were tested for pecking after hatching. Another group of twelve chicks was not exposed to 'kow' calls during pipping but was tested in the pecking situation after hatching. These chicks had been tested with 'crooning' before, which may have affected the performance in the subsequent 'kow' test. Seventeen eggs were observed during the prenatal exposures to 'kow' calls.
478
ANIMAL
BEHAVIOUR,
19,
3
7 CROON
6 5 4 ~3 N
--r-2.
~O-
r
r
T
Z
U.I
~6u-5
4.
:3 2
0"~ TIME (SEC) i
1"5
Fig. 1. Spectrograms of 'crooning' and 'kow' call made on a Kay Electric Co. Sonagraph with a narrow band filter. (Both are sections from the tape used in the experiments;)
Results
Despite this prenatal experience such chicks pecked more in the no sound than in the sound condition (Table I). The relative scores hardly differed from those of 'no sound' experienced birds though the total pecking scores were much lower. Their total pecking scores were also lower than those of 'crooning' experienced chicks, but the difference is not statistically significant. Moreover observations of their bill-movements during the P3-stage showed that the embryos were not more active during the sound than during the no sound condition. Discussion
The results show that prenatal experience of 'crooning' affects the postnatal responsiveness to this call. As to the question whether 'crooning' heard prenatally enhances the pecking response in incubator hatched chicks, the results do not provide a clear-cut answer. In contrast to 'no sound' experienced chicks 'crooning' experienced chicks pecked more often in the sound than in the no sound condition. From this result one would conclude that parental 'crooning' enhances pecking if heard prenatally. However the fact that the
total pecking score of 'crooning' raised chicks was not higher than that of birds without prenatal 'crooning' experience does not support such a conclusion. In the present experiments the chicks were tested between 489 and 12 hr after hatching, before they were ever fed. Even in absence of additional stimulation many chicks readily pecked at the red stimulus rod. This differs from the situation in the wild where calls are emitted when the chicks do not peck immediately and thus are probably not very hungry (see 'Introduction'). It is possible that some of the experimental birds were maximally responsive to the visual stimulus alone. Further experiments will have to show whether more satiated chicks would differ in their absolute peckingrate under the two treatments. Can one conclude that chicks simply peck most in a situation made familiar to them through prenatal exposure: 'crooning' in one case and 'no crooning' in the other? Both groups of embryos experienced 'no sound' during such exposures and during the time they spent in the incubator; thus such an interpetation cannot fully explain the results. The fact that 'no sound' experienced chicks tended to peek less often in the sound con-
IMPEKOVEN: PRENATAL EXPERIENCE IN LAUGHING GULL CHICKS dition than in the no sound condition calls for an explanation. To these chicks 'crooning' was a novel stimulus and thus may have elicited a 'listening' response or 'orienting reflex' which is subject to habituation with repeated presentation of the novel stimulus (Sokolov 1960). Accordingly 'crooning' experienced chicks may have become habituated to the novelty effect of 'crooning' through prenatal exposure to this call. Further research is required to determine the limits of auditory sensitivity in terms of developmental age. More recent data indicate that embryos respond to 'crooning' during the P1 and early P2 stage on days 19 and 20 (Gold & Impekoven, in preparation). Probably postnatal responsiveness to 'crooning' is not only affected by prior exposure to this particular call but to other calls sharing certain characteristics with 'crooning'. Bursts of a variation of short, low pitched sometimes disyllabic notes with smooth onset are given by many birds in association with shifting of the eggs and resettling over much of the incubation time. Similarly, calls accompanying 'choking'-displays after the landing of a mate by the nest with nesting material consist of a rapid sequence of even shorter, low pitched notes. In response to both types of calls embryos in the P3-stage responded similarly though not as strongly as to 'crooning' (Impekoven, in preparation). The effect of exposure to such calls on postnatal responsiveness to 'crooning' has not been tested. In response to 'crooning', pipping embryos showed an increase in the amount of their billmovements. Similar findings were made with respect to ducklings (Gottlieb 1965). The comparison of activity periods in 'crooning' and 'no sound' exposed chicks suggests that 'crooning' in these embryos did not raise the overall readiness for bill-movements but changed the temporal distribution of their occurrences. The measurements for bill-activity in this study were very crude and further tests will have to show whether the actual number and amplitude of bill-movements is also unaffected under the two treatments. Responsiveness to 'crooning' in pipping embryos may be affected by its frequent temporal association with photic and mechanical stimulation which occurs during nest-relief, egg-shifting and resettling and in the experiment by taking the eggs from the incubator, carrying them and returning them to the incubator.
479
Experiment 2 showed that despite prenatal experience with 'kow' calls such birds pecked less often in the sound than in the no sound condition. Actually some of these chicks did not peck at all in response to 'kow' calls but crouched. The results with 'kow' calls suggest that 'Crooning' may have specific features that lead to its particular effect. What these features are (pitch, temporal pattern, smoothness of onset or timbre) remains to be discovered. In contrast to 'crooning', 'kow' calls seem to have characteristics that inhibit pecking despite repeated prenatal exposure to this call. Unlike 'crooning', 'kow' calls may elicit an avoidance response or defensive reaction that interferes with the ongoing behaviour. According to Fischer & Gilman (1969) avoidance responses appear to be caused by a sudden onset of sound which is one of the characteristics of 'kow' calls. The difference in the total pecking score between 'kow' and 'no kow' experienced chicks cannot be interpreted any further at this point since it may merely be due to the fact that 'no kow' experienced chicks were tested with 'crooning' before. Differential responsiveness to the maternal 'feeding' and 'distress' call ('alarm' call?) has also been established for naive red jungle-fowl chicks (Snapp 1969) although the details of that study differ much from the present one.
Acknowledgments I thank Dr W. M. Schleidt and Dr J. P. Hailman for advice and equipment and Dr J. S. Rosenblatt, Dr C. G. Beer and Dr D. S. Lehrman for comments on the manuscript. The cooperation and hospitality of the Brigantine National Wildlife Refuge are greatly acknowledged. This study was supported by Public Health Service Grant GM122774 and GM16727. REFERENCES Beer, C. G. (1970). On the responses of laughing gull chicks to the calls of adults. II. Age changes and responses to differenttypes of calls. Anim. Behav., 18, 661-677. Evans, R. M. (1970). Parental recognition and analysis of the 'mew' call in black-billed gulls (Larus bulleri). The Auk, 87, 503-513. Fischer, G. J. & Gilman, S. A. (1969). Followingduring imprinting as a function of auditory stimulus intensity. Develop. PsychoL, 1, 216-218. Gottlieb, G. (1965). Prenatal auditory sensitivity in chickens and ducks. Science, N.Y., 147, 15961598. Gotflieb, G. (1968). Prenatal behavior of birds. Quart. Rev. BioL, 43, 148-174.
480
ANIMAL
BEHAVIOUR,
Gottlieb, G. (1971). Development o f Species Identification in Birds: An Inquiry into the Prenatal Determinants of Perception. Chicago: University of Chicago Press.
Grier, J. B., Counter, S. A. & Shearer, W. M. (1967). Prenatal auditory imprinting in chickens. Science, N.Y., 155, 1692-1693. Hailman, J. P. (1967). The ontogeny of an instinct. The pecking response in chicks of the laughing gull and related species. Behaviour, Suppl. 15. Oppenheim, R. W. (1971). Prehatching and hatching behaviour in birds: a comparative study of altricial and precocial species. Anim. Behav. (In press). Sedlfi~k, J. (1964). Further findings on the conditions of formation of the temporary connection in chick embryos. Physiol. Bohemoslov., 13, 421-424, as cited in Oottlieb (1968).
19,
3
Snapp, B. D. (1969). Recognition of maternal calls by parentally naive Gallus gallus chicks. Anim. Behav., 17, 440 445. Sokolov, E. N. (1960). Neuronal models and the orienting reflex, In: The Central Nervous System and Behavior (Ed. by M. A. B. Brazier), pp. 187-276. Madison: Madison Printing Co. Tschanz, B. (1968). Trottellummen. Die Entstehung der persoenlichen Beziehung zwischen Jungvogel und Eltern. Z. Tierpsychol., Suppl., 4. Vanzulli, A. & Garcia-Austt, E. (1963). Development of cochlear microphonic potentials in the chick embryo. Acta Neurol. Latinoamer., 9, 19-23, as cited in Gottlieb (1968).
(Received 16 March 1970; revised 18 August 1970; second revision 18 December 1970; MS. number: A962)
PRENATAL EXPERIENCE OF PARENTAL CALLS AND PECKING IN THE LAUGHING GULL (LARUSATRICILLA L.) BY MONICA IMPEKOVEN
Institute of Animal Behavior, Rutgers University, Newark, New Jersey, U.S.A. Abstract. Laughing gulls emit a call referred to as 'crooning' with increasing frequency shortly before the hatching of their young. Uttered to newly hatched chicks this call appears to enhance pecking for food. The adult birds 'kow' call in response to disturbances near the nest. Incubator raised chicks respond differentially to these two calls, both pre- and post-natally. An experiment was designed to discover whether the hearing of such vocalizations prenatally would have any bearing on their postnatal effectiveness in eliciting pecking. With respect to 'crooning' an effect was found but it would not be clearly demonstrated that 'crooning' heard prenatally enhances pecking. Chicks pecked less often when hearing 'kow' calls regardless of prenatal experience with this call. Visual stimuli eliciting pecking in gulls have been studied extensively (e.g. Hailman 1967) but auditory aspects of the stimulus situation have received little attention. The adult laughing gull utters a smooth, long-drawn, low-pitched call referred to as 'crooning' or 'mew' call (Fig. 1) with increasing frequency shortly before the hatching of its young. Under the same labels functionally and structurally similar calls have been described for other gull species (reviewed by Evans 1970). Mate reliefs for incubation become more frequent as hatching approaches and the oncoming mate 'croons' besides giving other types of calls (according to my impressions on several nests): Also when alone the incubating bird may give a shorter version of this call after rising and before resettling or even while sitting on its pipping eggs (Impekoven, in preparation). After hatching, some parents 'croon' in the context of feeding the young. On the first and second day after hatching the chicks usually do not locomote but snuggle or sit nestled against the parent's plumage. Before feeding, the parent adopts a stooping posture so that its beak is presented directly in front of the chicks' eyes. According to Beer (1970) and personal observations, the adult then 'croons! if the chicks do not peck immediately. At the beginning of a feeding sequence the call may stimulate the chicks to peck at the parent's bill which in turn seems to promote regurgitation of food by the parent. At the end of the sequence the parent may 'croon' again if the chicks have not eaten all the food presented to them. Chicks of a clutch of eggs may hatch on successive days, thus late comers are exposed to 'crooning' uttered during such feedings whilst still in the egg.
From the 2nd day on when the young become more mobile, 'crooning' may function to attract them to the source of food from a distance also (Beer 1970).
Experiment 1 An experiment was designed to discover whether 'crooning' enhances pecking in incubator hatched chicks and whether the fact that the chicks hear this call prior to hatching has any bearing on the call's postnatal effectiveness. Effects of prenatal auditory experience on approach and following have been demonstrated in young guillemots (Tschanz 1968), domestic chicks (Grier, Counter & Shearer 1967) and ducklings (Gottlieb 1971) but the pecking response was not investigated quantitatively in these studies. Methods Approximately seventy gull chicks were tested in the Department of Zoology, University of Maryland and in the field-station of the Institute of Animal Behavior, situated near a large laughing gull colony in the Brigantine National Wildlife refuge, New Jersey. Subjects, Eggs collected from the gullery were hatched communally in an incubator at approximately 38 ~ to 39-4~ and around 70 per cent R.H. They were turned four to eight times per day till they started to pip. Such eggs were taken at various stages of the incubation cycle up to 3 days before hatching, thus some of them probably had some experience of adult gulls' calls prior to my treatments, others not. It is known that chick embryos respond to auditory stimuli electrophysiologically as early as 7 to 8 days before hatching (Vanzulli & Garcia- Austt 1963) 475
476
ANIMAL
BEHAVIOUR,
and behaviourally as early as 3 to 4 days (Sedlacek 1964). The incubation period of chickens is approximately 21 days, that of laughing gulls 23 days. Apparatus. Calls were recorded from nest-sites of gulls with 0 to 2 day old chicks by means of a Uher-4000-L Report tape-recorder and an omnidirectional microphone (M515). The same tape-recorder was used for playing calls to pipping eggs and incubator hatched chicks. Sound level measurements were made on scale B of a calibrated General Radio soundlevel meter. Eggs were hatched in a force-draft 'Gooser' (Humidaire Co.) or a still-air kerosene incubator (make unknown). The above mentioned incubation temperature refers to the latter. Procedure. A few days before hatching, a starshaped crack appears near the pole of the large blunt end of the shell. This was thought of as being the first stage of pipping and thus was referred to as P1. Yet recent investigations showed that this crack is produced by the rightlifting movements of head and beak during tucking (Oppenheim, personal communication). In the second stage (P2) cracks become visible over an enlarged area. In the third stage (P3) a small hole appears. This pipping hole is enlarged and after it reaches a certain size the actual hatching process starts. In field-observations using microphones placed in nests, calls from the egg did not become audible until late P2 which corresponds with the time when the bill penetrates into the air-space (Oppenheim, personal communication and own observation). Often in response to these calls the parent may call during late P2 and more so during P3 (Impekoven, in preparation). Accordingly one group containing 28 eggs was repeatedly exposed to 'crooning' during the P3-stage till they began to hatch. 'Crooning was played at 76 to 84 db measured near the egg, with a background noiselevel of 50 db or less. Each egg was exposed to the sound individually; it was taken from the incubator, carried to another room where 'crooning' calls were played to it in four bursts of 15-s duration separated by 15-s periods of no sound. The recording consisted of a natural sequence of nine 'croons' of a parent gull towards its day-old chick. The sequence contained only one chick-call. The median interval between 'croons' was 0.7 s. This treatment was repeated every 13 or 2 hr except for an interval of several hours over night. It was given between one and eight times depending
19,
3
on how fast pipping proceeded which was very variable from egg to egg. This treatment differs from the situation in the wild where the incubating bird may call only once or twice in close succession but does so quite frequently. Intervals between nest-reliefs and the number of 'croons' given by the oncoming mate are very variable. Another group of twenty-one eggs was not exposed to 'crooning'. Eight of these eggs were never taken from the incubator; thirteen of them were exposed to 'no sound' for times roughly comparable with those of eggs exposed to 'crooning', in order to control for the possibility that the handling and light-exposure rather than the sound itself would affect the subsequent test-response. The two groups of chicks were tested for pecking between 43 and 12 hr after hatching (i.e. at an age when they stand and peck but when they do not walk). Wild chicks view the parent's dark red beak in a more or less vertical position against the green grass surrounding the nest. Accordingly pecking experiments were carried out in a black box with a vertical red dowel rod placed in front of a green cloth wall. The rod was kept stationary and its tip at the chick's eye level; from behind the green wall 'crooning' calls were played. These calls were the same as those presented in the prenatal exposures except for the intensity near the chick which now was 84 to 90 db. Each chick was tested first for 89min with two 15-s sequences of sound, i.e. eighteen calls and then 3 rain with no sound or vice versa. The two tests were separated from one another by 3 rain or 13 min during which periods the chick was kept under a translucent container in front of the pecking stimulus. Recorded were the number of pecks directed at the red stimulus rod during the sound and no sound condition. In order to see whether and in what way the embryos would respond to the calls during the prenatal exposures thirty-eight eggs were observed as soon as the beak was visible through the enlarged pipping hole. Only twenty-nine of these e g g s were retested after hatching, sixteen of the 'crooning' experienced group and thirteen of the 'no sound' experienced group. When the pipping hole is enlarged bill-movements like bill-clapping, yawning, grinding and back-thrusts against the shell can be recognized. I recorded whether such bill-activities occurred during the 15-s sound and no sound periods in the 'crooning' exposed birds and comparable 15-s no sound periods in birds not exposed to 'crooning'.
IMPEKOVEN: PRENATAL EXPERIENCE IN LAUGHING GULL CHICKS
477
Table I. Chicks: Median Number of Peeks Towards a Red Stimulus Rod
Test-condition No.
Sound
No sound 4"5 10
14.5 16
<0.01 NS
7 13
9 17
<0.05 <0.001
'Crooning' Prenatal condition*
Sound No sound
28 21
10 6
'Kow' Prenatal conditiont
Sound No Sound
12 12
2 4
Total
P
*Difference between prenatally sound and no-sound experienced chicks P<0.01 tDifference between prenatally 'crooning' experienced and 'kow' experienced chicks P<0-002 Results
Experiment 2
'Crooning' experienced chicks pecked more often when hearing the sound than when not. 'No sound' experienced chicks tended to peck more in the no sound than in the sound condition (Table I). The total pecking scores were not different under the two treatments. The relative pecking scores of the 'no sound' experienced chicks under the two testing conditions were the same regardless of whether the eggs were taken from the incubator or not. The total pecking scores were higher in the thirteen 'exposed' chicks than in the eight 'unexposed' ones suggesting that the prenatal handling and or light exposure affected the activity level after hatching. Similarly 'crooning' exposed embryos showed a higher number of 15-s activity periods in the sound than in the no sound situation but the total number of such periods was not higher than that of 'no sound' experienced birds (Table II). Table II. Embryos: Median Number of 15-s Bill-Activity Periods per Minute Exposure
No.
Exposure Sound No sound Total
P
'Crooning'
19
1.3
0.5
1.8
<0.01
'Kow'
17
0.6
0.75
1.35
iS
19
No sound 1.0
1.0
2.0
'No sound'
Statistical tests: Wilcoxon two-tailed for comparison between different test-conditions, Mann-Whitney U two-tailed for comparison between groups with different prenatal experience.
From the result of the first experiment the question arose whether the described effect of 'crooning' was stimulus specific or not. I approached this problem by comparing some of the 'crooning' experienced birds with others raised and tested with 'kow' calls. 'Kow' calls differ from 'crooning' in their sudden onset, shorter duration, higher pitch and harshness (Fig. 1). Single birds 'kow' call at the nest-site in response to minor disturbances of various kinds, and many b i r d s 'kow' call in flight in response to ground predators during incubation and hatching. Functionally this call could be described as an 'alarm' call. Methods
The methods were essentially the same as the ones used in the first experiment. In temporal alternation with some of the eggs exposed to 'crooning' or 'no sound', seventeen other eggs were exposed to 'kow' calls, made by a single bird played at similar intensity levels as 'crooning' and with a comparable number of exposures during the P3-stage. The training tape consisted of three natural sequences of six 'kows' each, the test tape of six such sequences. The median interval between such calls was 0.5 s. Twelve of these chicks were tested for pecking after hatching. Another group of twelve chicks was not exposed to 'kow' calls during pipping but was tested in the pecking situation after hatching. These chicks had been tested with 'crooning' before, which may have affected the performance in the subsequent 'kow' test. Seventeen eggs were observed during the prenatal exposures to 'kow' calls.
478
ANIMAL
BEHAVIOUR,
19,
3
7 CROON
6 5 4 ~3 N
--r-2.
~O-
r
r
T
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Fig. 1. Spectrograms of 'crooning' and 'kow' call made on a Kay Electric Co. Sonagraph with a narrow band filter. (Both are sections from the tape used in the experiments;)
Results
Despite this prenatal experience such chicks pecked more in the no sound than in the sound condition (Table I). The relative scores hardly differed from those of 'no sound' experienced birds though the total pecking scores were much lower. Their total pecking scores were also lower than those of 'crooning' experienced chicks, but the difference is not statistically significant. Moreover observations of their bill-movements during the P3-stage showed that the embryos were not more active during the sound than during the no sound condition. Discussion
The results show that prenatal experience of 'crooning' affects the postnatal responsiveness to this call. As to the question whether 'crooning' heard prenatally enhances the pecking response in incubator hatched chicks, the results do not provide a clear-cut answer. In contrast to 'no sound' experienced chicks 'crooning' experienced chicks pecked more often in the sound than in the no sound condition. From this result one would conclude that parental 'crooning' enhances pecking if heard prenatally. However the fact that the
total pecking score of 'crooning' raised chicks was not higher than that of birds without prenatal 'crooning' experience does not support such a conclusion. In the present experiments the chicks were tested between 489 and 12 hr after hatching, before they were ever fed. Even in absence of additional stimulation many chicks readily pecked at the red stimulus rod. This differs from the situation in the wild where calls are emitted when the chicks do not peck immediately and thus are probably not very hungry (see 'Introduction'). It is possible that some of the experimental birds were maximally responsive to the visual stimulus alone. Further experiments will have to show whether more satiated chicks would differ in their absolute peckingrate under the two treatments. Can one conclude that chicks simply peck most in a situation made familiar to them through prenatal exposure: 'crooning' in one case and 'no crooning' in the other? Both groups of embryos experienced 'no sound' during such exposures and during the time they spent in the incubator; thus such an interpetation cannot fully explain the results. The fact that 'no sound' experienced chicks tended to peek less often in the sound con-
IMPEKOVEN: PRENATAL EXPERIENCE IN LAUGHING GULL CHICKS dition than in the no sound condition calls for an explanation. To these chicks 'crooning' was a novel stimulus and thus may have elicited a 'listening' response or 'orienting reflex' which is subject to habituation with repeated presentation of the novel stimulus (Sokolov 1960). Accordingly 'crooning' experienced chicks may have become habituated to the novelty effect of 'crooning' through prenatal exposure to this call. Further research is required to determine the limits of auditory sensitivity in terms of developmental age. More recent data indicate that embryos respond to 'crooning' during the P1 and early P2 stage on days 19 and 20 (Gold & Impekoven, in preparation). Probably postnatal responsiveness to 'crooning' is not only affected by prior exposure to this particular call but to other calls sharing certain characteristics with 'crooning'. Bursts of a variation of short, low pitched sometimes disyllabic notes with smooth onset are given by many birds in association with shifting of the eggs and resettling over much of the incubation time. Similarly, calls accompanying 'choking'-displays after the landing of a mate by the nest with nesting material consist of a rapid sequence of even shorter, low pitched notes. In response to both types of calls embryos in the P3-stage responded similarly though not as strongly as to 'crooning' (Impekoven, in preparation). The effect of exposure to such calls on postnatal responsiveness to 'crooning' has not been tested. In response to 'crooning', pipping embryos showed an increase in the amount of their billmovements. Similar findings were made with respect to ducklings (Gottlieb 1965). The comparison of activity periods in 'crooning' and 'no sound' exposed chicks suggests that 'crooning' in these embryos did not raise the overall readiness for bill-movements but changed the temporal distribution of their occurrences. The measurements for bill-activity in this study were very crude and further tests will have to show whether the actual number and amplitude of bill-movements is also unaffected under the two treatments. Responsiveness to 'crooning' in pipping embryos may be affected by its frequent temporal association with photic and mechanical stimulation which occurs during nest-relief, egg-shifting and resettling and in the experiment by taking the eggs from the incubator, carrying them and returning them to the incubator.
479
Experiment 2 showed that despite prenatal experience with 'kow' calls such birds pecked less often in the sound than in the no sound condition. Actually some of these chicks did not peck at all in response to 'kow' calls but crouched. The results with 'kow' calls suggest that 'Crooning' may have specific features that lead to its particular effect. What these features are (pitch, temporal pattern, smoothness of onset or timbre) remains to be discovered. In contrast to 'crooning', 'kow' calls seem to have characteristics that inhibit pecking despite repeated prenatal exposure to this call. Unlike 'crooning', 'kow' calls may elicit an avoidance response or defensive reaction that interferes with the ongoing behaviour. According to Fischer & Gilman (1969) avoidance responses appear to be caused by a sudden onset of sound which is one of the characteristics of 'kow' calls. The difference in the total pecking score between 'kow' and 'no kow' experienced chicks cannot be interpreted any further at this point since it may merely be due to the fact that 'no kow' experienced chicks were tested with 'crooning' before. Differential responsiveness to the maternal 'feeding' and 'distress' call ('alarm' call?) has also been established for naive red jungle-fowl chicks (Snapp 1969) although the details of that study differ much from the present one.
Acknowledgments I thank Dr W. M. Schleidt and Dr J. P. Hailman for advice and equipment and Dr J. S. Rosenblatt, Dr C. G. Beer and Dr D. S. Lehrman for comments on the manuscript. The cooperation and hospitality of the Brigantine National Wildlife Refuge are greatly acknowledged. This study was supported by Public Health Service Grant GM122774 and GM16727. REFERENCES Beer, C. G. (1970). On the responses of laughing gull chicks to the calls of adults. II. Age changes and responses to differenttypes of calls. Anim. Behav., 18, 661-677. Evans, R. M. (1970). Parental recognition and analysis of the 'mew' call in black-billed gulls (Larus bulleri). The Auk, 87, 503-513. Fischer, G. J. & Gilman, S. A. (1969). Followingduring imprinting as a function of auditory stimulus intensity. Develop. PsychoL, 1, 216-218. Gottlieb, G. (1965). Prenatal auditory sensitivity in chickens and ducks. Science, N.Y., 147, 15961598. Gotflieb, G. (1968). Prenatal behavior of birds. Quart. Rev. BioL, 43, 148-174.
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ANIMAL
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Grier, J. B., Counter, S. A. & Shearer, W. M. (1967). Prenatal auditory imprinting in chickens. Science, N.Y., 155, 1692-1693. Hailman, J. P. (1967). The ontogeny of an instinct. The pecking response in chicks of the laughing gull and related species. Behaviour, Suppl. 15. Oppenheim, R. W. (1971). Prehatching and hatching behaviour in birds: a comparative study of altricial and precocial species. Anim. Behav. (In press). Sedlfi~k, J. (1964). Further findings on the conditions of formation of the temporary connection in chick embryos. Physiol. Bohemoslov., 13, 421-424, as cited in Oottlieb (1968).
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Snapp, B. D. (1969). Recognition of maternal calls by parentally naive Gallus gallus chicks. Anim. Behav., 17, 440 445. Sokolov, E. N. (1960). Neuronal models and the orienting reflex, In: The Central Nervous System and Behavior (Ed. by M. A. B. Brazier), pp. 187-276. Madison: Madison Printing Co. Tschanz, B. (1968). Trottellummen. Die Entstehung der persoenlichen Beziehung zwischen Jungvogel und Eltern. Z. Tierpsychol., Suppl., 4. Vanzulli, A. & Garcia-Austt, E. (1963). Development of cochlear microphonic potentials in the chick embryo. Acta Neurol. Latinoamer., 9, 19-23, as cited in Gottlieb (1968).
(Received 16 March 1970; revised 18 August 1970; second revision 18 December 1970; MS. number: A962)