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The acoustic basis of mate recognition by female Zebra finches (Taeniopygia guttata)
Anim. Behuv., 1979,27,376-380
THE ACOUSTIC BASIS OF MATE RECOGNITION BY DAVID
BY FEMALE ZEBRA
B. MILLER*
Department of Ethology, Faculty of Biology, University of Bielefeld
Abstract. Laboratory
experiments were conducted to assessthe extent to which female zebra tinches to the song of their own mate versus the song of a neighbouring conspecific male. Following a 2 to 3 day period of separation from their mates, 20 females were tested individually in 30-min simultaneous auditory choice tests. Of the birds that showed clear preferences as assessed via approach duration scores, 14 strongly preferred the song of their mate, and two preferred the song of a neighbour. Thus, one possible function of male zebra finch song, which is highly variable inter-individually, is to provide his mate with an acoustic basis of individual recognition that may serve to strengthen and/or maintain the pair bond. (Tueniopygiu guttuta) respond preferentially
Important coevolutionary adaptations in animals that are monogamous and form durable, lifelong pair bonds are (a) physical or behavioural attributes that are inter-individually variable and intra-individually stable, and (b) perceptual met hanisms that facilitate intersexual, individual recognition in the particular sensory modalities that convey these stimulus attributes. Zebra finches (Tueniopygiu guttutu), one of several species of Australian grassfinches (family Estrildidae), form life-long pair bonds (Immelmann 1965; Butterfield 1970), as do other congeneric species (Zann 1977). One of the more striking behavioural attributes that, by virtue of its inter-individual variability and intra-individual stereotypy, could provide a basis for individual recognition is the song of the male (Immelmann 1965, 1969). Moreover, since male zebra finches are non-territorial (Irnmelmann 1965), there would appear to be little selective pressure for intermale auditory recognition, unlike the case in most passerines. Males typically sing when courting a female (i.e. courtship song) and when separated from a mate (i.e. solitary or undirected song). The courtship and solitary songs are, for the most part, identical in all physical characteristics (Immehnann 1969 ; Butterfield 1970; unpublished observations by the author). While a number of authors have suggested that bird vocalizations may function to strengthen or maintain pair bonds (Thorpe & North 1965; Irnmehnann 1968; Sullivan 1976; Erickson 1977; Collias & Collias 1978; Jenkins 1978), only a few investigators have experimentally validated this assumption (e.g. in *Present address : Anderson Hall, Dorothea Hospital, Raleigh, North Carolina 27611, U.S.A.
laughing gulls, L.arus atricillu, Beer 1970; in Curduelis tristti, American goldfjnches, Mundinger 1970; in gannets, Sula bussunu, White 1971). Several investigators have suggested that male zebra 8nch song promotes individual recognition by females and thereby functions to maintain the pair bond (Morris 1954; Immehnann 1965, 1969; Butterfield 1970; Zann 1974, personal communication); however, the only experimental demonstrations of pair bond durability in zebra finches have involved visual and/or combined audiovisual aspects of mates (Morris 1954; Butterfield 1970; Caryl 1976). In the present study, I attempt to elucidate the extent to which male zebra finch song may functionally promote pair bond maintenance by assessing the preferential responsiveness of adult females in simultaneous auditory choice tests involving the song of their mate versus the song of a neighbour. Methods Subjects and Housing Conditions Twenty pairs of adult male and female domestic zebra finches, all of which had zebra finch parents, were extracted from the breeding colony at the University of Bielefeld and housed pairwise in a separate room containing 20 plastic and wire breeding cages (82-O x 39.0 x 30.0 cm). Hanging out of each cage was a wooden nest box (15-O x 16.0 x 14.0 cm) with a 12.5 x 6.5-cm opening cut out on one side near the top. The breeding room was small, and the breeding cages were physically touching at least three or four other cages. Thus, females were well exposed to songs of other males in addition to those of their mate. Also, females
Dix 376
MILLER:
ZEBRA
FINCH
were able to see other breeding pairs across the small room but were exposed only to the vocal aspects of their immediate neighbours. The breeding room was maintained on a light/dark cycle of 14/10 h and at a temperature of 20 to 23 C to keep the birds in breeding condition all year round. Each pair had successfully reared at least one brood of young, though most pairs raised multiple broods. All birds had been paired at least 6 to 12 months prior to testing, and in some cases up to two years. Thus, at the time of testing the pair bonds were presumably well established. Apparatus The test apparatus (Fig. l), constructed of a wood frame with wire ‘bars’ and measuring 211.5 x 46.0 x 37.5 cm, was housed in a 3.22 x 2.23 x 3.02-m soundproof anechoic chamber. The apparatus was divided into two approach zones at opposite ends separated by a neutral zone, each zone measuring 70.5 cm in length. Each approach zone contained four perches, and the neutral zone contained three perches and a wood and wire start box (S in Fig. 1) measuring 11-O x 16.0 x 11.0 cm. A guillotine door on the front of the start box could be raised remotely by pulling a string, thereby providing the bird with access to the apparatus. Loudspeakers (LS in Fig. 1) (Braun L 710/l) were located at opposite ends of the apparatus adjacent to each approach zone. To minimize experimenter interference with the bird, the tests were monitored remotely in an adjoining room via a video camera and microphone situated inside the anechoic chamber. Sounds were broadcast via two Uher 4400 Report Stereo IC tape recorders connected to a Teleton Hi-Fi Stereo Amplifier (Model GA-202; Mitsubishi Corp., Japan). Test Stimuli Solitary and courtship songs of the 20 adult male zebra finches were recorded inside the anechoic chamber on a Uher 4400 Report Stereo TC tape recorder using a directional
Fig. 1. Apparatus employed in simultaneous choice tests. S = start box; LS = loudspeaker.
auditory
MATE
RECOGNITION
311
microphone (either a Uher M537 or a Uher M815). Singing was induced by isolating the male from his mate for a few hours up to a day in a small wood and wire cage (45.0 x 32-O x 24.0 cm) inside the anechoic chamber. This often resulted in the male singing solitary song. Courtship song was easily induced by introducing his mate to the cage. All recordings were made 2 to 6 months before the particular female was tested. One to five songs per male (selected on the basis of clarity with no female vocalizations in the background) were re-recorded onto test tapes using the Uher tape recorder in conjunction with an Akai GX-280D-SS tape recorder. Most of the test songs were courtship songs, and there was no evidence that the females’ preferences depended on the number or type of songs chosen to make up the test tape for a particular male. The songs varied considerably in duration (mean = 5.28 s, SD = 2.78 s, iV = 88 songs), and each was separated by 5.0s of silence on the test tape. Each test tape contained the songs of only one male and had a duration of 30 min. Procedure Prior to testing, the female was separated from her mate and placed in a wood and wire cage (70.5 x 46.0 x 37.5 cm) inside the anechoic chamber for two to three days under a 14/10 light/dark cycle. This period of separation simulates the maximum period of time that a female might be separated from her mate in nature (Immelmann, personal communication). All birds were tested between 08.00 and 12.00 hours. Just prior to testing, the female was transferred to the start box inside the test apparatus. The experimenter left the anechoic chamber and allowed the bird 3 min to adapt to the transfer. (Most birds calmed down immediately after the experimenter left the chamber.) After 3 min of adaptation, the experimenter turned on both tape recorders, each containing a tape of songs from a different male. The tapes were broadcast at an amplitude of 60 f 4 dB, as measured from the area of the start box with a Briiel and Kjaer Type 2203 Precision Sound Level Meter set at Scale A, fast. At the same time, three stopwatches were activated simultaneously to time the total trial (30 min), latency to the right approach zone, and latency to the left approach zone. The songs were broadcast synchronously at the onset of the
378
ANIMAL
BEHAVIOUR,
trial, but the synchrony was soon attenuated due to the varying song durations. Seven seconds later, the guillotine door of the start box was raised by pulling a string, and the behaviour of the female was monitored for the next 30 min in a simultaneous choice test involving the song of her mate versus the song of a neighbour. Thus, each female was given a choice between two familiar songs, only one of which came from a male with which she had mated and presumably formed a pair bond. The mate’s song was broadcast from the right speaker for 50% of the birds and from the left speaker for the other 50 % to control for possible (yet undetected) positional biases. As soon as a female entered an approach zone, the latency stopwatch was turned off and another stopwatch was activated to measure duration of approach. Duration scores could be amassed by repeated entries into an approach zone. A preference was scored only if the female spent twice as much time in one approach zone as in the other for a minimum of 3 min (i.e. 10% of the trial). To assess the durability of the initial pair bond, 12 females that preferred their mate’s song in the preference test were re-paired with different males. A new pair bond was considered established if the new pair successfully reared at least one brood of young. Only six pairs met this criterion, and these females were retested with the song of the first mate versus the song of the second mate using the above procedure. Statistical Analysis The present analysis focuses on incidence of responding (i.e. number of birds showing a preference for one song over the other), latency of approach (i.e. the time elapsing between the raising of the guillotine door and the female entering an approach zone), and duration of approach (i.e. the total amount of time spent in each approach zone in the 30-min trial). Mean latencies and durations are based only on those animals that responded. If an animal approached only one song, it was assigned a latency score of 1800 s and a duration score of 0 s with respect to the non-approached song, and these figures were involved in the statistical analysis and in the computation of the means in Tables I and II. Incidences of responding were assessed by the &i-square one-sample test, and latency and duration scores (in seconds) were evaluated by the Mann-Whitney U-test employing the cor-
27,
2
rection factor for tied ranks (Siegel 1956). All probability values are 2-tailed. ReSUltS As shown in Fig. 2, female zebra finches had a significant preference for the song of their mate versus the song of a neighbour (~2 = 9.0, P < 0.01, df = 1). Three females showed no preference in #at they spent about as much time in one approach zone as in the other, and one female preferred neither song in that she remained inside the start box during the entire 30-min trial. As shown in Table I, there was a non-significant trend for females to have shorter latencies of approach to their mate’s song versus a neighbour’s song. However, females spent significantly more time in their mate’s approach zone than in the neighbour’s approach zone (P --c 0401). In the present context, duration scores are probably more valid measures of preference than latency scores in that several females were apparently startled by the raising of the start box guillotine door and flew quickly out of the start box. They often landed in the approach zone adjacent to the speaker broadcasting the neighbour’s song, and then immediately or eventually flew to the other approach zone broadcasting their mate’s song where they would remain for the rest of the trial. 167 co l4 !fi
12.
; u. L 0
lo-
$j
6:
i
4-
=
2-
8-
~ I
MATE
I
l---l
I
I
r-l
I
NEIGHBOUR
BOTH
I
I NEITHER
PREFERENCE
Fig. 2. Number of females preferring the song of their
mate, the song of their neighbour, both songs equally, and neither song (i.e. non-responders) in simultaneous auditory choice tests.
MILLER:
ZEBRA
FINCH
Of the six females that successfully met the criterion of having formed a new pair bond with a second male, three preferred the hrst mate, two preferred the second mate, and one did not respond; thus, there was no significant preference for one mate over the other. However, as shown in Table II, females had a significantly shorter latency to the song of the first mate than to the song of the second mate (P < O-02), while differences in duration scores were nonsignificant. Although the sample size is small, it would appear that some females are capable of remembering and preferring the song of their first mate to the song of their second mate. However, teasing apart primacy versus recency effects in the context of mate recognition necessitates a larger sample of successful rematings than is achieved in the present study. Discussion These data provide experimental evidence for one functional aspect of male zebra finch song by showing that females learn the song of their mate and respond preferentially to it following a period of separation. Thus, as previously suggested by other investigators (Morris 1954; Immelmann 1965, 1969; Butterfield 1970; Zann 1974), the song of the male can function to strengthen and maintain the pair bond to the extent that the female, using this acoustic stimulus configuration, can recognize and show a preference for her own mate versus neighbouring males. This is not to suggest, however, that song does not serve other functions as well. For example, song may also be involved in mate selection by female zebra finches (Miller in press), as well as having other possible functions. Solitary song, which is identical to directed courtship song in terms of acoustic structure, has been suggested to play a role in pair bond maintenance (Morris 1954; Immelmann 1968). Since, in the field, males have been observed to Table I. Latency and Duration of Response of 16 Female Zebra Finches that Showed a Prekwxe in 30-min Simnltaaeous Auditory Choice Tests Involving tbe Song of their Mate Versus tbe Song of a Neigbbour Latency (s) Test song Mate
Mean 434
Neighbour
SD
Mean
559
1048 P <
NS
VS.
803
Duration
831
349
MATE
RECOGNITION
sing in the area of the nest while visually separated from their incubating mates (Immelmann, personal communication), the present data add further substance to the presumed functional significance of solitary song in maintaining a pair bond. This is insofar as females are capable of recognizing the songs of their own mates. Although only a small number of birds in the present study formed pair bonds with new mates when denied access to their former mates, it is interesting that, upon retesting, each of the females that responded had very short latencies to the song of the first mate versus the song of the second mate (Table II). This is at least suggestive that females are capable of remembering the song of their first mate following very long periods of separation (up to six months in the present study) with intervening exposure to a new mate’s song. It is also suggestive that they have an initial preference for the song of the former mate that may or may not become attenuated during the course of the test session (i.e. three birds remained near the first mate’s song, and two birds switched over to the second mate’s song in terms of approach durations). It is important to recognize that the pair bond is probably maintained by more than song alone. Indeed, others have demonstrated that visual and/or combined audiovisual cues play a role in pair bond maintenance (Morris 1954 ; Butterfield 1970; Caryl 1976). The present study does demonstrate, however, that in the absence of visual cues (as when the male is singing solitary song out of visual range of his incubating mate), song can provide a sufficient basis by which a female can recognize her mate. Acknowledgments This research was conducted while I was supported by a fellowship from the Alexander von Humboldt-Stiftung. I thank Klaus Immelmann for sponsoring my stay in Germany, Table II. Latency and Duration of Response of 5 Female zebra Finches that Sbowed a Prehence in 30411 Simultaneous Auditory Choice Tests Involving tbe Song of their First Mate Versus the Song of their Second Mate Latency (s)
(s) SD
532 0.001 519
319
Test song First mate
Duration
Mean
SD
Mean
26
18
875
764
946
SD
809 NS
P < 0.02
Second mate
(s)
557
687
380
ANIMAL
BEHAVIOUR,
for generously providing full access to his laboratory facilities, and for suggesting this study. I also thank Linda L. Miller for carefully preparing the figures. REFERENCES Beer, C. G. 1970. Individual recognition of voice in the social behavior of birds. In: Advances in rlre Study ofBehavior, Vol. 3 (Ed. by D. S. Lehrman, R. A. Hinde & E. Shaw), pp. 27-74. New York: Academic Press. Butterfield, P. A. 1970. The pair bond in the Zebra finch. In : Social Behaviour in Birds and Mammals: Essays on the Social Ethology of Animals and Man (Ed. by J. H. Crook), pp. 249-278. London: Academic Press. Caryl, P. G. 1976. Sexual behaviour in the zebra f&h Taeniopygia guttata: Response to familiar and novel uartners. Anim. Behav.. 24. 93-107. Collias, E.~C: & Collias, N. E. 1978: N&t building and nesting behaviour of the Sociable Weaver Philetairus socius. Ibis, 120, l-15. Erickson, C. J. 1977. The nature and function of pairbonds. In: Grzimek’s Encyclopedia of Ethology (Ed. by K. Immelmann), pp. 469-486. New York: Van Nostrand Reinhold. Immelmann, K. 1965. Australian Finches in Bush and Aviary. Sydney: Angus and Robertson. Immelmann, K. 1968. Zur biologischen Bedeutung des Estrildidengesanges. J. Ornithol., 109, 284-299. Immelmann, K. 1969. Song development in the zebra finch and other Estrildid finches. In : Bird Vocalizations (Ed. by R. A. Hinde), pp. 61-74. London: Cambridge University Press.
27,
2
Jenkins, P. F. 1978. Cultural transmission of song patterns and dialect development in a free-living bird population. Anim. Behav., 26, 50-78. Miller, D. B. In press. Beyond sexual imprinting. Proc. int. ornithol. Congr., 17, in press. Morris, D. 1954. The reproductive behaviour of the Zebra finch (Poephila guttata), with specialreference to pseudofemale behaviour and displacement activities. Behaviour, 6, 271-322. Mundinger, 9.. C. 1970. Vocal imitation and individual ;ecca~p of 6nch calls. Science, N. Y., 168, Siegel, S. 1956. Nonparametric Statistics. New York: McGraw-Hill. Sullivan, G. A. 1976. Song of the finch Lugonosticta seneaala: Intersnecific mimicrv bv its broodpa&site Vidua chalybeata and the rhle of song in the host’s social context. Anim. Behav., 24, 880-888. Thorpe, W. H. & North, M. E. W. 1965. Origin and significance of the power of vocal imitation: with special reference to the antiphonal singing of birds. Nature, Lond., 208, 219-222. White, S. J. 1971. Selective responsiveness by the gannet (Sula bussuna) to played-back calls. Anim. Behuv., 19, 125-131. Zann, R. 1974. Undirected song in Poephilu grasstinches (Estrildidae). Paper presented at the XVIth International Ornithological Congress, Canberra. Zann, R. 1977. Pair-bond and bonding behaviour in three species of grassfinches of the genus Poephifa (Gould). Emu, 77, 97-106. (Received 1 May 1978; revised 3 June 1978 ; MS. number: 1754)
THE ACOUSTIC BASIS OF MATE RECOGNITION BY DAVID
BY FEMALE ZEBRA
B. MILLER*
Department of Ethology, Faculty of Biology, University of Bielefeld
Abstract. Laboratory
experiments were conducted to assessthe extent to which female zebra tinches to the song of their own mate versus the song of a neighbouring conspecific male. Following a 2 to 3 day period of separation from their mates, 20 females were tested individually in 30-min simultaneous auditory choice tests. Of the birds that showed clear preferences as assessed via approach duration scores, 14 strongly preferred the song of their mate, and two preferred the song of a neighbour. Thus, one possible function of male zebra finch song, which is highly variable inter-individually, is to provide his mate with an acoustic basis of individual recognition that may serve to strengthen and/or maintain the pair bond. (Tueniopygiu guttuta) respond preferentially
Important coevolutionary adaptations in animals that are monogamous and form durable, lifelong pair bonds are (a) physical or behavioural attributes that are inter-individually variable and intra-individually stable, and (b) perceptual met hanisms that facilitate intersexual, individual recognition in the particular sensory modalities that convey these stimulus attributes. Zebra finches (Tueniopygiu guttutu), one of several species of Australian grassfinches (family Estrildidae), form life-long pair bonds (Immelmann 1965; Butterfield 1970), as do other congeneric species (Zann 1977). One of the more striking behavioural attributes that, by virtue of its inter-individual variability and intra-individual stereotypy, could provide a basis for individual recognition is the song of the male (Immelmann 1965, 1969). Moreover, since male zebra finches are non-territorial (Irnmelmann 1965), there would appear to be little selective pressure for intermale auditory recognition, unlike the case in most passerines. Males typically sing when courting a female (i.e. courtship song) and when separated from a mate (i.e. solitary or undirected song). The courtship and solitary songs are, for the most part, identical in all physical characteristics (Immehnann 1969 ; Butterfield 1970; unpublished observations by the author). While a number of authors have suggested that bird vocalizations may function to strengthen or maintain pair bonds (Thorpe & North 1965; Irnmehnann 1968; Sullivan 1976; Erickson 1977; Collias & Collias 1978; Jenkins 1978), only a few investigators have experimentally validated this assumption (e.g. in *Present address : Anderson Hall, Dorothea Hospital, Raleigh, North Carolina 27611, U.S.A.
laughing gulls, L.arus atricillu, Beer 1970; in Curduelis tristti, American goldfjnches, Mundinger 1970; in gannets, Sula bussunu, White 1971). Several investigators have suggested that male zebra 8nch song promotes individual recognition by females and thereby functions to maintain the pair bond (Morris 1954; Immehnann 1965, 1969; Butterfield 1970; Zann 1974, personal communication); however, the only experimental demonstrations of pair bond durability in zebra finches have involved visual and/or combined audiovisual aspects of mates (Morris 1954; Butterfield 1970; Caryl 1976). In the present study, I attempt to elucidate the extent to which male zebra finch song may functionally promote pair bond maintenance by assessing the preferential responsiveness of adult females in simultaneous auditory choice tests involving the song of their mate versus the song of a neighbour. Methods Subjects and Housing Conditions Twenty pairs of adult male and female domestic zebra finches, all of which had zebra finch parents, were extracted from the breeding colony at the University of Bielefeld and housed pairwise in a separate room containing 20 plastic and wire breeding cages (82-O x 39.0 x 30.0 cm). Hanging out of each cage was a wooden nest box (15-O x 16.0 x 14.0 cm) with a 12.5 x 6.5-cm opening cut out on one side near the top. The breeding room was small, and the breeding cages were physically touching at least three or four other cages. Thus, females were well exposed to songs of other males in addition to those of their mate. Also, females
Dix 376
MILLER:
ZEBRA
FINCH
were able to see other breeding pairs across the small room but were exposed only to the vocal aspects of their immediate neighbours. The breeding room was maintained on a light/dark cycle of 14/10 h and at a temperature of 20 to 23 C to keep the birds in breeding condition all year round. Each pair had successfully reared at least one brood of young, though most pairs raised multiple broods. All birds had been paired at least 6 to 12 months prior to testing, and in some cases up to two years. Thus, at the time of testing the pair bonds were presumably well established. Apparatus The test apparatus (Fig. l), constructed of a wood frame with wire ‘bars’ and measuring 211.5 x 46.0 x 37.5 cm, was housed in a 3.22 x 2.23 x 3.02-m soundproof anechoic chamber. The apparatus was divided into two approach zones at opposite ends separated by a neutral zone, each zone measuring 70.5 cm in length. Each approach zone contained four perches, and the neutral zone contained three perches and a wood and wire start box (S in Fig. 1) measuring 11-O x 16.0 x 11.0 cm. A guillotine door on the front of the start box could be raised remotely by pulling a string, thereby providing the bird with access to the apparatus. Loudspeakers (LS in Fig. 1) (Braun L 710/l) were located at opposite ends of the apparatus adjacent to each approach zone. To minimize experimenter interference with the bird, the tests were monitored remotely in an adjoining room via a video camera and microphone situated inside the anechoic chamber. Sounds were broadcast via two Uher 4400 Report Stereo IC tape recorders connected to a Teleton Hi-Fi Stereo Amplifier (Model GA-202; Mitsubishi Corp., Japan). Test Stimuli Solitary and courtship songs of the 20 adult male zebra finches were recorded inside the anechoic chamber on a Uher 4400 Report Stereo TC tape recorder using a directional
Fig. 1. Apparatus employed in simultaneous choice tests. S = start box; LS = loudspeaker.
auditory
MATE
RECOGNITION
311
microphone (either a Uher M537 or a Uher M815). Singing was induced by isolating the male from his mate for a few hours up to a day in a small wood and wire cage (45.0 x 32-O x 24.0 cm) inside the anechoic chamber. This often resulted in the male singing solitary song. Courtship song was easily induced by introducing his mate to the cage. All recordings were made 2 to 6 months before the particular female was tested. One to five songs per male (selected on the basis of clarity with no female vocalizations in the background) were re-recorded onto test tapes using the Uher tape recorder in conjunction with an Akai GX-280D-SS tape recorder. Most of the test songs were courtship songs, and there was no evidence that the females’ preferences depended on the number or type of songs chosen to make up the test tape for a particular male. The songs varied considerably in duration (mean = 5.28 s, SD = 2.78 s, iV = 88 songs), and each was separated by 5.0s of silence on the test tape. Each test tape contained the songs of only one male and had a duration of 30 min. Procedure Prior to testing, the female was separated from her mate and placed in a wood and wire cage (70.5 x 46.0 x 37.5 cm) inside the anechoic chamber for two to three days under a 14/10 light/dark cycle. This period of separation simulates the maximum period of time that a female might be separated from her mate in nature (Immelmann, personal communication). All birds were tested between 08.00 and 12.00 hours. Just prior to testing, the female was transferred to the start box inside the test apparatus. The experimenter left the anechoic chamber and allowed the bird 3 min to adapt to the transfer. (Most birds calmed down immediately after the experimenter left the chamber.) After 3 min of adaptation, the experimenter turned on both tape recorders, each containing a tape of songs from a different male. The tapes were broadcast at an amplitude of 60 f 4 dB, as measured from the area of the start box with a Briiel and Kjaer Type 2203 Precision Sound Level Meter set at Scale A, fast. At the same time, three stopwatches were activated simultaneously to time the total trial (30 min), latency to the right approach zone, and latency to the left approach zone. The songs were broadcast synchronously at the onset of the
378
ANIMAL
BEHAVIOUR,
trial, but the synchrony was soon attenuated due to the varying song durations. Seven seconds later, the guillotine door of the start box was raised by pulling a string, and the behaviour of the female was monitored for the next 30 min in a simultaneous choice test involving the song of her mate versus the song of a neighbour. Thus, each female was given a choice between two familiar songs, only one of which came from a male with which she had mated and presumably formed a pair bond. The mate’s song was broadcast from the right speaker for 50% of the birds and from the left speaker for the other 50 % to control for possible (yet undetected) positional biases. As soon as a female entered an approach zone, the latency stopwatch was turned off and another stopwatch was activated to measure duration of approach. Duration scores could be amassed by repeated entries into an approach zone. A preference was scored only if the female spent twice as much time in one approach zone as in the other for a minimum of 3 min (i.e. 10% of the trial). To assess the durability of the initial pair bond, 12 females that preferred their mate’s song in the preference test were re-paired with different males. A new pair bond was considered established if the new pair successfully reared at least one brood of young. Only six pairs met this criterion, and these females were retested with the song of the first mate versus the song of the second mate using the above procedure. Statistical Analysis The present analysis focuses on incidence of responding (i.e. number of birds showing a preference for one song over the other), latency of approach (i.e. the time elapsing between the raising of the guillotine door and the female entering an approach zone), and duration of approach (i.e. the total amount of time spent in each approach zone in the 30-min trial). Mean latencies and durations are based only on those animals that responded. If an animal approached only one song, it was assigned a latency score of 1800 s and a duration score of 0 s with respect to the non-approached song, and these figures were involved in the statistical analysis and in the computation of the means in Tables I and II. Incidences of responding were assessed by the &i-square one-sample test, and latency and duration scores (in seconds) were evaluated by the Mann-Whitney U-test employing the cor-
27,
2
rection factor for tied ranks (Siegel 1956). All probability values are 2-tailed. ReSUltS As shown in Fig. 2, female zebra finches had a significant preference for the song of their mate versus the song of a neighbour (~2 = 9.0, P < 0.01, df = 1). Three females showed no preference in #at they spent about as much time in one approach zone as in the other, and one female preferred neither song in that she remained inside the start box during the entire 30-min trial. As shown in Table I, there was a non-significant trend for females to have shorter latencies of approach to their mate’s song versus a neighbour’s song. However, females spent significantly more time in their mate’s approach zone than in the neighbour’s approach zone (P --c 0401). In the present context, duration scores are probably more valid measures of preference than latency scores in that several females were apparently startled by the raising of the start box guillotine door and flew quickly out of the start box. They often landed in the approach zone adjacent to the speaker broadcasting the neighbour’s song, and then immediately or eventually flew to the other approach zone broadcasting their mate’s song where they would remain for the rest of the trial. 167 co l4 !fi
12.
; u. L 0
lo-
$j
6:
i
4-
=
2-
8-
~ I
MATE
I
l---l
I
I
r-l
I
NEIGHBOUR
BOTH
I
I NEITHER
PREFERENCE
Fig. 2. Number of females preferring the song of their
mate, the song of their neighbour, both songs equally, and neither song (i.e. non-responders) in simultaneous auditory choice tests.
MILLER:
ZEBRA
FINCH
Of the six females that successfully met the criterion of having formed a new pair bond with a second male, three preferred the hrst mate, two preferred the second mate, and one did not respond; thus, there was no significant preference for one mate over the other. However, as shown in Table II, females had a significantly shorter latency to the song of the first mate than to the song of the second mate (P < O-02), while differences in duration scores were nonsignificant. Although the sample size is small, it would appear that some females are capable of remembering and preferring the song of their first mate to the song of their second mate. However, teasing apart primacy versus recency effects in the context of mate recognition necessitates a larger sample of successful rematings than is achieved in the present study. Discussion These data provide experimental evidence for one functional aspect of male zebra finch song by showing that females learn the song of their mate and respond preferentially to it following a period of separation. Thus, as previously suggested by other investigators (Morris 1954; Immelmann 1965, 1969; Butterfield 1970; Zann 1974), the song of the male can function to strengthen and maintain the pair bond to the extent that the female, using this acoustic stimulus configuration, can recognize and show a preference for her own mate versus neighbouring males. This is not to suggest, however, that song does not serve other functions as well. For example, song may also be involved in mate selection by female zebra finches (Miller in press), as well as having other possible functions. Solitary song, which is identical to directed courtship song in terms of acoustic structure, has been suggested to play a role in pair bond maintenance (Morris 1954; Immelmann 1968). Since, in the field, males have been observed to Table I. Latency and Duration of Response of 16 Female Zebra Finches that Showed a Prekwxe in 30-min Simnltaaeous Auditory Choice Tests Involving tbe Song of their Mate Versus tbe Song of a Neigbbour Latency (s) Test song Mate
Mean 434
Neighbour
SD
Mean
559
1048 P <
NS
VS.
803
Duration
831
349
MATE
RECOGNITION
sing in the area of the nest while visually separated from their incubating mates (Immelmann, personal communication), the present data add further substance to the presumed functional significance of solitary song in maintaining a pair bond. This is insofar as females are capable of recognizing the songs of their own mates. Although only a small number of birds in the present study formed pair bonds with new mates when denied access to their former mates, it is interesting that, upon retesting, each of the females that responded had very short latencies to the song of the first mate versus the song of the second mate (Table II). This is at least suggestive that females are capable of remembering the song of their first mate following very long periods of separation (up to six months in the present study) with intervening exposure to a new mate’s song. It is also suggestive that they have an initial preference for the song of the former mate that may or may not become attenuated during the course of the test session (i.e. three birds remained near the first mate’s song, and two birds switched over to the second mate’s song in terms of approach durations). It is important to recognize that the pair bond is probably maintained by more than song alone. Indeed, others have demonstrated that visual and/or combined audiovisual cues play a role in pair bond maintenance (Morris 1954 ; Butterfield 1970; Caryl 1976). The present study does demonstrate, however, that in the absence of visual cues (as when the male is singing solitary song out of visual range of his incubating mate), song can provide a sufficient basis by which a female can recognize her mate. Acknowledgments This research was conducted while I was supported by a fellowship from the Alexander von Humboldt-Stiftung. I thank Klaus Immelmann for sponsoring my stay in Germany, Table II. Latency and Duration of Response of 5 Female zebra Finches that Sbowed a Prehence in 30411 Simultaneous Auditory Choice Tests Involving tbe Song of their First Mate Versus the Song of their Second Mate Latency (s)
(s) SD
532 0.001 519
319
Test song First mate
Duration
Mean
SD
Mean
26
18
875
764
946
SD
809 NS
P < 0.02
Second mate
(s)
557
687
380
ANIMAL
BEHAVIOUR,
for generously providing full access to his laboratory facilities, and for suggesting this study. I also thank Linda L. Miller for carefully preparing the figures. REFERENCES Beer, C. G. 1970. Individual recognition of voice in the social behavior of birds. In: Advances in rlre Study ofBehavior, Vol. 3 (Ed. by D. S. Lehrman, R. A. Hinde & E. Shaw), pp. 27-74. New York: Academic Press. Butterfield, P. A. 1970. The pair bond in the Zebra finch. In : Social Behaviour in Birds and Mammals: Essays on the Social Ethology of Animals and Man (Ed. by J. H. Crook), pp. 249-278. London: Academic Press. Caryl, P. G. 1976. Sexual behaviour in the zebra f&h Taeniopygia guttata: Response to familiar and novel uartners. Anim. Behav.. 24. 93-107. Collias, E.~C: & Collias, N. E. 1978: N&t building and nesting behaviour of the Sociable Weaver Philetairus socius. Ibis, 120, l-15. Erickson, C. J. 1977. The nature and function of pairbonds. In: Grzimek’s Encyclopedia of Ethology (Ed. by K. Immelmann), pp. 469-486. New York: Van Nostrand Reinhold. Immelmann, K. 1965. Australian Finches in Bush and Aviary. Sydney: Angus and Robertson. Immelmann, K. 1968. Zur biologischen Bedeutung des Estrildidengesanges. J. Ornithol., 109, 284-299. Immelmann, K. 1969. Song development in the zebra finch and other Estrildid finches. In : Bird Vocalizations (Ed. by R. A. Hinde), pp. 61-74. London: Cambridge University Press.
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