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Models for song learning in the zebra finch: fathers or others?
Anita. Behav., 1990, 39, 745-757
Models for song learning in the zebra finch: fathers or others? HEATHER
WILLIAMS*
The Roekefeller University Field Research Center for Ethology and Ecology, Millbrook, NY 12545, U.S.A.
Abstract. Previous research with individually caged breeding pairs of zebra finches, Taenopygia guttata, led to the conclusion that young males imprint upon their fathers at an early age, and model their songs upon their fathers' songs. In this study, an aviary containing 10 breeding pairs of zebra finches and two non-breeding males was observed while the offspring were raised to independence. The young remained in the colony until sexual maturity (90 days), when song learning is complete. The songs of young males and their putative fathers were then analysed and compared. The mean number of syllables in the sons' songs was greater than the number in the fathers' songs. Portions of each adult male's song were copied by at least one young male, but sons did not preferentially copy their putative fathers' songs. The majority of the sons copied syllables from at least two of the adult males in the parental population. Two adult males were chosen as song models by a disproportionate number of young males; these two adult males had a greater number of interactions with fledglings and gave a greater amount of parental care to fledglings (including those that were not their own) than did the other adult males in the colony. Young male zebra finches reared in a colonial environment are not restricted to one song model, but may instead make choices about which adult males to copy and, hence, how to represent themselves through their own songs. Likewise, adult males may be able to pass on their songs without successfully reproducing.
Song learning in zebra finches, Taenopygia guttata, has been the subject of many anatomical, physiological and hormonal studies (Williams, 1990). Zebra finch song has also been studied in the context of imprinting (Immelmann 1972; ten Cate 1982), mate choice (Miller 1979a) and pair-bond formation (Silcox & Evans 1982). These studies discuss the role of learned song and its neural substrates in terms of information derived from laboratory studies of song acquisition. Zebra finches are thought to learn their songs only from their fathers/foster fathers (Immelmann 1969; B6hner 1983) or, if young males are separated at an early age from their fathers, from adult males whose song resembles that of their fathers (Clayton 1987). Conclusions based upon these laboratory results are often further extrapolated to form inferences about the behavioural ecology (at present unknown) of wild zebra finches (Miller 1979b; Slater & Clements 1981). Because zebra finches fledge by day 21 (Immelmann 1965, 1969) and the sensitive period for song learning in the zebra finch can extend past 40 days (Eales 1985; Clayton 1987), it seems possible that young zebra finches, living in the *Present address: Department of Biology, Williams College, Williamstown, MA 01267, U.S.A. 0003 3472/90/040745+13 $03.00/0
social environment of the breeding colony, might acquire song models from adults other than their father. In previous studies, however, young male zebra finches learned only their father's song. When B6hner (1983) gave young male zebra finches the choice between their fathers and other males as song models, the young males learned only song elements sung by their fathers. Clayton (1987) exposed fledgling male zebra finches to two adult males, singing different songs, one of which was similar to the father's song; the young males chose the song most similar to their father's as the model for song learning. In both of these studies, however, the social environment of the young zebra finches was restricted: young males were raised to fledging (or later) in cages containing only one pair of adult zebra finches, the parents. Physical access to conspecifics was also restricted after fledging: in B6hner's (1983) study, young males were housed in separate cages adjacent to the adult pairs' cages, and in Clayton's (1987) study, no adult females were present. Zebra finches are highly social, colonial breeders; restricting physical access to conspecifics before and after fledging is not natural, and may strongly influence song learning. The present report focuses upon choices of song models by young male zebra finches raised in a naturalistic, colonial environment.
9 1990 The Association for the Study of Animal Behaviour 745
Animal Behaviour, 39, 4
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METHODS Subjects The subjects were 12 colour-banded adult male zebra finches whose songs had previously been recorded and 11 colour-banded adult female zebra finches (one female died during the course of the study). All adults were obtained from commercial breeders or from an in-house breeding programme, and had not bred previously. None of the adults used were siblings, and none of the females had ever been previously housed with any of the males. Breeding males were recorded (see below) before they were introduced into the aviary.
Aviary Conditions An enclosed indoor aviary measuring 4 x 2 . 5 x 2 m was maintained on a 12:12h light: dark cycle and provided with 12 nestboxes, a large number of perches, nesting material, and water and seed ad libitum. The aviary environment allowed the zebra finches to interact freely, as would be the case in a wild population: contact between young males, their siblings and adults was not restricted by wire, sound isolation or separation before maturity. The first egg was laid 7 days after the adults were introduced into the aviary, and the first hatch followed 14 days later. The first clutches of each of the 10 nesting pairs were used in this study: 35 young were produced, of which 16 were males. These males hatched over a period spanning 31 days (all but two hatched within a 10-day period). The young remained in the colony until they reached sexual maturity (90 days), when they were removed. At this time, the males' songs are crystallized, and show the stereotypy that characterizes adult song (Immelmann 1969; Price 1979).
Behavioural Observations Pairings, nest sites and the dates of egg laying, hatching and fledging were recorded. The male associated with a nestbox was termed the 'father' of all young hatched in that box. Paternity can only be putative, given that egg dumping and extra-pair copulations may have occurred. However, the probability that the putative father was indeed the father is probably high: in an aviary environment similar to that used in this study, only 5.6% of the offspring were confirmed to have extra-pair paternity (Birkhead et al. 1988).
Focal-nest sampling was used to record interactions between adults and nestlings during daily observation periods. Each brood of young was banded with a distinctive colour as nestlings. After fledging, all but two broods (one of which hatched 23 days later than the others)joined a crSche which was formed within a restricted area of the aviary (see Immelmann 1965). The concentration of fledglings within the crSche made it possible to record all interactions between adults and fledglings during daily 30-min observation periods that alternated between morning and evening feeding periods (see Zann 1984). Adults were easily identifiable, although in some cases fledgling identity could not be determined due to crowding around adults in the crSche. Behavioural observations were discontinued when fledglings reached 40 days of age; at this time adults were re-nesting and no longer fed or associated with the young, and the sensitive period for song learning had closed (Immehnann 1969; Price 1979; Eales 1985). Behaviour directed by adults to fledglings were classified as (1) parental: feeding, preening, clumping (perching together in close contact), defending; (2) aggressive: chasing, pecking; or (3) other: mounting.
Song Recording Songs were recorded at 33ips on Scotch Dynarange tape with a Tandberg Series 15 reel-toreel recorder. Males were caged individually for up to a week before being recorded, but were never housed out of sight of females. At the time of recording, they were moved to a separate room and placed near a microphone; a separate cage containing a female was then placed immediately adjacent to the male's cage. The procedure invariably elicited song within 5 rain; most males sang to the female within a few seconds. At least 10 song bouts were recorded; males that were not ready singers were recorded on two separate occasions. All songs used in this study were 'directed song', the song type used in courtship (Sossinka & B6hner 1980).
Song Analysis A Kay Digital Sonagraph was used to plot sonagrams of the songs of the 28 male zebra finches (12 'fathers' and 16 'sons') used in the study. The identities of the singers were not matched to their songs until the analysis was complete. Songs were divided into syllables and analysed at that level. A syllable was defined as a sound unit
Williams: Models for zebra finch song learning lasting at least 30 ms, consisting of related frequency components, and separated from its neighbours by a silent period of at least 10 ms or by an abrupt frequency transition. This definition broke song into units, or syllables, that corresponded to the units that appeared to be learned by young males independently of the preceding or following song units. Two aspects of the song were analysed: the phonology of individual syllables and the sequence (or order) of similar syllables within different songs. Zebra finch song consists of a short (0'5-1"5 s) series of syllables delivered in a consistently stereotyped order (Price 1979; Sossinka & B6hner 1980). Several lines of evidence suggest that bird songs consisting of identical syllables delivered in different orders cannot be considered identical songs: song dialects differing only in syllable order have been described in the swamp sparrow, Melospiza georgiana (Marler & Pickert 1984); the pattern in which syllables are delivered affects the response to songs played back to song sparrows, Melospiza melodia (Searcy et al. 198l); and two components from a song of the white-crowned sparrow, Zonotrichia leucophrys, activate song centre neurons only when presented in the correct order (Margoliash 1983). The analysis used in this study weighted the ordering of the syllables and the syllable structure equally. Song data presented here were scored by the author. Subsets of the data (chosen at random) were also scored for phonology by two colleagues, one familiar with zebra finch song and the other naive in song analysis. The agreement between scorers was high: 93% of the syllables scored by the experienced scorer (and 76 % of those scored by the naive scorer) corresponded to the scores given by the author. The songs of the 16 young males were compared with each other and with the 12 adult males' songs. For each syllable in a young male's song, the phonologically best-matching syllables in the other male's song were determined first. The strength of the similarity between each syllable pair was scored on a 0-4 scale (0: no similarity; 1: slight similarity; 2: moderate similarity; 3: strong simlarity; 4: identity). Each syllable was then independently matched to the syllable in the adult's song that showed the strongest similarity in sequence, and again assigned a score of 0-4. This sequence score was based upon the similarity of the immediately preceding and following syllables, with reference to
747
their lengths and the interval between them as well as to the syllables' similarity in phonology; for example, a score of 4 indicated that both adjacent syllables closely corresponded to those in the comparison song, while a score of 2 indicated strong correspondence by one adjacent syllable or moderate correspondence by both adjacent syllables. Similarity rankings are an ordinal scale; because the intervals between scores cannot be assumed to be constant, averaged similarity scores cannot be used for statistical comparisons. Therefore, the ordinal scale was reduced to two groups, representing matching and non-matching syllables. Syllable pairs scoring 3 or 4 ('strong similarity' or 'identity') in phonology were considered to be matching or copied syllables. Similarly, syllable pairs scoring 2, 3 or 4 for sequence (i.e. with at least one adjacent syllable in common) were considered to be matching or copied in sequence. For each comparison of two songs, the number of syllable pairs with matching phonology was divided by the total number of syllables in the longer of the two songs (to adjust for differences in song length between two otherwise similar songs). Likewise, the number of syllable pairs with matching sequence was divided by the number of syllables in the longer of the two songs being compared. This procedure yields two measures of song similarity, one for syllable phonology and another for the syllable sequence. The two measures were weighted equally (averaged). This overall measure provides a song similarity index for each comparison of any two songs within the entire population of 28 males (12 fathers, 16 sons). An example of the song scoring procedure and its outcome is shown in Fig. 1. Because some syllables were shared by two or more adult males (with only relatively minor differences in structure or phonology), the scoring system and the overall song similarity measures do not indicate which of these adult males with similar songs provided the model for syllable within a young male's song. As a measure of which adult males provided models for young males' syllables, the best-matching syllable (determined separately for structure and context) from among the entire population of adults' songs was determined for each syllable in every young male's song. If the 'best-matching' model syllable was also a 'matching' syllable in the analysis outlined above, it was considered to be copied from the adult's song; otherwise, it was considered to be improvised. The
748
Animal Behaviour, 39, 4 the importance of an adult male as a model for a young male's song syllables.
(a) RESULTS
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Number of Syllables
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Comparison of Fathers' and Sons' Songs ~ ~',1
.L., ',ii' o
The songs of sons averaged (+sE) 11-75 +0.67 syllables in length, significantly longer (t=24.86, P<0.001) than the fathers' songs, which averaged 9.75 • syllables long. This increase in length was not due to an increase in syllable repetition within the song: when syllable repeats were not included in counts of song length, the difference between the average length of sons' songs (10.69 + 0.50 syllables) as compared with fathers' songs (8-67 -+0.72) remained (t = 26'39, P < 0.001). These results indicate that young males produced longer songs by adding new syllables to a model's song.
mr 0.1 s
Figure 1. Similaritiesbetween the songs of a young male, rwb3 (b), and two adult males, R (a) and OW (c). Adults are designated by upper-case letters corresponding to band colours, and sons are indicated by their fathers' letters in lower-case followed by a number. Syllables in the young male's song scored as matching adult males' syllables in phonology and sequence are connected by a solid line and arrow; those scored only as matching in phonology are connected by a dotted line and arrow (see Methods for a description of the scoring criteria). The song similarity score (see Methods for derivation) for the songs ofrwb3 and R was 0.47; for rwb3 and OW, 0.53; for rwb3 and his father (RWB), 0. I0. The line between 5.5 and 8 kHz shows the amplitude profile of the song.
relative importance of each adult's song as a model was determined by tabulating the number of syllables derived from the adult male's song for (1) each individual young male and (2) the entire population of young males. These two measures define
Analysis of sonagrams of the fathers' and sons' did not support the model of strict father-to-son transmission of song. Figure 1 shows the song of one young male, rwb3, that of his father, RWB (recall that 'father' is defined as the male associated with the nestbox), and that of another adult male, OW, that fledged no young. There is little similarity between the father's and son's song, which appears to have been largely copied from the other male's song. This pattern was typical of the entire population: sons' songs most closely resembled those of adult males that were not their father. The song similarity index (see Methods) was computed for every possible comparison between the 12 adults' and the 16 young males' songs. These measures were grouped into five categories: (1) comparisons between fathers' and sons' songs, (2) between brothers' songs, (3) between unrelated adult males' songs, (4) between unrelated young males' songs, and (5) between young males' songs and unrelated adult males' songs (Table I). Unrelated males had slightly less similar songs than did fathers and their sons or young males and their brothers, and an analysis of variance showed this trend to be significant. Sons' songs were more similar to their fathers' songs than to other adults' songs (Table I). However, this relative similarity might be due to young males copying syllables from songs
Williams." Modelsfor zebrafinch song learning Table I. Song similarity of male zebra finches' songs as a function of age and kinship (F3~s--4"908, P<0.025 (two-tailed) Average song similarity index* Comparison
,Y
SE
No. of comparisons
Adults/adults Adults/young Young/young Fathers/sons Brothers/brothers
0.138 0.160 0.179 0.306 0.333
0.021 0.015 0.018 0.063 0.063
66 176 105 16 15
rwb2 I OW rwb5 y2 RWB 0 R db2 LG
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y ~-
dbl rl wl LB DB yJ RW W
by3 *The maximum song similarity index, corresponding to two songs identical in syllable phonology, number and sequence, is 1.00. similar to those of their fathers. According to the overall song similarity measure, the greatest resemblance between classes of songs is that between brothers' songs. The song similarity data for individual males is represented in Fig. 2 as a hierarchical tree derived from a cluster analysis. Fathers' and sons' songs are most often found in separate clusters that join only very distally in the hierarchy (with the exception of BY and his sons), again indicating that sons' songs are more similar to those of unrelated adult males than to those of their fathers. To test specifically whether the father's song served as the primary model for a young male zebra finch's song syllables, the distributions of bestmatching syllables derived from fathers' songs and from other males' songs were compared. This hypothesis was tested by tabulating the number of best-matching syllables each young male derived from (1) tile father's song and (2) other males' songs. For each case, the number of syllables in the father's song and in the songs of the remaining 11 adult males was also determined (Table II). When all young males are considered, sons derived a significant number of best-matching syllables from their fathers' songs (y 2 =27.59, df= 1, P<0.001). This result was due to one male's five sons copying his song: the 11 sons of males other than BY copied the syllables sung by their fathers slightly less often than would have been expected by chance, although this trend did not reach significance (X2 = 1.11, df=l, P>0.2). If young males followed a strategy in choosing song models, the nature of that strategy is not shown by these results.
GW rwbl Y by4 ~ ] _ . . _ . . BY Ibl by5 by2 rwl by I
Figure2. Cluster analysis of song similarity.The horizontal distance a line travels before being connected to another line represents the dissimilaritybetween the two birds' songs (or the two clusters of songs). The cluster analysis and diagram were derived from a matrix of song similarity indices for every possible comparison of the 28 males' songs, using the SPSS statistical package, CLUSTER procedure, with squared Euclidean distances and average linkage between groups.
Rare and Common Syllables are not Salient as Models
Certain syllables might have gained salience as models because of their relative abundance (being sung by several adult males), or, conversely, by their rarity (being heard only in the song of one adult male). Among the 113 syllables sung by adult males, 80 different syllables were distinguished (33 syllables were duplicates of syllables within a bird's song or in another song). Some syllables were repeated more than once (see Table III). If salience as a model depended upon the number of times a syllable occurs within the adult song population, syllables with high or low frequences in the adult song population should have been disproportionately represented within the songs of the young males. This.was not the case; the number of times any given syllable was copies in the young males' songs was proportional to the number of times that syllable occurred in adult males' songs (X2 =4.66, df=4, P>0.3). Rare or common syllables within
Animal Behaviour, 39, 4
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Table II. Best-matching syllables derived from the songs of fathers and from the songs of other adult males
Young male
No. syllables from father*
No. syllables from others' songst
No. syllables in father's song
No. syllables in others' songs
byl by2 by3 by4 by5 dbl db2 Ibl rl rwl rwbl rwb2 rwb3 wl yl y2
2 6.5 1.5 11.5 6.5 0.5 1 0 0 4 0 0 0 1 0 0
5.5 2.5 8.5 0.5 1 12.5 12 9.5 11.5 8.5 10 13 14.5 10 7.5 8
11 11 11 11 11 10 10 12 7 6 10 10 10 5 10 10
102 102 102 102 102 103 103 101 106 107 103 103 103 108 103 103
*Number of syllables can be halves or odd because each syllable was scored twice, once for phonology and once for sequence. t N o t all syllables were derived from adult males' songs; some were improvised. 100
Table III, Numbers of syllables repeated within the population of adult males' songs and the frequency with which these syllables were copied by young males No. syllable repeats in adult song population
No. syllable types in adult males' songs
No. copies in young males' songs
1
59 15 3 2 1
97 39 11 6 11
8o 60
ea
2 3 4 7
the adult song p o p u l a t i o n were n o t especially salient as models for y o u n g males' songs.
Some Adult Males' Syllables are Copied Preferentially T h e results described a b o v e seem to indicate t h a t song models were chosen r a n d o m l y f r o m within the adult male population, which would seem to imply t h a t each adult male was equally likely to be chosen as a song model. To test this hypothesis, the distrib u t i o n o f best-matching adult syllable models for the young males' song syllables was analysed (Fig.
OW RWB 0
R LG LB DB RW W Adult male
GW Y
BY
Figure 3. Salience of the adult males' songs as models. For each syllable in the song of every young male, the bestmatching syllable among the adult population was determined. The number of best-matching syllable copies from an adult male's song that scored at least 3 (strong similarity) for phonology is shown by the solid bar. The number of copies of the syllable sequence scoring at least 2 (at least one adjacent syllable in common) is shown by the open bar. 3). Syllables from each adult male's song were copies by y o u n g males, but three o f the 12 adult males, L G , B Y a n d OW, were models for 62% of the syllables t h a t were copied from the adult population (106 o f 170 total syllable copies). This distrib u t i o n differed significantly from the distribution expected if song syllable models were chosen without reference to the male t h a t sang t h e m
Williams: Models for zebrafinch song learning
751
Figure 4. Spatial arrangement of adult song models and their imitators. All nestboxes were attached to one wall of the aviary. Nestboxes occupied and defended by adult males are shown as squares. Two nestboxes were used by two males and are shown as double rectangles (one box was occupied sequentially by two breeding pairs, and the other was contested by two males without a female); one nestbox was not used. Young males are represented by circlesunder the nestboxesin which they hatched, and linesconnect them to the boxes of the adult maleswhose syllablesthey copied. The thickness of the line corresponds to the number of syllablescopied from the adult male as determinedby best-matching syllables(fiveline thicknessescorresponding to I-3.5,3.6-6.0,6.1-8.5,8.5 ll.0, and >ll.0syllabtescopied).Theline thickness of the circlesdenoting young males similarlycorresponds to the number of improvised syllablesin the song.
(/~2 : 101.9, df= 1 t, P < 0.001). The identity of the male singing a syllable dramatically altered the probability that the syllable would be learned by a young male.
Factors Influencing the Salience of a Song Model Although the number of males present made it difficult to quantify song rates and song delivery locations, adult males often sang within or immediately outside their nestboxes, and nestboxes were the only area defended from other males. Young male zebra finches might have learned the songs of adult males occupying neighbouring nestboxes. Figure 4 maps the nestbox locations of the young males and the nestboxes of the adult males from which they learned song syllables. The similarity between an adult and a young male's songs was not related to the linear distance between their nestboxes (r=0'16). However, there may be a brooddependent effect for the young of RWB: this male sequestered his young near their nestbox (see Fig. 4) after fledging and kept them separate from the creche that the other fledglings formed at the opposite end of the aviary (see Immelmann 1965).
The three sons of RWB copied 86% of the syllables in their songs from three nearest neighbour males, OW, Y and R (see Figs 4 and 1) and did not incorporate any syllables from RWB's song into their own song. A multiple regression was performed on the number of syllable copies drawn from each adult male song tutor and 14 behavioural, physical and song measures of those males (Table IV). The only adult male characteristics that correlated significantly (P < 0.05) with an adult male's prominence as a model for learned song were the male's total number of interactions with all fledglings and the amount of parental care a male delivered to all fledglings; the correlation to song length approached significance. Such characteristics as aggressive behaviour, song repetitiveness and breeding success (as measured by date of first egg laying, hatching, number of fledglings and number of male fledglings) did not predict an adult male's salience as a song model. Parental care given to fledglings composed 83% of the interactions between all adults (males and females) and fledglings. Males provided 91% of the parental care; most females began re-nesting soon
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Table IV. Regression on adultmales' song, physical and behavioural characteristics and their salience as song models Regression on syllables copied r 2
Adult male characteristic Interactions with fledglings Parental care No. syllables in song Leg band colour~ No. non-repeated syllables in song % Total population syllables in song % Non-repeated syllables in song No. males fledged % Song syllables shared with other adults Date of first egg Aggression to fledglings Date of first hatch No. song syllables shared with other adults No. young fledged
r
0.63* 0.58*
(adjustedt)
- 0.41
0.34 0.27 0.24 0.09
0.41
0.09
0.40
0.07
- 0.38 0.35
0.06 0.03
- 0.34 -0.31 0.27 -0.27
0.03 0.01 -0.02 -0.02
- 0.14 - 0.08
- 0.08 - 0.09
0.55
*Significant at the P < 0.05 level (F-test, df= 11). tr 2 was adjusted for sample size and the number of coefficients in the regression equation. :~A measure for leg band colour was derived by rating leg bands on a scale of - 3 to + 3 for the attractiveness or their colours according to Burley et al. (1982). This characteristic was negatively, but not significantly, correlated to an adult male's salience as a song tutor.
after the young fledged. Females provided parental care only to their own young, while males' parental care, which consisted primarily of feeding, was given indiscriminately to all young: 11% of adult males' interactions with fledglings took place between fathers and sons. RWB, the adult male that kept his young segregated from the creche, was the only male that exclusively cared for the fledglings from his own nestbox. Some mated males without fledglings of their own fed and preened young assiduously; notable among these was LG, whose three hatchlings died before fledging. The overall distribution of parental care given by males did not differ from the level expected if males had failed to discriminate between their own and others' young (Z2=15.46, d f = l l , P>0-10).
Paternal care to fledglings was primarily feeding (87% of all behavioural interactions between adult males and fledglings). Lack of discrimination in the object of paternal care was reflected by the feedingrelated behaviour of the young; fledglings approached, gave begging calls and assumed the typical begging posture in response to any male landing nearby. A male feeding fledglings was immediately surrounded by as many as nine young, and those that gained positions nearest the male were fed. Begging usually ceased only when the male left the creche area.
Songs are Copied from Multiple Models In the aviary environment, young zebra finches were able to hear and interact with several adult males, and m a n y young males modelled their syllables upon those of more than one adult male (see Fig. 1). The number of adult males that formed the model for either the phonology or sequence of at least one best-matching syllable copy in each young male's song was counted. Syllables in some young males' songs had no models among the adult males' songs; in these cases, improvisation was counted as the source for that syllable. Only one young male had a single source for his song; the median number of sources for song syllables was 4.5 and the median number of adult song models copied by a young male was 3.5 (Fig. 5a). Because the scoring process may have resulted in an overestimation of the number of models contributing to a young male's song for some cases (a single syllable could be counted as best matching the phonology in one song and the sequence in another), the number of sources contributing to 10% or more of the young male's songs was also tabulated (Fig. 5b). Using these more stringent criteria, a median of two song models and two song sources contributed to the syllables forming a young male's song. Six young males (37.5%) derived their songs from three or more sources. Figure 6 shows the relative importance of sources for syllables in the young males' songs. Y o u n g male zebra finches copied an average of 60' 1% of their song syllables from a primary song model sung by an adult male. Other models contributed 30.4% of the syllables in the young males' songs, and 9-5% of the syllables sung by the 16 young males were improvised (Fig. 6). The four most important song sources (primary, secondary and tertiary adult male song models, plus improvisation) accounted
Williams. Models for zebra finch song learning
753
DISCUSSION
Issues of Relatedness
z
0
I
2
4
:3
5
6
7
8
9
Number of models and sources contributing to the song I0 ! .
(b)
g
~6 "6
z 2~
0
I
2
:3
4
Number of models ond sources contributing to the song
Figure5. Derivation of syllablesin young males' songs. (a) Total number of sources contributing to a young male's song. 9 Number of sources (tutors plus improvisation) that contributed to the song; []: number of song models from which syllableswere copied. (b) Number of sources contributing to more than 10% of a young male's song. 9 Number of sources that contributed to more than 10% of the song syllables; []: number of adult song models from which more than 10% of the syllables in the song were copied.
120 IOC
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E= 4o z 20
2~
3~
4~
5~
6~
7~
8 ~ ImprovisGtion
Source of syllobles in young moles' songs
Figure 6. The percentage of young males' songs derived from primary, secondary, etc. song models and from improvisation. for 93' 1% of all the syllables sung by young males. Multiple sources for young males' songs were the rule (87.5% using stringent criteria) rather than the exception.
I have used the term 'father' to refer to the male who defended a nestbox, incubated the eggs, and associated with the female who used the nestbox; 'son' in speaking of the males hatched and raised in their 'father's' nestbox; and 'brother' in referring to nestbox mates. It is possible that these terms do not reflect genetic reality, as a low level of extra-pair matings is known to occur among zebra finches in an aviary or colony environment (Birkhead et al. 1988). Other uncontrolled factors may also have affected relatedness: the possibility of brood parasitism cannot be ruled out, and the relatedness of the adult males was unknown (though they were not brothers). However, if the level of extra-pair paternity was similar to that reported by Birkhead et al. (1988), approximately 90% of the young in the colony were sired by their 'fathers'.
Some Model Acquisition Zebra finches, like white-crowned sparrows (Baptista & Morton 1988) and long-billed marsh wrens, Telmatodytes palustris (Kroodsma & Picker 1980), do not necessarily learn their songs from their fathers, but instead appear to evaluate the conspecific song environment before choosing song models. The best predictor of an adult male's salience as a song model was not his putative relationship to a fledgling, the location of his nestboxes or any of a number of song characteristics, but the number of behavioural interactions between that adult male and the fledgling population (see Table III). Feeding, preening and clumping were the main types of interactions between adult males and fledglings, and parental care given by a male to the fledgling population at large was also significantly correlated with his salience as a song model. Behavioural interactions have previously been shown to be important in determining the choice of a song model in zebra finch males raised by Bengalese finch, Lonchura striata, foster fathers (Immelmann 1969; Eales 1987). In this study, aggression was not an important factor in the young males' choice of song models. The importance of parental care as opposed to aggression differs from the relationship between aggression and song model salience reported in indigo buntings, Passerina cyanea (Payne 1981) and
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suggested for groups of zebra finch fledglings caged with adult males (Clayton 1987). The behavioural correlates of a successful song model may differ between colonial (zebra finch) and territorial (indigo bunting) species. Housing conditions may also be important for the normal social correlates of song learning to become manifest; group aviary housing is a more naturalistic environment than small wire cages. Individual variation in quantity and quality of paternal care, and thus a potential basis for differential song model prominence, has been shown in studies that measured male parental investment by zebra finches (ten Cate 1982; Delesalle 1986). Adult males were the primary providers of parental care to fledgling zebra finches in the aviary environment. All but one of the 12 males in this study provided care indiscriminately; upon landing with a full crop in the creche, an adult male was immediately surrounded by begging fledglings and seemingly had little chance to discriminate among the scrambling mass of gapes. The one male (RWB) that cared only for his own young segregated his fledglings near his own nestbox, and hence did not enter the space occupied by the cr6che while providing parental care; his sons primarily copied the songs of two males (OW and Y) competing for and singing near an adjacent nestbox. In the absence of detailed field studies of wild populations of identified zebra finches, it is impossible to resolve the issue of whether wild adult males feed fledglings that are not their own. Indiscriminate feeding may be an artefact of the restricted size of the aviary and the unlimited food supply. However, a combination of factors known to exist in wild finch colonies may well combine to promote indiscriminate feeding of fledglings: (1) Immelmann (1965) described the formation of creches in the social areas of wild finch colonies; (2) the breeding season of Australian zebra finches is triggered by the rainy season and is thus synchronized within the colony (Farner & Serventy 1960); and (3) there are specific times of day during which the adults feed before returning to the colony (Zann & Straw 1984). If young hatch at the same time, congregate in creches and are fed at the same times of day, the environmental conditions promoting indiscriminate feeding in the aviary might also occur in the wild. The issue of helping has not been addressed in zebra finches. If colonial males are normally closely related and do not recognize their own fledglings,
indiscriminate feeding might be a favourable strategy. Another possibility is that adult male zebra finches might have adjusted the amount and discrimination of paternal care they gave to fledglings to their projected paternity of fledglings, as judged by (1) the number of extra-pair matings they had achieved and (2) the extra-pair matings that had been received by their mates. Investment of paternal care has been shown to be predicated upon males' matings in dunnocks, Prunella modularis (Burke et al. 1989). If paternal care in the zebra finch aviary reflects success in gaining extra-pair copulations, it is possible that males were able to recognize their own young raised in the nests of others and feed them after fledging. However, it seems unlikely that males could choose which young to feed, given the competition among young for access to feeding males. Although adult males may have provided more parental care if they obtained more matings and hence become more salient as song models, the increased number of copies of these salient adult songs was most probably not restricted to the young that they sired or could potentially have sired. Song Model Salience and Relatedness A tendency for young males to learn syllables from their fathers' songs was shown by analyses of overall song similarity and of best-matching syllable copies. In both cases, the similarity of fathers' and sons' songs appears to reflect either (1) adult male BY's prominence both as a song tutor and as a father of sons, or (2) a tendency among some young males to copy a song similar to their father's song. Clayton (1987) reported that young males caged with two strange adult males chose the song most similar to their father's as a model. In the aviary, fathers were continually present, and this effect is most probably not important. The salience of adult male BY as a song tutor extended beyond his own five sons (see Fig. 2), one of whom did not copy his song. It may be that the nest father is a less salient song model than are males providing parental care to fledglings, but when the two roles are filled by one male, the song's salience is potentiated. Siblings affect sexual imprinting in zebra finches (Kruijt et al. 1983), and songs of brothers were the most similar of any of the groupings of males compared in Table II. This similarity reflects copying of the same models and not joint improvisation; the
Williams: Models for zebra finch song learning scoring criteria for matching syllables were 'strong similarity' and 'identity', levels unlikely to be reached by improvisation, as judged by comparison with songs generated by birds raised in another aviary. Bonding between siblings may influence song learning either directly, through brothers attending to each others' songs, or indirectly, either because brothers clumped together within the fledgling creche and thus were influenced by the same adult males or because their sisters attended more to some adult males' songs, making those songs in turn more salient models for their brothers. The role of females in guiding zebra finch song learning is not known. The responses of cowbird, Molothrus ater, females to songs affect what young male cowbirds learn (West et al. 1981; King & West 1983). If the responses of adult female zebra finches to the songs of adult males and young males learning their songs influences the song model that is chosen by a young male, studies that present young male zebra finches with adult males as song models in the absence of adult females (e.g. Clayton 1987) may yield results differing from those obtained in a mixed aviary or a colony environment.
Sexual Imprinting and the Sensitive Period for Song Learning Zebra finches are thought to imprint upon their parents or foster parents at an early age (Immelmann 1972; ten Cate et al. 1984). The results reported here support the suggestion that choice of a song model occurs after, and independently of, sexual imprinting (Eales 1985, 1987; Clayton 1988). Young males learned the songs of adult males other than their fathers, and the song they learned was not related to the distance between their own and the model's nest. The sensitive period for song learning must be at its peak during the fledgling period (or even later), since the interactions with adult males of young zebra finches whose sensitive period for song learning was restricted or centered on times before day 21 (fledging) would be restricted to their nests and hence almost exclusively to their fathers in the nest.
Song Length The trend towards longer songs in the young males recalls the observations of Immelmann (1969) and B6hner (1983) that wild zebra finches have
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longer, 'more complex' songs than do domesticated strains. It may be that the song environment of domesticated young zebra finch males (bred in single cages with physical access to only one tutor) is impoverished, and their songs are consequently shorter and tess varied than those of wild or aviaryraised males. In this context, it is interesting to note that song length had a relatively high (nearly significant) correlation with a male's salience as a song model. The three most prominent song models had at least 11 song syllables. If short songs with little syllable variety are indeed impoverished, young males may avoid these songs when choosing a model.
Multiple Models for Zebra Finch Song Young males learned to sing a composite song consisting of portion s of several adults' songs added to their own improvised notes. The majority of young male zebra finches modelled their songs upon those of more than one adult male. Using multiple models for a song may enable a young male to construct a song that is unique and thus serves as an individual signature. However, this rationale is not entirely satisfactory, as an exact copy of a song and a minor variant on another were produced by two of the young males in this sample. Young zebra finch males with physical as well as auditory access to several adult males may model their songs upon those of adult males that are the most salient stimuli because of their interactions with the fledglings. The young males may, in effect, evaluate the behavioural characteristics of the adult males in the population. Young males may then choose to copy adult males' songs based upon an assessment of the parental care given by adult males. Female zebra finches reared in single-pair breeding cages have long-term memories of (and preferences for) the songs of their fathers, and they appear to choose their mates on the basis of song (Miller 1979a, b); hence, the level of parental care given by an adult male to young females may represent a measure of that male's present fitness and future attractiveness to females. The young female zebra finches in the aviary study were exposed to the same paternal care as were the males, and may also have learned to prefer the songs of adult males other than their fathers. If the learned song preferences of young females are based upon the characteristics of the adult males they encounter as fledglings, young males that made the correct
Animal Behaviour, 39, 4
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choice of song models are likely to become preferred mates for females f-rom their cohort. By c o m p o u n d i n g their songs o f syllables or syllable sequences derived from different adult males, young males may, in effect, be covering their bets, by representing themselves as possessing the attractive qualities o f a n u m b e r o f different adult males. W h e n there are multiple models for a young zebra finch's song, at most one o f t h e m c a n have been provided by his genetic father. Syllables derived f r o m the songs o f n o n - p a t e r n a l adult males m u s t then be transmitted independently o f genetic information, t h o u g h there m a y be a n indirect link if a male gaining more extra-pair matings also gives more p a r e n t a l care to fledglings. I n this sense, an adult male zebra finch has a 'cultural fitness' (uncoupled from his 'genetic fitness'), which is d e p e n d e n t u p o n his ability to figure as a model for young males' songs. Multiple song models m a y m a k e zebra finches an interesting system for studying the transmission o f cultural traits.
ACKNOWLEDGMENTS I t h a n k F e r n a n d o N o t t e b o h m a n d Jeffrey Cynx for valuable c o m m e n t s o n the manuscript, Stephen J. C l a r k for advice o n statistical m e t h o d s , a n d Jeffrey Cynx and A n d r e a deMajewski for scoring syllables. This study was s u p p o r t e d by A F O S R g r a n t 86-0336.
REFERENCES Baptista, L. F. & Morton, M. L. 1988. Song learning in montane white-crowned sparrows: from whom and when. Anita. Behav., 36, 1753-1764. Birkhead, T. R., Pellatt, J. & Hunter, F. M. 1988. Extrapair copulation and sperm competition in the zebra finch. Nature, Lond., 334, 60-62. B6hner, J. 1983. Song learning in the zebra finch (Taenopygiaguttata): selectivity in choice of a tutor and accuracy of song copies. AnOn. Behav., 31, 231-237. Burke, T., Davies, N. B., Bruford, M. W. & Hatchwell, B. J. 1989. Parental care and mating behaviour of polyandrous dunnocks Prunella modular& related to paternity by DNA fingerprinting. Nature, Lond., 338, 249-251. Burley, N., Kratzenberg, G. & Radman, P. 1982. Influence of colour-banding on the conspecific preferences of zebra finches. Anita. Behav., 30, 444-455, Clayton, N. S. 1987. Song tutor choice in zebra finches. Anon. Behav., 35, 714-721.
Clayton, N. S. 1988. Song learning and mate choice in estrildid finches raised by two species. Anim. Behav., 36, 1589-1600. Delesalle, V. A. 1986. Division of parental care and reproductive success in the zebra finch (Taenopygia guttata). Behav. Proe., 12, 1-22. Eales, L. A. 1985. Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim. Behav., 33, 1293 1300. Eales, L. A. 1987. Do zebra finch males that have been raised by another species still tend to select a conspecific song tutor? Anita. Behav., 35, 1347-1355. Farner, D. S. & Serventy, D. L. 1960. The timing of reproduction in the arid regions of Australia. Anat. Ree., 137, 354. Immetmann, K. 1965. Australian Finches in Bush and Aviary. Sydney: Angus & Robertson. Immelmann, K. 1969. Song development in the zebra finch and other estrildid finches. In: Bird Vocalizations (Ed. by R. A. Hinde), pp. 61 74. Cambridge: Cambridge University Press. Immelmann, K. 1972. Sexual and other long-term aspects of imprinting in birds and other species. In: Advances in the Study of Behaviour. Vol. 4. (Ed. by D. S. Lehrman, R. A. Hinde & E. Shaw), pp. 147-174. New York: Academic Press. King, A. P. & West, M. J. 1983. Epigenesis of cowbird song: a joint endeavour of males and females. Nature. Lond., 305, 704-706. Kroodsma, D. E. & Pickert, R. 1980. Environmentally dependent sensitive periods for avian vocal learning. Nature, Lond., 288, 477-479. Kruijt, J. P., ten Cate, C. J. & Meeuwissen, G. B. 1983. The influence of siblings on the development of sexual preferences of male zebra finches. Devl Psychobiol., 16, 233-239. Margoliash, D. 1983. Acoustic parameters underlying the responses of song-specific neurons in the whitecrowned sparrow. J. Neurosci., 3, 1039-1057. Marler, P. & Pickert, R. 1984. Species-universal microstructure in the learned song of the swamp sparrow (Melospiza georgiana). Anim. Behav., 32, 673-689. Miller, D. B. 1979a. Long-term recognition of fathers' songs by female zebra finches. Nature, Lond., 280, 389-391. Miller, D. B. 1979b. The acoustic basis of mate recognition by female zebra finches (Taenopygia guttata). AnOn. Behav, 27, 376-380. Payne, R. B. 1981. Song learning and social interactions in indigo buntings. AnOn. Behav., 29, 688-697. Price, P. H. 1979. Developmental determinants of structure in zebra finch song. J. comp. physiol. Psychol., 93, 260-277. Searcy, W. A , Marler, P. & Peters, S. S. 1981. Species song discrimination in adult female song and swamp sparrows. Anita. Behav., 29, 997-1003. Silcox, A. P. & Evans, M. S. 1982. Factors affecting the formation and maintenance of pair bonds in the zebra finch, Taenopygia guttata. Anita. Behav, 30, 1237-1243. Slater, P. J. B. & Clements, F. A. 1981. Incestuous mating in zebra finches. Z. Tierpsychol., 57, 201-208.
Williams; Models for zebra finch song learning Sossinka, R. & B6hner, J. 1980. Song types in the zebra finch (Poephila guttata castanotis). Z. Tierpsychol., 53, 123-132. ten Cate, C. t982. Behavioural differences between zebra finch and bengalese finch (foster) parents raising zebra finch young. Behaviour, 81, 152-172. ten Cate, C., Los, L. & Schilperoord, L. 1984. The influence of differences in social experience on the development of species recognition in the zebra finch. Anita. Behav., 32, 852-860. Williams, H. 1990. Bird song. In: Neurobiology of Comparative Cognition (Ed. by R. E. Kesner & D. S. Olton), pp. 77-126. Hillsdale, New Jersey: Erlbaum.
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West, M. J., King, A. P. & Eastzer, D. H. 1981. Validating the female bioassay of cowbird song: relating differences in song potency to mating success. Anim. Behav., 29, 490-50 I. Zann, R. & Straw, B. 1984. Feeding ecology of zebra finches (Poephila guttata) in Northern Victoria. Austral. Wildl. Res., 11, 533-552.
(Received 9 June 1989; initial acceptance 26 June 1989; final acceptance 10 July 1989; MS. number: A5160)
Models for song learning in the zebra finch: fathers or others? HEATHER
WILLIAMS*
The Roekefeller University Field Research Center for Ethology and Ecology, Millbrook, NY 12545, U.S.A.
Abstract. Previous research with individually caged breeding pairs of zebra finches, Taenopygia guttata, led to the conclusion that young males imprint upon their fathers at an early age, and model their songs upon their fathers' songs. In this study, an aviary containing 10 breeding pairs of zebra finches and two non-breeding males was observed while the offspring were raised to independence. The young remained in the colony until sexual maturity (90 days), when song learning is complete. The songs of young males and their putative fathers were then analysed and compared. The mean number of syllables in the sons' songs was greater than the number in the fathers' songs. Portions of each adult male's song were copied by at least one young male, but sons did not preferentially copy their putative fathers' songs. The majority of the sons copied syllables from at least two of the adult males in the parental population. Two adult males were chosen as song models by a disproportionate number of young males; these two adult males had a greater number of interactions with fledglings and gave a greater amount of parental care to fledglings (including those that were not their own) than did the other adult males in the colony. Young male zebra finches reared in a colonial environment are not restricted to one song model, but may instead make choices about which adult males to copy and, hence, how to represent themselves through their own songs. Likewise, adult males may be able to pass on their songs without successfully reproducing.
Song learning in zebra finches, Taenopygia guttata, has been the subject of many anatomical, physiological and hormonal studies (Williams, 1990). Zebra finch song has also been studied in the context of imprinting (Immelmann 1972; ten Cate 1982), mate choice (Miller 1979a) and pair-bond formation (Silcox & Evans 1982). These studies discuss the role of learned song and its neural substrates in terms of information derived from laboratory studies of song acquisition. Zebra finches are thought to learn their songs only from their fathers/foster fathers (Immelmann 1969; B6hner 1983) or, if young males are separated at an early age from their fathers, from adult males whose song resembles that of their fathers (Clayton 1987). Conclusions based upon these laboratory results are often further extrapolated to form inferences about the behavioural ecology (at present unknown) of wild zebra finches (Miller 1979b; Slater & Clements 1981). Because zebra finches fledge by day 21 (Immelmann 1965, 1969) and the sensitive period for song learning in the zebra finch can extend past 40 days (Eales 1985; Clayton 1987), it seems possible that young zebra finches, living in the *Present address: Department of Biology, Williams College, Williamstown, MA 01267, U.S.A. 0003 3472/90/040745+13 $03.00/0
social environment of the breeding colony, might acquire song models from adults other than their father. In previous studies, however, young male zebra finches learned only their father's song. When B6hner (1983) gave young male zebra finches the choice between their fathers and other males as song models, the young males learned only song elements sung by their fathers. Clayton (1987) exposed fledgling male zebra finches to two adult males, singing different songs, one of which was similar to the father's song; the young males chose the song most similar to their father's as the model for song learning. In both of these studies, however, the social environment of the young zebra finches was restricted: young males were raised to fledging (or later) in cages containing only one pair of adult zebra finches, the parents. Physical access to conspecifics was also restricted after fledging: in B6hner's (1983) study, young males were housed in separate cages adjacent to the adult pairs' cages, and in Clayton's (1987) study, no adult females were present. Zebra finches are highly social, colonial breeders; restricting physical access to conspecifics before and after fledging is not natural, and may strongly influence song learning. The present report focuses upon choices of song models by young male zebra finches raised in a naturalistic, colonial environment.
9 1990 The Association for the Study of Animal Behaviour 745
Animal Behaviour, 39, 4
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METHODS Subjects The subjects were 12 colour-banded adult male zebra finches whose songs had previously been recorded and 11 colour-banded adult female zebra finches (one female died during the course of the study). All adults were obtained from commercial breeders or from an in-house breeding programme, and had not bred previously. None of the adults used were siblings, and none of the females had ever been previously housed with any of the males. Breeding males were recorded (see below) before they were introduced into the aviary.
Aviary Conditions An enclosed indoor aviary measuring 4 x 2 . 5 x 2 m was maintained on a 12:12h light: dark cycle and provided with 12 nestboxes, a large number of perches, nesting material, and water and seed ad libitum. The aviary environment allowed the zebra finches to interact freely, as would be the case in a wild population: contact between young males, their siblings and adults was not restricted by wire, sound isolation or separation before maturity. The first egg was laid 7 days after the adults were introduced into the aviary, and the first hatch followed 14 days later. The first clutches of each of the 10 nesting pairs were used in this study: 35 young were produced, of which 16 were males. These males hatched over a period spanning 31 days (all but two hatched within a 10-day period). The young remained in the colony until they reached sexual maturity (90 days), when they were removed. At this time, the males' songs are crystallized, and show the stereotypy that characterizes adult song (Immelmann 1969; Price 1979).
Behavioural Observations Pairings, nest sites and the dates of egg laying, hatching and fledging were recorded. The male associated with a nestbox was termed the 'father' of all young hatched in that box. Paternity can only be putative, given that egg dumping and extra-pair copulations may have occurred. However, the probability that the putative father was indeed the father is probably high: in an aviary environment similar to that used in this study, only 5.6% of the offspring were confirmed to have extra-pair paternity (Birkhead et al. 1988).
Focal-nest sampling was used to record interactions between adults and nestlings during daily observation periods. Each brood of young was banded with a distinctive colour as nestlings. After fledging, all but two broods (one of which hatched 23 days later than the others)joined a crSche which was formed within a restricted area of the aviary (see Immelmann 1965). The concentration of fledglings within the crSche made it possible to record all interactions between adults and fledglings during daily 30-min observation periods that alternated between morning and evening feeding periods (see Zann 1984). Adults were easily identifiable, although in some cases fledgling identity could not be determined due to crowding around adults in the crSche. Behavioural observations were discontinued when fledglings reached 40 days of age; at this time adults were re-nesting and no longer fed or associated with the young, and the sensitive period for song learning had closed (Immehnann 1969; Price 1979; Eales 1985). Behaviour directed by adults to fledglings were classified as (1) parental: feeding, preening, clumping (perching together in close contact), defending; (2) aggressive: chasing, pecking; or (3) other: mounting.
Song Recording Songs were recorded at 33ips on Scotch Dynarange tape with a Tandberg Series 15 reel-toreel recorder. Males were caged individually for up to a week before being recorded, but were never housed out of sight of females. At the time of recording, they were moved to a separate room and placed near a microphone; a separate cage containing a female was then placed immediately adjacent to the male's cage. The procedure invariably elicited song within 5 rain; most males sang to the female within a few seconds. At least 10 song bouts were recorded; males that were not ready singers were recorded on two separate occasions. All songs used in this study were 'directed song', the song type used in courtship (Sossinka & B6hner 1980).
Song Analysis A Kay Digital Sonagraph was used to plot sonagrams of the songs of the 28 male zebra finches (12 'fathers' and 16 'sons') used in the study. The identities of the singers were not matched to their songs until the analysis was complete. Songs were divided into syllables and analysed at that level. A syllable was defined as a sound unit
Williams: Models for zebra finch song learning lasting at least 30 ms, consisting of related frequency components, and separated from its neighbours by a silent period of at least 10 ms or by an abrupt frequency transition. This definition broke song into units, or syllables, that corresponded to the units that appeared to be learned by young males independently of the preceding or following song units. Two aspects of the song were analysed: the phonology of individual syllables and the sequence (or order) of similar syllables within different songs. Zebra finch song consists of a short (0'5-1"5 s) series of syllables delivered in a consistently stereotyped order (Price 1979; Sossinka & B6hner 1980). Several lines of evidence suggest that bird songs consisting of identical syllables delivered in different orders cannot be considered identical songs: song dialects differing only in syllable order have been described in the swamp sparrow, Melospiza georgiana (Marler & Pickert 1984); the pattern in which syllables are delivered affects the response to songs played back to song sparrows, Melospiza melodia (Searcy et al. 198l); and two components from a song of the white-crowned sparrow, Zonotrichia leucophrys, activate song centre neurons only when presented in the correct order (Margoliash 1983). The analysis used in this study weighted the ordering of the syllables and the syllable structure equally. Song data presented here were scored by the author. Subsets of the data (chosen at random) were also scored for phonology by two colleagues, one familiar with zebra finch song and the other naive in song analysis. The agreement between scorers was high: 93% of the syllables scored by the experienced scorer (and 76 % of those scored by the naive scorer) corresponded to the scores given by the author. The songs of the 16 young males were compared with each other and with the 12 adult males' songs. For each syllable in a young male's song, the phonologically best-matching syllables in the other male's song were determined first. The strength of the similarity between each syllable pair was scored on a 0-4 scale (0: no similarity; 1: slight similarity; 2: moderate similarity; 3: strong simlarity; 4: identity). Each syllable was then independently matched to the syllable in the adult's song that showed the strongest similarity in sequence, and again assigned a score of 0-4. This sequence score was based upon the similarity of the immediately preceding and following syllables, with reference to
747
their lengths and the interval between them as well as to the syllables' similarity in phonology; for example, a score of 4 indicated that both adjacent syllables closely corresponded to those in the comparison song, while a score of 2 indicated strong correspondence by one adjacent syllable or moderate correspondence by both adjacent syllables. Similarity rankings are an ordinal scale; because the intervals between scores cannot be assumed to be constant, averaged similarity scores cannot be used for statistical comparisons. Therefore, the ordinal scale was reduced to two groups, representing matching and non-matching syllables. Syllable pairs scoring 3 or 4 ('strong similarity' or 'identity') in phonology were considered to be matching or copied syllables. Similarly, syllable pairs scoring 2, 3 or 4 for sequence (i.e. with at least one adjacent syllable in common) were considered to be matching or copied in sequence. For each comparison of two songs, the number of syllable pairs with matching phonology was divided by the total number of syllables in the longer of the two songs (to adjust for differences in song length between two otherwise similar songs). Likewise, the number of syllable pairs with matching sequence was divided by the number of syllables in the longer of the two songs being compared. This procedure yields two measures of song similarity, one for syllable phonology and another for the syllable sequence. The two measures were weighted equally (averaged). This overall measure provides a song similarity index for each comparison of any two songs within the entire population of 28 males (12 fathers, 16 sons). An example of the song scoring procedure and its outcome is shown in Fig. 1. Because some syllables were shared by two or more adult males (with only relatively minor differences in structure or phonology), the scoring system and the overall song similarity measures do not indicate which of these adult males with similar songs provided the model for syllable within a young male's song. As a measure of which adult males provided models for young males' syllables, the best-matching syllable (determined separately for structure and context) from among the entire population of adults' songs was determined for each syllable in every young male's song. If the 'best-matching' model syllable was also a 'matching' syllable in the analysis outlined above, it was considered to be copied from the adult's song; otherwise, it was considered to be improvised. The
748
Animal Behaviour, 39, 4 the importance of an adult male as a model for a young male's song syllables.
(a) RESULTS
w
II h
o
Number of Syllables
! -'
-1//1,
0
V
J
,l,d kkkl-ll,;i
.17_
Z_UI
~ m
Comparison of Fathers' and Sons' Songs ~ ~',1
.L., ',ii' o
The songs of sons averaged (+sE) 11-75 +0.67 syllables in length, significantly longer (t=24.86, P<0.001) than the fathers' songs, which averaged 9.75 • syllables long. This increase in length was not due to an increase in syllable repetition within the song: when syllable repeats were not included in counts of song length, the difference between the average length of sons' songs (10.69 + 0.50 syllables) as compared with fathers' songs (8-67 -+0.72) remained (t = 26'39, P < 0.001). These results indicate that young males produced longer songs by adding new syllables to a model's song.
mr 0.1 s
Figure 1. Similaritiesbetween the songs of a young male, rwb3 (b), and two adult males, R (a) and OW (c). Adults are designated by upper-case letters corresponding to band colours, and sons are indicated by their fathers' letters in lower-case followed by a number. Syllables in the young male's song scored as matching adult males' syllables in phonology and sequence are connected by a solid line and arrow; those scored only as matching in phonology are connected by a dotted line and arrow (see Methods for a description of the scoring criteria). The song similarity score (see Methods for derivation) for the songs ofrwb3 and R was 0.47; for rwb3 and OW, 0.53; for rwb3 and his father (RWB), 0. I0. The line between 5.5 and 8 kHz shows the amplitude profile of the song.
relative importance of each adult's song as a model was determined by tabulating the number of syllables derived from the adult male's song for (1) each individual young male and (2) the entire population of young males. These two measures define
Analysis of sonagrams of the fathers' and sons' did not support the model of strict father-to-son transmission of song. Figure 1 shows the song of one young male, rwb3, that of his father, RWB (recall that 'father' is defined as the male associated with the nestbox), and that of another adult male, OW, that fledged no young. There is little similarity between the father's and son's song, which appears to have been largely copied from the other male's song. This pattern was typical of the entire population: sons' songs most closely resembled those of adult males that were not their father. The song similarity index (see Methods) was computed for every possible comparison between the 12 adults' and the 16 young males' songs. These measures were grouped into five categories: (1) comparisons between fathers' and sons' songs, (2) between brothers' songs, (3) between unrelated adult males' songs, (4) between unrelated young males' songs, and (5) between young males' songs and unrelated adult males' songs (Table I). Unrelated males had slightly less similar songs than did fathers and their sons or young males and their brothers, and an analysis of variance showed this trend to be significant. Sons' songs were more similar to their fathers' songs than to other adults' songs (Table I). However, this relative similarity might be due to young males copying syllables from songs
Williams." Modelsfor zebrafinch song learning Table I. Song similarity of male zebra finches' songs as a function of age and kinship (F3~s--4"908, P<0.025 (two-tailed) Average song similarity index* Comparison
,Y
SE
No. of comparisons
Adults/adults Adults/young Young/young Fathers/sons Brothers/brothers
0.138 0.160 0.179 0.306 0.333
0.021 0.015 0.018 0.063 0.063
66 176 105 16 15
rwb2 I OW rwb5 y2 RWB 0 R db2 LG
749
y ~-
dbl rl wl LB DB yJ RW W
by3 *The maximum song similarity index, corresponding to two songs identical in syllable phonology, number and sequence, is 1.00. similar to those of their fathers. According to the overall song similarity measure, the greatest resemblance between classes of songs is that between brothers' songs. The song similarity data for individual males is represented in Fig. 2 as a hierarchical tree derived from a cluster analysis. Fathers' and sons' songs are most often found in separate clusters that join only very distally in the hierarchy (with the exception of BY and his sons), again indicating that sons' songs are more similar to those of unrelated adult males than to those of their fathers. To test specifically whether the father's song served as the primary model for a young male zebra finch's song syllables, the distributions of bestmatching syllables derived from fathers' songs and from other males' songs were compared. This hypothesis was tested by tabulating the number of best-matching syllables each young male derived from (1) tile father's song and (2) other males' songs. For each case, the number of syllables in the father's song and in the songs of the remaining 11 adult males was also determined (Table II). When all young males are considered, sons derived a significant number of best-matching syllables from their fathers' songs (y 2 =27.59, df= 1, P<0.001). This result was due to one male's five sons copying his song: the 11 sons of males other than BY copied the syllables sung by their fathers slightly less often than would have been expected by chance, although this trend did not reach significance (X2 = 1.11, df=l, P>0.2). If young males followed a strategy in choosing song models, the nature of that strategy is not shown by these results.
GW rwbl Y by4 ~ ] _ . . _ . . BY Ibl by5 by2 rwl by I
Figure2. Cluster analysis of song similarity.The horizontal distance a line travels before being connected to another line represents the dissimilaritybetween the two birds' songs (or the two clusters of songs). The cluster analysis and diagram were derived from a matrix of song similarity indices for every possible comparison of the 28 males' songs, using the SPSS statistical package, CLUSTER procedure, with squared Euclidean distances and average linkage between groups.
Rare and Common Syllables are not Salient as Models
Certain syllables might have gained salience as models because of their relative abundance (being sung by several adult males), or, conversely, by their rarity (being heard only in the song of one adult male). Among the 113 syllables sung by adult males, 80 different syllables were distinguished (33 syllables were duplicates of syllables within a bird's song or in another song). Some syllables were repeated more than once (see Table III). If salience as a model depended upon the number of times a syllable occurs within the adult song population, syllables with high or low frequences in the adult song population should have been disproportionately represented within the songs of the young males. This.was not the case; the number of times any given syllable was copies in the young males' songs was proportional to the number of times that syllable occurred in adult males' songs (X2 =4.66, df=4, P>0.3). Rare or common syllables within
Animal Behaviour, 39, 4
750
Table II. Best-matching syllables derived from the songs of fathers and from the songs of other adult males
Young male
No. syllables from father*
No. syllables from others' songst
No. syllables in father's song
No. syllables in others' songs
byl by2 by3 by4 by5 dbl db2 Ibl rl rwl rwbl rwb2 rwb3 wl yl y2
2 6.5 1.5 11.5 6.5 0.5 1 0 0 4 0 0 0 1 0 0
5.5 2.5 8.5 0.5 1 12.5 12 9.5 11.5 8.5 10 13 14.5 10 7.5 8
11 11 11 11 11 10 10 12 7 6 10 10 10 5 10 10
102 102 102 102 102 103 103 101 106 107 103 103 103 108 103 103
*Number of syllables can be halves or odd because each syllable was scored twice, once for phonology and once for sequence. t N o t all syllables were derived from adult males' songs; some were improvised. 100
Table III, Numbers of syllables repeated within the population of adult males' songs and the frequency with which these syllables were copied by young males No. syllable repeats in adult song population
No. syllable types in adult males' songs
No. copies in young males' songs
1
59 15 3 2 1
97 39 11 6 11
8o 60
ea
2 3 4 7
the adult song p o p u l a t i o n were n o t especially salient as models for y o u n g males' songs.
Some Adult Males' Syllables are Copied Preferentially T h e results described a b o v e seem to indicate t h a t song models were chosen r a n d o m l y f r o m within the adult male population, which would seem to imply t h a t each adult male was equally likely to be chosen as a song model. To test this hypothesis, the distrib u t i o n o f best-matching adult syllable models for the young males' song syllables was analysed (Fig.
OW RWB 0
R LG LB DB RW W Adult male
GW Y
BY
Figure 3. Salience of the adult males' songs as models. For each syllable in the song of every young male, the bestmatching syllable among the adult population was determined. The number of best-matching syllable copies from an adult male's song that scored at least 3 (strong similarity) for phonology is shown by the solid bar. The number of copies of the syllable sequence scoring at least 2 (at least one adjacent syllable in common) is shown by the open bar. 3). Syllables from each adult male's song were copies by y o u n g males, but three o f the 12 adult males, L G , B Y a n d OW, were models for 62% of the syllables t h a t were copied from the adult population (106 o f 170 total syllable copies). This distrib u t i o n differed significantly from the distribution expected if song syllable models were chosen without reference to the male t h a t sang t h e m
Williams: Models for zebrafinch song learning
751
Figure 4. Spatial arrangement of adult song models and their imitators. All nestboxes were attached to one wall of the aviary. Nestboxes occupied and defended by adult males are shown as squares. Two nestboxes were used by two males and are shown as double rectangles (one box was occupied sequentially by two breeding pairs, and the other was contested by two males without a female); one nestbox was not used. Young males are represented by circlesunder the nestboxesin which they hatched, and linesconnect them to the boxes of the adult maleswhose syllablesthey copied. The thickness of the line corresponds to the number of syllablescopied from the adult male as determinedby best-matching syllables(fiveline thicknessescorresponding to I-3.5,3.6-6.0,6.1-8.5,8.5 ll.0, and >ll.0syllabtescopied).Theline thickness of the circlesdenoting young males similarlycorresponds to the number of improvised syllablesin the song.
(/~2 : 101.9, df= 1 t, P < 0.001). The identity of the male singing a syllable dramatically altered the probability that the syllable would be learned by a young male.
Factors Influencing the Salience of a Song Model Although the number of males present made it difficult to quantify song rates and song delivery locations, adult males often sang within or immediately outside their nestboxes, and nestboxes were the only area defended from other males. Young male zebra finches might have learned the songs of adult males occupying neighbouring nestboxes. Figure 4 maps the nestbox locations of the young males and the nestboxes of the adult males from which they learned song syllables. The similarity between an adult and a young male's songs was not related to the linear distance between their nestboxes (r=0'16). However, there may be a brooddependent effect for the young of RWB: this male sequestered his young near their nestbox (see Fig. 4) after fledging and kept them separate from the creche that the other fledglings formed at the opposite end of the aviary (see Immelmann 1965).
The three sons of RWB copied 86% of the syllables in their songs from three nearest neighbour males, OW, Y and R (see Figs 4 and 1) and did not incorporate any syllables from RWB's song into their own song. A multiple regression was performed on the number of syllable copies drawn from each adult male song tutor and 14 behavioural, physical and song measures of those males (Table IV). The only adult male characteristics that correlated significantly (P < 0.05) with an adult male's prominence as a model for learned song were the male's total number of interactions with all fledglings and the amount of parental care a male delivered to all fledglings; the correlation to song length approached significance. Such characteristics as aggressive behaviour, song repetitiveness and breeding success (as measured by date of first egg laying, hatching, number of fledglings and number of male fledglings) did not predict an adult male's salience as a song model. Parental care given to fledglings composed 83% of the interactions between all adults (males and females) and fledglings. Males provided 91% of the parental care; most females began re-nesting soon
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752
Table IV. Regression on adultmales' song, physical and behavioural characteristics and their salience as song models Regression on syllables copied r 2
Adult male characteristic Interactions with fledglings Parental care No. syllables in song Leg band colour~ No. non-repeated syllables in song % Total population syllables in song % Non-repeated syllables in song No. males fledged % Song syllables shared with other adults Date of first egg Aggression to fledglings Date of first hatch No. song syllables shared with other adults No. young fledged
r
0.63* 0.58*
(adjustedt)
- 0.41
0.34 0.27 0.24 0.09
0.41
0.09
0.40
0.07
- 0.38 0.35
0.06 0.03
- 0.34 -0.31 0.27 -0.27
0.03 0.01 -0.02 -0.02
- 0.14 - 0.08
- 0.08 - 0.09
0.55
*Significant at the P < 0.05 level (F-test, df= 11). tr 2 was adjusted for sample size and the number of coefficients in the regression equation. :~A measure for leg band colour was derived by rating leg bands on a scale of - 3 to + 3 for the attractiveness or their colours according to Burley et al. (1982). This characteristic was negatively, but not significantly, correlated to an adult male's salience as a song tutor.
after the young fledged. Females provided parental care only to their own young, while males' parental care, which consisted primarily of feeding, was given indiscriminately to all young: 11% of adult males' interactions with fledglings took place between fathers and sons. RWB, the adult male that kept his young segregated from the creche, was the only male that exclusively cared for the fledglings from his own nestbox. Some mated males without fledglings of their own fed and preened young assiduously; notable among these was LG, whose three hatchlings died before fledging. The overall distribution of parental care given by males did not differ from the level expected if males had failed to discriminate between their own and others' young (Z2=15.46, d f = l l , P>0-10).
Paternal care to fledglings was primarily feeding (87% of all behavioural interactions between adult males and fledglings). Lack of discrimination in the object of paternal care was reflected by the feedingrelated behaviour of the young; fledglings approached, gave begging calls and assumed the typical begging posture in response to any male landing nearby. A male feeding fledglings was immediately surrounded by as many as nine young, and those that gained positions nearest the male were fed. Begging usually ceased only when the male left the creche area.
Songs are Copied from Multiple Models In the aviary environment, young zebra finches were able to hear and interact with several adult males, and m a n y young males modelled their syllables upon those of more than one adult male (see Fig. 1). The number of adult males that formed the model for either the phonology or sequence of at least one best-matching syllable copy in each young male's song was counted. Syllables in some young males' songs had no models among the adult males' songs; in these cases, improvisation was counted as the source for that syllable. Only one young male had a single source for his song; the median number of sources for song syllables was 4.5 and the median number of adult song models copied by a young male was 3.5 (Fig. 5a). Because the scoring process may have resulted in an overestimation of the number of models contributing to a young male's song for some cases (a single syllable could be counted as best matching the phonology in one song and the sequence in another), the number of sources contributing to 10% or more of the young male's songs was also tabulated (Fig. 5b). Using these more stringent criteria, a median of two song models and two song sources contributed to the syllables forming a young male's song. Six young males (37.5%) derived their songs from three or more sources. Figure 6 shows the relative importance of sources for syllables in the young males' songs. Y o u n g male zebra finches copied an average of 60' 1% of their song syllables from a primary song model sung by an adult male. Other models contributed 30.4% of the syllables in the young males' songs, and 9-5% of the syllables sung by the 16 young males were improvised (Fig. 6). The four most important song sources (primary, secondary and tertiary adult male song models, plus improvisation) accounted
Williams. Models for zebra finch song learning
753
DISCUSSION
Issues of Relatedness
z
0
I
2
4
:3
5
6
7
8
9
Number of models and sources contributing to the song I0 ! .
(b)
g
~6 "6
z 2~
0
I
2
:3
4
Number of models ond sources contributing to the song
Figure5. Derivation of syllablesin young males' songs. (a) Total number of sources contributing to a young male's song. 9 Number of sources (tutors plus improvisation) that contributed to the song; []: number of song models from which syllableswere copied. (b) Number of sources contributing to more than 10% of a young male's song. 9 Number of sources that contributed to more than 10% of the song syllables; []: number of adult song models from which more than 10% of the syllables in the song were copied.
120 IOC
-7
8c "5 6O
E= 4o z 20
2~
3~
4~
5~
6~
7~
8 ~ ImprovisGtion
Source of syllobles in young moles' songs
Figure 6. The percentage of young males' songs derived from primary, secondary, etc. song models and from improvisation. for 93' 1% of all the syllables sung by young males. Multiple sources for young males' songs were the rule (87.5% using stringent criteria) rather than the exception.
I have used the term 'father' to refer to the male who defended a nestbox, incubated the eggs, and associated with the female who used the nestbox; 'son' in speaking of the males hatched and raised in their 'father's' nestbox; and 'brother' in referring to nestbox mates. It is possible that these terms do not reflect genetic reality, as a low level of extra-pair matings is known to occur among zebra finches in an aviary or colony environment (Birkhead et al. 1988). Other uncontrolled factors may also have affected relatedness: the possibility of brood parasitism cannot be ruled out, and the relatedness of the adult males was unknown (though they were not brothers). However, if the level of extra-pair paternity was similar to that reported by Birkhead et al. (1988), approximately 90% of the young in the colony were sired by their 'fathers'.
Some Model Acquisition Zebra finches, like white-crowned sparrows (Baptista & Morton 1988) and long-billed marsh wrens, Telmatodytes palustris (Kroodsma & Picker 1980), do not necessarily learn their songs from their fathers, but instead appear to evaluate the conspecific song environment before choosing song models. The best predictor of an adult male's salience as a song model was not his putative relationship to a fledgling, the location of his nestboxes or any of a number of song characteristics, but the number of behavioural interactions between that adult male and the fledgling population (see Table III). Feeding, preening and clumping were the main types of interactions between adult males and fledglings, and parental care given by a male to the fledgling population at large was also significantly correlated with his salience as a song model. Behavioural interactions have previously been shown to be important in determining the choice of a song model in zebra finch males raised by Bengalese finch, Lonchura striata, foster fathers (Immelmann 1969; Eales 1987). In this study, aggression was not an important factor in the young males' choice of song models. The importance of parental care as opposed to aggression differs from the relationship between aggression and song model salience reported in indigo buntings, Passerina cyanea (Payne 1981) and
754
Animal Behaviour, 39, 4
suggested for groups of zebra finch fledglings caged with adult males (Clayton 1987). The behavioural correlates of a successful song model may differ between colonial (zebra finch) and territorial (indigo bunting) species. Housing conditions may also be important for the normal social correlates of song learning to become manifest; group aviary housing is a more naturalistic environment than small wire cages. Individual variation in quantity and quality of paternal care, and thus a potential basis for differential song model prominence, has been shown in studies that measured male parental investment by zebra finches (ten Cate 1982; Delesalle 1986). Adult males were the primary providers of parental care to fledgling zebra finches in the aviary environment. All but one of the 12 males in this study provided care indiscriminately; upon landing with a full crop in the creche, an adult male was immediately surrounded by begging fledglings and seemingly had little chance to discriminate among the scrambling mass of gapes. The one male (RWB) that cared only for his own young segregated his fledglings near his own nestbox, and hence did not enter the space occupied by the cr6che while providing parental care; his sons primarily copied the songs of two males (OW and Y) competing for and singing near an adjacent nestbox. In the absence of detailed field studies of wild populations of identified zebra finches, it is impossible to resolve the issue of whether wild adult males feed fledglings that are not their own. Indiscriminate feeding may be an artefact of the restricted size of the aviary and the unlimited food supply. However, a combination of factors known to exist in wild finch colonies may well combine to promote indiscriminate feeding of fledglings: (1) Immelmann (1965) described the formation of creches in the social areas of wild finch colonies; (2) the breeding season of Australian zebra finches is triggered by the rainy season and is thus synchronized within the colony (Farner & Serventy 1960); and (3) there are specific times of day during which the adults feed before returning to the colony (Zann & Straw 1984). If young hatch at the same time, congregate in creches and are fed at the same times of day, the environmental conditions promoting indiscriminate feeding in the aviary might also occur in the wild. The issue of helping has not been addressed in zebra finches. If colonial males are normally closely related and do not recognize their own fledglings,
indiscriminate feeding might be a favourable strategy. Another possibility is that adult male zebra finches might have adjusted the amount and discrimination of paternal care they gave to fledglings to their projected paternity of fledglings, as judged by (1) the number of extra-pair matings they had achieved and (2) the extra-pair matings that had been received by their mates. Investment of paternal care has been shown to be predicated upon males' matings in dunnocks, Prunella modularis (Burke et al. 1989). If paternal care in the zebra finch aviary reflects success in gaining extra-pair copulations, it is possible that males were able to recognize their own young raised in the nests of others and feed them after fledging. However, it seems unlikely that males could choose which young to feed, given the competition among young for access to feeding males. Although adult males may have provided more parental care if they obtained more matings and hence become more salient as song models, the increased number of copies of these salient adult songs was most probably not restricted to the young that they sired or could potentially have sired. Song Model Salience and Relatedness A tendency for young males to learn syllables from their fathers' songs was shown by analyses of overall song similarity and of best-matching syllable copies. In both cases, the similarity of fathers' and sons' songs appears to reflect either (1) adult male BY's prominence both as a song tutor and as a father of sons, or (2) a tendency among some young males to copy a song similar to their father's song. Clayton (1987) reported that young males caged with two strange adult males chose the song most similar to their father's as a model. In the aviary, fathers were continually present, and this effect is most probably not important. The salience of adult male BY as a song tutor extended beyond his own five sons (see Fig. 2), one of whom did not copy his song. It may be that the nest father is a less salient song model than are males providing parental care to fledglings, but when the two roles are filled by one male, the song's salience is potentiated. Siblings affect sexual imprinting in zebra finches (Kruijt et al. 1983), and songs of brothers were the most similar of any of the groupings of males compared in Table II. This similarity reflects copying of the same models and not joint improvisation; the
Williams: Models for zebra finch song learning scoring criteria for matching syllables were 'strong similarity' and 'identity', levels unlikely to be reached by improvisation, as judged by comparison with songs generated by birds raised in another aviary. Bonding between siblings may influence song learning either directly, through brothers attending to each others' songs, or indirectly, either because brothers clumped together within the fledgling creche and thus were influenced by the same adult males or because their sisters attended more to some adult males' songs, making those songs in turn more salient models for their brothers. The role of females in guiding zebra finch song learning is not known. The responses of cowbird, Molothrus ater, females to songs affect what young male cowbirds learn (West et al. 1981; King & West 1983). If the responses of adult female zebra finches to the songs of adult males and young males learning their songs influences the song model that is chosen by a young male, studies that present young male zebra finches with adult males as song models in the absence of adult females (e.g. Clayton 1987) may yield results differing from those obtained in a mixed aviary or a colony environment.
Sexual Imprinting and the Sensitive Period for Song Learning Zebra finches are thought to imprint upon their parents or foster parents at an early age (Immelmann 1972; ten Cate et al. 1984). The results reported here support the suggestion that choice of a song model occurs after, and independently of, sexual imprinting (Eales 1985, 1987; Clayton 1988). Young males learned the songs of adult males other than their fathers, and the song they learned was not related to the distance between their own and the model's nest. The sensitive period for song learning must be at its peak during the fledgling period (or even later), since the interactions with adult males of young zebra finches whose sensitive period for song learning was restricted or centered on times before day 21 (fledging) would be restricted to their nests and hence almost exclusively to their fathers in the nest.
Song Length The trend towards longer songs in the young males recalls the observations of Immelmann (1969) and B6hner (1983) that wild zebra finches have
755
longer, 'more complex' songs than do domesticated strains. It may be that the song environment of domesticated young zebra finch males (bred in single cages with physical access to only one tutor) is impoverished, and their songs are consequently shorter and tess varied than those of wild or aviaryraised males. In this context, it is interesting to note that song length had a relatively high (nearly significant) correlation with a male's salience as a song model. The three most prominent song models had at least 11 song syllables. If short songs with little syllable variety are indeed impoverished, young males may avoid these songs when choosing a model.
Multiple Models for Zebra Finch Song Young males learned to sing a composite song consisting of portion s of several adults' songs added to their own improvised notes. The majority of young male zebra finches modelled their songs upon those of more than one adult male. Using multiple models for a song may enable a young male to construct a song that is unique and thus serves as an individual signature. However, this rationale is not entirely satisfactory, as an exact copy of a song and a minor variant on another were produced by two of the young males in this sample. Young zebra finch males with physical as well as auditory access to several adult males may model their songs upon those of adult males that are the most salient stimuli because of their interactions with the fledglings. The young males may, in effect, evaluate the behavioural characteristics of the adult males in the population. Young males may then choose to copy adult males' songs based upon an assessment of the parental care given by adult males. Female zebra finches reared in single-pair breeding cages have long-term memories of (and preferences for) the songs of their fathers, and they appear to choose their mates on the basis of song (Miller 1979a, b); hence, the level of parental care given by an adult male to young females may represent a measure of that male's present fitness and future attractiveness to females. The young female zebra finches in the aviary study were exposed to the same paternal care as were the males, and may also have learned to prefer the songs of adult males other than their fathers. If the learned song preferences of young females are based upon the characteristics of the adult males they encounter as fledglings, young males that made the correct
Animal Behaviour, 39, 4
756
choice of song models are likely to become preferred mates for females f-rom their cohort. By c o m p o u n d i n g their songs o f syllables or syllable sequences derived from different adult males, young males may, in effect, be covering their bets, by representing themselves as possessing the attractive qualities o f a n u m b e r o f different adult males. W h e n there are multiple models for a young zebra finch's song, at most one o f t h e m c a n have been provided by his genetic father. Syllables derived f r o m the songs o f n o n - p a t e r n a l adult males m u s t then be transmitted independently o f genetic information, t h o u g h there m a y be a n indirect link if a male gaining more extra-pair matings also gives more p a r e n t a l care to fledglings. I n this sense, an adult male zebra finch has a 'cultural fitness' (uncoupled from his 'genetic fitness'), which is d e p e n d e n t u p o n his ability to figure as a model for young males' songs. Multiple song models m a y m a k e zebra finches an interesting system for studying the transmission o f cultural traits.
ACKNOWLEDGMENTS I t h a n k F e r n a n d o N o t t e b o h m a n d Jeffrey Cynx for valuable c o m m e n t s o n the manuscript, Stephen J. C l a r k for advice o n statistical m e t h o d s , a n d Jeffrey Cynx and A n d r e a deMajewski for scoring syllables. This study was s u p p o r t e d by A F O S R g r a n t 86-0336.
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Williams; Models for zebra finch song learning Sossinka, R. & B6hner, J. 1980. Song types in the zebra finch (Poephila guttata castanotis). Z. Tierpsychol., 53, 123-132. ten Cate, C. t982. Behavioural differences between zebra finch and bengalese finch (foster) parents raising zebra finch young. Behaviour, 81, 152-172. ten Cate, C., Los, L. & Schilperoord, L. 1984. The influence of differences in social experience on the development of species recognition in the zebra finch. Anita. Behav., 32, 852-860. Williams, H. 1990. Bird song. In: Neurobiology of Comparative Cognition (Ed. by R. E. Kesner & D. S. Olton), pp. 77-126. Hillsdale, New Jersey: Erlbaum.
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(Received 9 June 1989; initial acceptance 26 June 1989; final acceptance 10 July 1989; MS. number: A5160)