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Alternative motor patterns in chaffinch song
ALTERNATIVE MOTOR PATTERNS IN CHAFFINCH SONG By R . A . HINDE Ornithological Field Station, Madingley ; Department of Zoology, Cambridge portant external factor is the song of rival males (Marler, 1956) . Accordingly the effect of playing back recorded Chaffinch song on the occurrence of the various song types was also studied . The relationships revealed by this study are likely to have a qualitative generality, but their precise quantitative characteristics are relevant only to the particular individuals and circumstances concerned . Accordingly no attempt has been made to state the general conclusions in other than qualitative terms .
Introduction Male Chaffinches (Fringilla coelebs) often have more than one song type in their repertoire (Thorpe, 1954, 1956 ; Marler, 1956) . These occur apparently as alternatives, following each other in the same outburst of singing, and thus presumably sharing causal factors . However, if they were true alternatives, the distribution of each type through a song outburst would be random, and this is not the case . The analysis given here indicates the complexity of the factors, internal and external, controlling the type of song given in any particular instance . The Chaffinch has a relatively simple song consisting of a trill, often divisible into two phrases, and an end-phrase (Fig . la and b). It shows considerable individual and regional variation (Thorpe, 1954 ; 1956 ; Promptoff, 1930 ; Marler, 1952). Thorpe (loc . cit ., 1958 ; see also Poulsen, 1951) has shown that first year males, kept in auditory isolation from adults from a few days after hatching, develop a rather simple song (the "isolate" song) which usually consists of a series of notes of about the normal length and descending in pitch, but with at most a very simple end-phrase . All further details are acquired by individual learning, but this is sufficiently selective to ensure that the bird does not normally acquire notes from other species . Although Chaffinch song can be induced by injections of testosterone propionate (Collard & Grevendal, 1946 ; Poulsen, 1951 ; Hinde, in prep .) the short-term waxing and waning of song depends on internal factors which are not easily subject to experimental control . However, the frequency with which songs are given varies with time, and these fluctuations in rate can be used to establish relationships between rate (i .e . songs per minute) and other characteristics of the singing . Thus the mere recording of the temporal characteristics of the singing can give some indications about the factors governing the alternation of song types, though the information obtained in this way is of course far from complete . With regard to the external factors controlling song, singing is normally confined to the territory, and also to certain song posts within that territory. Apart from these, the most im-
Material Four of the five Chaffinches used in this study had acquired their song repertoire as a result of training experiments designed to investigate song learning (Thorpe, 1954, 1956, 1958) . In some of these a "song tutor"-a device for playing a particular song at frequent short intervals-had been employed . The birds used were as follows Bird A. Hand-reared from the age of c.8 days in 1954. Trained with a reversed Chaffinch song (i .e . a normal Chaffinch song played backwards) in March 1955, it developed both an isolate song (Song Type A/1) and a reversed song (Type A/2) . Bird B . Trapped as a juvenile in July 1951, and used as a control in a number of songlearning experiments . It developed two fairly normal songs, one having a rapidly repeated series of notes in the second phrase forming a trill, and a rather emphatic end-phrase (Song Type B/1, see Fig . la), while the other had a steady series of notes in the first two phrases (Type B/2, see Fig . lb). Bird C . Hand-reared from the age of c .8 days in 1955 . Exposed to several courses of Tree Pipit (Anthus trivialis) song from the song tutor between January and March 1956 . It developed an isolate song (Song Type C/1) and an abnormal song showing some of the pitch trends of the Tree Pipit song, but none of its note structure (Type C2 ird D . Hand-reared from the age of c .8 days in 1954 and exposed to reversed Chaffinch song from the song tutor in March 1955 . It developed an isolate song (Type D/1, in Fig. lc) and a reversed song (Type D/3) . When exposed to the singing of wild Chaffinches in the course of these experiments it developed an elaboration of its 211
212
ANIMAL BEHAVIOUR, VI, 3-4
i
(a) 6-
4
2
i
i
6
4 2
2 (c) 4
2
Bird E . Hand-reared in 1955 and exposed to normal Chaffinch song in November, 1955, and reversed song in the spring of 1956 . It developed a song in which the first two phrases resembled normal Chaffinch song, but there was no end-phrase . The differences between the songs in the repertoire of any one of the individuals A-D was thus greater than that between the songs of most individual wild Chaffinches, which are all recognisably "Chaffinch songs ." (The reference numbers assigned to the various song types given above and in Fig. 1 are of course arbitrary, and no relation is implied between (e.g .) the Type I songs of different individuals) . These birds were confined in cages approximately 100 x 100 x 50 cm . in an open field : under such conditions they soon came into full song .
Normal Singing "Normal singing" signifies singi ing when no recorded songs were being played back-other wild or (a) 6 caged Chaffinches may have been singing within earshot . It was t 1 •~ t studied simply by recording the 4 tI time (nearest second) and type of each song given . Analysis of 1411jil 1 A1 .0 2 samples of normal singing from birds A-D permit the following generalisations (i) The song types are not given (e) with equal frequency, some being 6 more common than others . (Table I) . In every case the observed fre4 '4 quencies differ from those which would occur if the song types were equally common with P<0 . 01 . 2 (ii) The proportions of each song type may change with the rate of singing. Furthermore, the relation 2 between the proportion of a par. Ordinate-frequency in Kcs. . Sound spectrograms of Chaffinch song Fig. 1 ticular song type and the rate of Abscissa-time in sees. (a) and (b) Bird B . (c)--(e) Bird D . singing mar change through the isolate song which differed from the latter in season . The data for Bird A were collected over too narrow a range of rates of singing to show having an end-phrase (Type D/2, see Fig . Id). this effect . The data for Bird B were collected Later in the spring it developed yet another new over a wide range of dates but with reasonably song (Type D/4, Fig . le) .
111
213
H1 NDE : ALTERNATIVE MOTOR PATTERNS IN CHAFFINCH SONG
(b)
50
0 640 U, CD W 0.30 I.-
20
10
4 6• 7• 8 2 SONGS PER MINUTE Fig. 2 . Relation between relative frequency of song types and rate of singing . (a) Bird B . Ordinate-percentage of type B/ 1 song . X period May 4th to June 12th . - period June 6th to 26th. (b) Bird D. Ordinate-percentage of D/1 +D/2 songs to total number of all songs (X) ; percentage of D/1 to total D/1 + D/2, April 27th-May 3rd (0) ; percentage of D/l to total D/1 + D/2, June 2nd-12th ( •) . Each point indicates mean for one watch (Bird B) or rate (D) . Table I . Percentage Frequency of the Various Song Types The data for Bird C were all collected within in the Analysed Samples 4 days, but the watches were long and the rate of singing varied within each watch. Accordingly Bird each watch was divided into 4-minute runs . The D Song Type A B C percentage of C/1 songs in each run decreased with increase in the total songs in that run . 1 33 .5 43 .5 40 .8 (33 .4 {127 (Corrln . coeff. -0 .34, N=85) . .6 .2 .7 2 66 .5 52 59 The data for Bird D were collected in two periods-April 27th to May 3rd and June 2-12th . 3 0 .1 The relation between the number of song types - 4 38 .8 D/1 and D/2* in each run to the total number of songs in that run showed no change between the Size of sample 2180 1827 776 *As shown in Fig . lc and d, song type D/2 was closely (number of songs)j 75' I similar to type D/1 in form. They were therefore treated together . In fact type D/1 can be regarded as short watches on each day . The relation between an incomplete form of type D/2, its frequency becoming the percentage of type B/1 songs on each day less relative to that of type D/2 as the rate of and the rate of singing changed during the course singing increased (Fig. 2b). Further evidence in favour of this view lies in the way in which they were interof the observation period as shown in Fig. 2a mingled in the song sequences (see below), the song(Corrln . coeff. -0 .62 (N=9) for the period May song intervals between types D/1 and D/2 and between 4th to June 2nd, + 0 .76 (N= 15) for June 6th types D/2 and D/1 being no longer than between types to 26th) . D/1 and D/1 or types D/2 and D/2 . I
2
3
4
5•
214
ANIMAL BEHAVIOUR, VI, 3-4
two periods, the correlation (r= -0 . 29, N=45 runs) being just significant at P<0 . 05 . The relations between the proportion of type D/ 1 to types D/I and D/2, however, were quite different between the two periods . For the earlier one the negative correlation between the number of songs in each 4-minute run and the proportion of type D/l was significant at P<0 . 05 (r=0.65, N=20) . The data for the later period differed significantly (P<0 .01) from the data from the former : within this group, however, there was no significant correlation between the proportion of type D/1 and the rate of singing. Thus with all these birds the proportion of the various song types changed with the rate of singing. (iii) Each song is more likely to be followed by a similar song than by a dissimilar song . This is
shown by the ratio No . of times song of one type followed by song of same type No. of times this song type followed by song of different type
in Table II . X2 tests showed that the number of times that a song of one type was followed by a song of the same type exceeded that to be expected on a chance distribution of song types at P<0. 01 in every case . The songs are thus given in a sequence of one song type followed by a sequence of another, and not at random . (Marler (1956) gives similar data from field observations) .
Table II . Ratio Between Number of Occasions Song of a Given Type was Followed by Song of Same Type to Number of Occasions it was Followed by Song of a Different Type Bird Song type
A
B
C
1
3.8
9 .0
5.3
2
9.7
13 . 2
8.3
4
-
-
-
D 10 .4* 6 .3
*See above. (iv) The average interval between two songs of the same type is roughly the same for all song types in the repertoire . The average interval between two songs of the same type (i .e . the intervals between songs in one sequence) is shorter than that between songs of different types (i.e . the intervals between sequences) . This is shown in Table III .
For Birds A, B and C the data for all possible intervals are given, that for Bird B being split according to the rate of singing (p . 215) . For Bird D, which had 4 types of song, the data are grouped into intervals between similar song types and intervals in which there was a change of song type. The frequency distribution of song-song intervals for Bird A is shown in Fig . 3 . The distri-
Table IN Mean and Median Intervals Between Songs Bird
Interval between song types
N
Mean
Median
A
1-1 2-2 1-2 2-1
203 439 53 45
15 .5 13 .7 24 .2 34.4
10 . 2 9.5 16 . 8 19 . 5
B (songs per min . between 2.5 and 4.0)
1-1 2-2 1-2 2-1
86 236 36 34
15 .4 15 .4 24 .4 32 . 1
13 . 4 13 . 5 22 . 0 28 . 7
B (songs per min . between 4.1 and 6.6)
1-1 2-2 1-2 2-1
352 396 37 41
9 .5 10.0 13 .2 14 . 4
8.9 9.3 11 . 5 11 .4
C
1-1 2-2 1-2 2-1
627 966 117 117
12 . 2 14 .2 22.9 20.4
8 .5 8 .5 15 .3 15 . 3
12 .3
-
D
Intervals between similar songs Intervals between dissimilar songs
83
17 .5
215
HINDE : ALTERNATIVE MOTOR PATTERNS IN CHAFFINCH SONG
butions for the other individuals were similar, and for each the variability of intervals between songs of different type was greater than that of intervals between songs of the same type .
so(
O
X
U7oW N v
30-
J60-
(a)
20
0
0 Z,60O 5O .
W
x
W50 z L,)40-
0 O
6wad
4d. 30~
X
I 1
x
N2Om 10-
i s
.
QD 0
10[ 0
i'
.x x -
xx 08 m
o is r-
XX
s
, -1
-
(d)
4
-
Q
8 12 28 >28 16 20 24 INTERVAL - SECS . Fig. 3 . Frequency distribution of song-song intervals for Bird A. (a) A/1-A/1 . (b) A/2-A/2 . (c) A/1-A/2. (d) A/2-A/l .
i
g
! SONGS
PER
MINUTE Fig. 4 . Relation between song-song interval and rate of singing. Bird . B . (o) B/1-B/1 . 0 B/2B/2. X B/1-B/2. . B/2-B/i .
(v) As suggested by the data for Bird B in Table III, the difference between the average interval between songs of the same type and the average interval between songs,of different types decreases at high rates of singing . This is shown
directly by Bird B in Fig. 4. The data for Birds A, C and D were similar . In each case the ratio average interval between dissimilar songs average interval between similar songs
approached 1 at higher rates of singing, the decrease in the ratio being significant at P<0 . 05 or better. (vi) The average number of songs per sequence increases with the rate of singing . This is shown
for the song type 2 of Chaffinch B, the type 1 of C and the type 4 of D in Fig . 5 . The data for the other songs of each bird are very similar, and the increase in each case is significant at P<0 . 01 or better . This increase in the number of songs per sequence could be due to an increase in the duration of the sequence, a decrease in the songsong intervals, or both . The latter certainly occurs (see Fig . 4) . The duration of the sequence is variable : with Chaffinch B it increased with the rate of singing, but with Chaffinches C and D there was no clear change in the mean duration
NGS PE Fig . 5 . Relation between rate of songs per sequence and rate of singing. 0 B/2 . X C/1 • D/4 .
216
ANIMAL BEHAVIOUR,
of song sequences with the rate of singing . In these cases, therefore, the change over from one song type to another depends more on the duration of the preceding sequence than on the number of times the song has been sung . The Effect of Played-back Song on the Proportion of Song Types The response to records of Chaffinch song was studied as follows : Each song which was to be used as a stimulus was recorded on disc . A second disc was then prepared on which the same song was recorded at intervals of approximately 15 seconds. Each experiment consisted of a sequence of 15 of one stimulus song from such a record, played over loudspeakers, a one minute gap, a sequence of 15 of a second stimulus song type, and so on . This was repeated a number of times, each stimulus song type being played an equal number of times on each day. The "reply" songs given by the Chaffinch to which the songs were being played was noted . (These are referred to here as `reply" songs though, in fact, they are not necessarily replies to particular stimulus songs : indeed the bird was nearly always singing before the experiment started.) The results are shown in Table IV and can be summarised as follows : (i) For each bird playing of the song t31e which was given by the bird most frequently in normal singing (see Table I) was more effective in stimulating singing than playing other songs
V1 . 3-4
.from the bird's repertoire . The most effective songs were A/2 for Bird A, B/2 for Bird B, C/2 for Bird C . With Bird D, types D/l and D/2 together (see footnote, p . ) were more frequent than D/4, and D/2 was more effective in stimulating song . (ii) The song from a bird's repertoire which is most effective in stimulating song when played back is not related to its resemblance to "normal" song . Thus for Birds A and C the more effective Type 2 songs were less like normal songs than the Type I (isolate) songs . (No judgment of the relative similarities to "normal" song of the songs in the repertoire of Birds B and D could be made .) Furthermore, with three birds the effectiveness of playing back "normal" song was tested . In two cases (Birds A and E) it was significantly less effective in stimulating song than the more effective song from the bird's own repertoire, and in one case (C) it was slightly, but not significantly, more effective . (iii) When the singing is in some measure a response to a stimulus song type fromn the bird's own repertoire, the proportion of that song ripe tends to increase . This is shown in the last two columns of Table IV, where the number of Type 1 (in the case of D, Type 1 and Type 2) replies to each stimulus song type is shown . With Birds A, B and C the proportion of Type I replies was significantly greater when Type I was used as a stimulus song than when Type 2 was used . With Bird D the proportion of Type
Table IV. Effect of Playing Stimulus Songs on the Bird's Own Singing Bird A
Stimulus song
No . of replies
Difference from equality significant at P<
A/I A/2 Normal
158 242 162
0 . 001
403
(0-7)
No . of type I replies
I I
Difference signficant at P<
76(48%) 1 56(23 %) 59 (36 %)
0 . 001 0 . 001
2267 17 (50 %) }
0 . 05
B
B/2
C
C/I C/2 Normal
481 557 581
0.001
193(40%)l 162 (29 %) 245(42 %)
0 . 001 0 . 001
D/l D/2 D/4
511 571 511
0.001
314* (61%)1 336* (59%) r 289* (56%)l J
0 . 05
573 427
0 .001
D
E
Own song Normal
j
*Totals refer to Type D/1 plus Type D/2
HINDE : ALTERNATIVE MOTOR PATTERNS IN CHAFFINCH SONG D/l plus Type D/2 replies was significantly greater with Type D/1 as stimulus song than with Type D/4 . The difference between D/2 and D/4 was in the same direction, but not significant . With Birds A and C there was no significant difference between the proportion of Type 1 replies when normal song was used as the stimulus song and the proportion which occurred in normal singing (Table I) . Although the effect of playing a given stimulus song on the proportion of that song type as demonstrated in these experiments was not large, this may be due to the particular length of the sequences of stimulus songs . Further, in nature the use of a particular song type towards a rival would become accentuated by conditioning to stimuli other than the rival's song (e.g . landmarks) . Marler (1956) has stressed that when two wild Chaffinches sing against each other, they do not counter song with song, but each sings in its own rhythm, so that they soon get out of step . A similar conclusion was reached from these experiments-the reply songs were distributed almost at random over the 15-second interval between stimulus songs, with at most a slight concentration in the period 3-8 seconds after the stimulus song. The tendency to reply with a song similar to that being played is thus to be regarded not as a process of imitating the pattern just perceived, but as a facilitation of one of the "alternative" motor patterns in preference to the other(s) . Discussion The data summarised in the preceding sections have implications concerning three problems (i) The Complexity of the Factors Underlying the Alternation Between Song Types (a) The frequency of singing fluctuates during the course of each song outburst . Such fluctuations have not been studied here, and must be ascribed to as yet unanalysed fluctuations in the variables underlying singing or in other interfering activities . (b) Since an interval of less than 3 seconds between songs is extremely rare, it may be suggested that each song is accompanied by an inhibitory effect on singing which is dissipated with time . That this inhibitory effect is a consequence of performance seems probable from the fact that the song-song intervals after the occasional incomplete songs tend to be shorter than those after normal songs ; but it could be peripheral, or central, or both .
217
(c) If this inhibitory effect acted on both songs equally, the mechanism of change-over between song types remains unexplained . If it merely affected the song type just uttered more than the others, alternation would occur more often than on a random distribution of song types, instead of less. It is ,therefore necessary to postulate the existence, during the course of each song sequence, of a persisting tendency to repeat the song last uttered : this we may describe as a facilitative effect . This facilitative effect could be merely a consequence of slight differences between the motivational factors for each song type . On this view the alternation between song types would depend on fluctuations in these factors, resulting in a dominance of first one type, then the other . This would be in harmony with, for instance, the fact that in some cases the temporal duration of the sequences is independent of the rate of singing, and thus of the number of times the song has been uttered. Although no observations have been made on differences between the motivation of song types in the Chaffinch, Great Tit (Pares major) males sometimes use a different song when waiting outside the box for the female from that used in territorial disputes (personal observation) . However, since the birds studied here were confined in small cages, there were no obvious changes in the external world likely to produce a change in motivation other than the singing itself. An alternative possibility is that the facilitative effect is a consequence of performance . The alternation between sequences would then be due to a difference between the time constants of the decay of the facilitative and inhibitory effects . There are too many unknowns for it to be profitable to suggest a specific model along these lines, but most of the features of the song sequences discussed in the first part of this paper could be accounted for in such a way . The significant aspect of performance could be the act of uttering, a proprioceptive feed-back, or the auditory perception of the consequent sound pattern : the importance of the latter is suggested by the facilitative effect of the playing back of one song type on the production of that type . (ii) Song Learning The songs which Chaffinches A-D sang most often were also most effective in eliciting song when played back . Further, the songs which Chaffinches A and E had learnt to sing, although
218
ANIMAL BEHAVIOUR . VI,
abnormal, were more effective in eliciting song when played back than was normal song . Thus the process of learning a song type determines not only what song will be sung, but also what will be effective in inducing singing. While the learning of the motor pattern, and the acquisition of the mechanism whereby a stimulus song is responded to, could be independent processes, this suggests that they depend on the same initial stage-namely the development of a selective responsiveness to the stimulus song . This is in harmony with what happens in the development of full song, which Thorpe (1954) describes as "so to speak `crystallising out' of the amorphous subsong," the transformation of subsong into song consisting largely "in the gradual dropping out of the extreme frequencies ." What "crystallises out" is determined by what the bird has heard in the past, which must be retained in some way as a pattern towards which the song gradually develops . Indeed, some characteristics of the song are learnt in the bird's youth, before it is itself able to sing . Thus, as Thorpe points out, the learning is not in the first place the acquisition merely of a motor pattern, but of a receptory mechanism responsive to the song which is being acquired . (iii) Functional Aspects In nature, song attracts females and repels males : it plays an important role in the defence of the territory (Marler, 1956) . Since song is more likely to evoke a response from another Chaffinch if it resembles that Chaffinch's own song (p . 216), there will be a selective advantage in developing a song type like that of one's neighbours . Since each territory-owning male is likely to have several neighbours, there will be an advantage in having several songs and in replying to a song of one type with a similar one . Further, it will be disadvantageous to develop a song markedly different from the normal . All this, however, assumes an initial variability between the songs of individuals given variability, there is a selective advantage to individual males in developing songs like those of their neighbours . The significance of the initial variability is another question, but is presumably related to the role of song in permitting individual recognition at a distance : this is especially likely to be important in pair formation and the maintenance of the pair bond .
3-4
Summary 1 . When a Chaffinch has more than one song type in its repertoire, each song outburst consists of a sequence of one song type followed by a sequence of another, and so on . Data concerning various aspects of the succession of song sequences in an outburst are presented . It is suggested that the uttering of each song is associated with both inhibitory and facilitative effects on the repetition of that type . and that differences in the decay constants of the effects govern the alternation of song types . 2. When songs are played back to a Chaffinch, those song types which it utters most frequently itself are most effective in evoking singing . irrespective of whether they resemble normal song . Further, the frequency of the song type played tends to increase in the bird's own singing . This supports the view that song-learning consists primarily in the acquisition of a selective responsiveness to a particular song type (or range of types) . Acknowledgments I am grateful to Dr . W . H . Thorpe for making available birds previously trained by him for use in this experiment, and to Dr . Thorpe and Dr . Marler for their comments on the manuscript . REFERENCES Collard, J . & Grevendal, L. (1946) . Etude sur les characteres sexuels des Pinsons Fringilla coelebs and F. ntontifringilla. Gerfaut, 2, 89-107 .
Marler, P. (1952) . Variation in the song of the Chaffinch (Fringilla coelebs) . Ibis, 94, 458-472 .
Marler, P . (1956) . The behaviour of the Chaffinch . Behaviour Supplement, No . 5, 1-178 . Poulsen, H . N . (1951) . Inheritance and learning in the song of the Chaffinch . Behaviour, 3 . 216-227 . Promptoff, A . (1930) . Die geographische Variabilitat des Buchfinkenschlags (Fringilla coelehs) L . in zusammenhang mit etlichen allegemeinen Fragen der Saisonvogelzuge. Bio . Zbl., 50, 478-503 . Thorpe, W . H . (1954) . The process of song-learning in the Chaffinch as studied by means of the sound spectograph. Nature (Lond.), 173, 465 . Thorpe, W . H . (1956) . Learning and instinct in animals. London : Methuen . Thorpe, W . H. (1958) . The learning of song patterns by birds, with special reference to the song of the Chaffinch. Ibis, 100, in press . Accepted for publication 3rd March . 1958 .
Introduction Male Chaffinches (Fringilla coelebs) often have more than one song type in their repertoire (Thorpe, 1954, 1956 ; Marler, 1956) . These occur apparently as alternatives, following each other in the same outburst of singing, and thus presumably sharing causal factors . However, if they were true alternatives, the distribution of each type through a song outburst would be random, and this is not the case . The analysis given here indicates the complexity of the factors, internal and external, controlling the type of song given in any particular instance . The Chaffinch has a relatively simple song consisting of a trill, often divisible into two phrases, and an end-phrase (Fig . la and b). It shows considerable individual and regional variation (Thorpe, 1954 ; 1956 ; Promptoff, 1930 ; Marler, 1952). Thorpe (loc . cit ., 1958 ; see also Poulsen, 1951) has shown that first year males, kept in auditory isolation from adults from a few days after hatching, develop a rather simple song (the "isolate" song) which usually consists of a series of notes of about the normal length and descending in pitch, but with at most a very simple end-phrase . All further details are acquired by individual learning, but this is sufficiently selective to ensure that the bird does not normally acquire notes from other species . Although Chaffinch song can be induced by injections of testosterone propionate (Collard & Grevendal, 1946 ; Poulsen, 1951 ; Hinde, in prep .) the short-term waxing and waning of song depends on internal factors which are not easily subject to experimental control . However, the frequency with which songs are given varies with time, and these fluctuations in rate can be used to establish relationships between rate (i .e . songs per minute) and other characteristics of the singing . Thus the mere recording of the temporal characteristics of the singing can give some indications about the factors governing the alternation of song types, though the information obtained in this way is of course far from complete . With regard to the external factors controlling song, singing is normally confined to the territory, and also to certain song posts within that territory. Apart from these, the most im-
Material Four of the five Chaffinches used in this study had acquired their song repertoire as a result of training experiments designed to investigate song learning (Thorpe, 1954, 1956, 1958) . In some of these a "song tutor"-a device for playing a particular song at frequent short intervals-had been employed . The birds used were as follows Bird A. Hand-reared from the age of c.8 days in 1954. Trained with a reversed Chaffinch song (i .e . a normal Chaffinch song played backwards) in March 1955, it developed both an isolate song (Song Type A/1) and a reversed song (Type A/2) . Bird B . Trapped as a juvenile in July 1951, and used as a control in a number of songlearning experiments . It developed two fairly normal songs, one having a rapidly repeated series of notes in the second phrase forming a trill, and a rather emphatic end-phrase (Song Type B/1, see Fig . la), while the other had a steady series of notes in the first two phrases (Type B/2, see Fig . lb). Bird C . Hand-reared from the age of c .8 days in 1955 . Exposed to several courses of Tree Pipit (Anthus trivialis) song from the song tutor between January and March 1956 . It developed an isolate song (Song Type C/1) and an abnormal song showing some of the pitch trends of the Tree Pipit song, but none of its note structure (Type C2 ird D . Hand-reared from the age of c .8 days in 1954 and exposed to reversed Chaffinch song from the song tutor in March 1955 . It developed an isolate song (Type D/1, in Fig. lc) and a reversed song (Type D/3) . When exposed to the singing of wild Chaffinches in the course of these experiments it developed an elaboration of its 211
212
ANIMAL BEHAVIOUR, VI, 3-4
i
(a) 6-
4
2
i
i
6
4 2
2 (c) 4
2
Bird E . Hand-reared in 1955 and exposed to normal Chaffinch song in November, 1955, and reversed song in the spring of 1956 . It developed a song in which the first two phrases resembled normal Chaffinch song, but there was no end-phrase . The differences between the songs in the repertoire of any one of the individuals A-D was thus greater than that between the songs of most individual wild Chaffinches, which are all recognisably "Chaffinch songs ." (The reference numbers assigned to the various song types given above and in Fig. 1 are of course arbitrary, and no relation is implied between (e.g .) the Type I songs of different individuals) . These birds were confined in cages approximately 100 x 100 x 50 cm . in an open field : under such conditions they soon came into full song .
Normal Singing "Normal singing" signifies singi ing when no recorded songs were being played back-other wild or (a) 6 caged Chaffinches may have been singing within earshot . It was t 1 •~ t studied simply by recording the 4 tI time (nearest second) and type of each song given . Analysis of 1411jil 1 A1 .0 2 samples of normal singing from birds A-D permit the following generalisations (i) The song types are not given (e) with equal frequency, some being 6 more common than others . (Table I) . In every case the observed fre4 '4 quencies differ from those which would occur if the song types were equally common with P<0 . 01 . 2 (ii) The proportions of each song type may change with the rate of singing. Furthermore, the relation 2 between the proportion of a par. Ordinate-frequency in Kcs. . Sound spectrograms of Chaffinch song Fig. 1 ticular song type and the rate of Abscissa-time in sees. (a) and (b) Bird B . (c)--(e) Bird D . singing mar change through the isolate song which differed from the latter in season . The data for Bird A were collected over too narrow a range of rates of singing to show having an end-phrase (Type D/2, see Fig . Id). this effect . The data for Bird B were collected Later in the spring it developed yet another new over a wide range of dates but with reasonably song (Type D/4, Fig . le) .
111
213
H1 NDE : ALTERNATIVE MOTOR PATTERNS IN CHAFFINCH SONG
(b)
50
0 640 U, CD W 0.30 I.-
20
10
4 6• 7• 8 2 SONGS PER MINUTE Fig. 2 . Relation between relative frequency of song types and rate of singing . (a) Bird B . Ordinate-percentage of type B/ 1 song . X period May 4th to June 12th . - period June 6th to 26th. (b) Bird D. Ordinate-percentage of D/1 +D/2 songs to total number of all songs (X) ; percentage of D/1 to total D/1 + D/2, April 27th-May 3rd (0) ; percentage of D/l to total D/1 + D/2, June 2nd-12th ( •) . Each point indicates mean for one watch (Bird B) or rate (D) . Table I . Percentage Frequency of the Various Song Types The data for Bird C were all collected within in the Analysed Samples 4 days, but the watches were long and the rate of singing varied within each watch. Accordingly Bird each watch was divided into 4-minute runs . The D Song Type A B C percentage of C/1 songs in each run decreased with increase in the total songs in that run . 1 33 .5 43 .5 40 .8 (33 .4 {127 (Corrln . coeff. -0 .34, N=85) . .6 .2 .7 2 66 .5 52 59 The data for Bird D were collected in two periods-April 27th to May 3rd and June 2-12th . 3 0 .1 The relation between the number of song types - 4 38 .8 D/1 and D/2* in each run to the total number of songs in that run showed no change between the Size of sample 2180 1827 776 *As shown in Fig . lc and d, song type D/2 was closely (number of songs)j 75' I similar to type D/1 in form. They were therefore treated together . In fact type D/1 can be regarded as short watches on each day . The relation between an incomplete form of type D/2, its frequency becoming the percentage of type B/1 songs on each day less relative to that of type D/2 as the rate of and the rate of singing changed during the course singing increased (Fig. 2b). Further evidence in favour of this view lies in the way in which they were interof the observation period as shown in Fig. 2a mingled in the song sequences (see below), the song(Corrln . coeff. -0 .62 (N=9) for the period May song intervals between types D/1 and D/2 and between 4th to June 2nd, + 0 .76 (N= 15) for June 6th types D/2 and D/1 being no longer than between types to 26th) . D/1 and D/1 or types D/2 and D/2 . I
2
3
4
5•
214
ANIMAL BEHAVIOUR, VI, 3-4
two periods, the correlation (r= -0 . 29, N=45 runs) being just significant at P<0 . 05 . The relations between the proportion of type D/ 1 to types D/I and D/2, however, were quite different between the two periods . For the earlier one the negative correlation between the number of songs in each 4-minute run and the proportion of type D/l was significant at P<0 . 05 (r=0.65, N=20) . The data for the later period differed significantly (P<0 .01) from the data from the former : within this group, however, there was no significant correlation between the proportion of type D/1 and the rate of singing. Thus with all these birds the proportion of the various song types changed with the rate of singing. (iii) Each song is more likely to be followed by a similar song than by a dissimilar song . This is
shown by the ratio No . of times song of one type followed by song of same type No. of times this song type followed by song of different type
in Table II . X2 tests showed that the number of times that a song of one type was followed by a song of the same type exceeded that to be expected on a chance distribution of song types at P<0. 01 in every case . The songs are thus given in a sequence of one song type followed by a sequence of another, and not at random . (Marler (1956) gives similar data from field observations) .
Table II . Ratio Between Number of Occasions Song of a Given Type was Followed by Song of Same Type to Number of Occasions it was Followed by Song of a Different Type Bird Song type
A
B
C
1
3.8
9 .0
5.3
2
9.7
13 . 2
8.3
4
-
-
-
D 10 .4* 6 .3
*See above. (iv) The average interval between two songs of the same type is roughly the same for all song types in the repertoire . The average interval between two songs of the same type (i .e . the intervals between songs in one sequence) is shorter than that between songs of different types (i.e . the intervals between sequences) . This is shown in Table III .
For Birds A, B and C the data for all possible intervals are given, that for Bird B being split according to the rate of singing (p . 215) . For Bird D, which had 4 types of song, the data are grouped into intervals between similar song types and intervals in which there was a change of song type. The frequency distribution of song-song intervals for Bird A is shown in Fig . 3 . The distri-
Table IN Mean and Median Intervals Between Songs Bird
Interval between song types
N
Mean
Median
A
1-1 2-2 1-2 2-1
203 439 53 45
15 .5 13 .7 24 .2 34.4
10 . 2 9.5 16 . 8 19 . 5
B (songs per min . between 2.5 and 4.0)
1-1 2-2 1-2 2-1
86 236 36 34
15 .4 15 .4 24 .4 32 . 1
13 . 4 13 . 5 22 . 0 28 . 7
B (songs per min . between 4.1 and 6.6)
1-1 2-2 1-2 2-1
352 396 37 41
9 .5 10.0 13 .2 14 . 4
8.9 9.3 11 . 5 11 .4
C
1-1 2-2 1-2 2-1
627 966 117 117
12 . 2 14 .2 22.9 20.4
8 .5 8 .5 15 .3 15 . 3
12 .3
-
D
Intervals between similar songs Intervals between dissimilar songs
83
17 .5
215
HINDE : ALTERNATIVE MOTOR PATTERNS IN CHAFFINCH SONG
butions for the other individuals were similar, and for each the variability of intervals between songs of different type was greater than that of intervals between songs of the same type .
so(
O
X
U7oW N v
30-
J60-
(a)
20
0
0 Z,60O 5O .
W
x
W50 z L,)40-
0 O
6wad
4d. 30~
X
I 1
x
N2Om 10-
i s
.
QD 0
10[ 0
i'
.x x -
xx 08 m
o is r-
XX
s
, -1
-
(d)
4
-
Q
8 12 28 >28 16 20 24 INTERVAL - SECS . Fig. 3 . Frequency distribution of song-song intervals for Bird A. (a) A/1-A/1 . (b) A/2-A/2 . (c) A/1-A/2. (d) A/2-A/l .
i
g
! SONGS
PER
MINUTE Fig. 4 . Relation between song-song interval and rate of singing. Bird . B . (o) B/1-B/1 . 0 B/2B/2. X B/1-B/2. . B/2-B/i .
(v) As suggested by the data for Bird B in Table III, the difference between the average interval between songs of the same type and the average interval between songs,of different types decreases at high rates of singing . This is shown
directly by Bird B in Fig. 4. The data for Birds A, C and D were similar . In each case the ratio average interval between dissimilar songs average interval between similar songs
approached 1 at higher rates of singing, the decrease in the ratio being significant at P<0 . 05 or better. (vi) The average number of songs per sequence increases with the rate of singing . This is shown
for the song type 2 of Chaffinch B, the type 1 of C and the type 4 of D in Fig . 5 . The data for the other songs of each bird are very similar, and the increase in each case is significant at P<0 . 01 or better . This increase in the number of songs per sequence could be due to an increase in the duration of the sequence, a decrease in the songsong intervals, or both . The latter certainly occurs (see Fig . 4) . The duration of the sequence is variable : with Chaffinch B it increased with the rate of singing, but with Chaffinches C and D there was no clear change in the mean duration
NGS PE Fig . 5 . Relation between rate of songs per sequence and rate of singing. 0 B/2 . X C/1 • D/4 .
216
ANIMAL BEHAVIOUR,
of song sequences with the rate of singing . In these cases, therefore, the change over from one song type to another depends more on the duration of the preceding sequence than on the number of times the song has been sung . The Effect of Played-back Song on the Proportion of Song Types The response to records of Chaffinch song was studied as follows : Each song which was to be used as a stimulus was recorded on disc . A second disc was then prepared on which the same song was recorded at intervals of approximately 15 seconds. Each experiment consisted of a sequence of 15 of one stimulus song from such a record, played over loudspeakers, a one minute gap, a sequence of 15 of a second stimulus song type, and so on . This was repeated a number of times, each stimulus song type being played an equal number of times on each day. The "reply" songs given by the Chaffinch to which the songs were being played was noted . (These are referred to here as `reply" songs though, in fact, they are not necessarily replies to particular stimulus songs : indeed the bird was nearly always singing before the experiment started.) The results are shown in Table IV and can be summarised as follows : (i) For each bird playing of the song t31e which was given by the bird most frequently in normal singing (see Table I) was more effective in stimulating singing than playing other songs
V1 . 3-4
.from the bird's repertoire . The most effective songs were A/2 for Bird A, B/2 for Bird B, C/2 for Bird C . With Bird D, types D/l and D/2 together (see footnote, p . ) were more frequent than D/4, and D/2 was more effective in stimulating song . (ii) The song from a bird's repertoire which is most effective in stimulating song when played back is not related to its resemblance to "normal" song . Thus for Birds A and C the more effective Type 2 songs were less like normal songs than the Type I (isolate) songs . (No judgment of the relative similarities to "normal" song of the songs in the repertoire of Birds B and D could be made .) Furthermore, with three birds the effectiveness of playing back "normal" song was tested . In two cases (Birds A and E) it was significantly less effective in stimulating song than the more effective song from the bird's own repertoire, and in one case (C) it was slightly, but not significantly, more effective . (iii) When the singing is in some measure a response to a stimulus song type fromn the bird's own repertoire, the proportion of that song ripe tends to increase . This is shown in the last two columns of Table IV, where the number of Type 1 (in the case of D, Type 1 and Type 2) replies to each stimulus song type is shown . With Birds A, B and C the proportion of Type I replies was significantly greater when Type I was used as a stimulus song than when Type 2 was used . With Bird D the proportion of Type
Table IV. Effect of Playing Stimulus Songs on the Bird's Own Singing Bird A
Stimulus song
No . of replies
Difference from equality significant at P<
A/I A/2 Normal
158 242 162
0 . 001
403
(0-7)
No . of type I replies
I I
Difference signficant at P<
76(48%) 1 56(23 %) 59 (36 %)
0 . 001 0 . 001
2267 17 (50 %) }
0 . 05
B
B/2
C
C/I C/2 Normal
481 557 581
0.001
193(40%)l 162 (29 %) 245(42 %)
0 . 001 0 . 001
D/l D/2 D/4
511 571 511
0.001
314* (61%)1 336* (59%) r 289* (56%)l J
0 . 05
573 427
0 .001
D
E
Own song Normal
j
*Totals refer to Type D/1 plus Type D/2
HINDE : ALTERNATIVE MOTOR PATTERNS IN CHAFFINCH SONG D/l plus Type D/2 replies was significantly greater with Type D/1 as stimulus song than with Type D/4 . The difference between D/2 and D/4 was in the same direction, but not significant . With Birds A and C there was no significant difference between the proportion of Type 1 replies when normal song was used as the stimulus song and the proportion which occurred in normal singing (Table I) . Although the effect of playing a given stimulus song on the proportion of that song type as demonstrated in these experiments was not large, this may be due to the particular length of the sequences of stimulus songs . Further, in nature the use of a particular song type towards a rival would become accentuated by conditioning to stimuli other than the rival's song (e.g . landmarks) . Marler (1956) has stressed that when two wild Chaffinches sing against each other, they do not counter song with song, but each sings in its own rhythm, so that they soon get out of step . A similar conclusion was reached from these experiments-the reply songs were distributed almost at random over the 15-second interval between stimulus songs, with at most a slight concentration in the period 3-8 seconds after the stimulus song. The tendency to reply with a song similar to that being played is thus to be regarded not as a process of imitating the pattern just perceived, but as a facilitation of one of the "alternative" motor patterns in preference to the other(s) . Discussion The data summarised in the preceding sections have implications concerning three problems (i) The Complexity of the Factors Underlying the Alternation Between Song Types (a) The frequency of singing fluctuates during the course of each song outburst . Such fluctuations have not been studied here, and must be ascribed to as yet unanalysed fluctuations in the variables underlying singing or in other interfering activities . (b) Since an interval of less than 3 seconds between songs is extremely rare, it may be suggested that each song is accompanied by an inhibitory effect on singing which is dissipated with time . That this inhibitory effect is a consequence of performance seems probable from the fact that the song-song intervals after the occasional incomplete songs tend to be shorter than those after normal songs ; but it could be peripheral, or central, or both .
217
(c) If this inhibitory effect acted on both songs equally, the mechanism of change-over between song types remains unexplained . If it merely affected the song type just uttered more than the others, alternation would occur more often than on a random distribution of song types, instead of less. It is ,therefore necessary to postulate the existence, during the course of each song sequence, of a persisting tendency to repeat the song last uttered : this we may describe as a facilitative effect . This facilitative effect could be merely a consequence of slight differences between the motivational factors for each song type . On this view the alternation between song types would depend on fluctuations in these factors, resulting in a dominance of first one type, then the other . This would be in harmony with, for instance, the fact that in some cases the temporal duration of the sequences is independent of the rate of singing, and thus of the number of times the song has been uttered. Although no observations have been made on differences between the motivation of song types in the Chaffinch, Great Tit (Pares major) males sometimes use a different song when waiting outside the box for the female from that used in territorial disputes (personal observation) . However, since the birds studied here were confined in small cages, there were no obvious changes in the external world likely to produce a change in motivation other than the singing itself. An alternative possibility is that the facilitative effect is a consequence of performance . The alternation between sequences would then be due to a difference between the time constants of the decay of the facilitative and inhibitory effects . There are too many unknowns for it to be profitable to suggest a specific model along these lines, but most of the features of the song sequences discussed in the first part of this paper could be accounted for in such a way . The significant aspect of performance could be the act of uttering, a proprioceptive feed-back, or the auditory perception of the consequent sound pattern : the importance of the latter is suggested by the facilitative effect of the playing back of one song type on the production of that type . (ii) Song Learning The songs which Chaffinches A-D sang most often were also most effective in eliciting song when played back . Further, the songs which Chaffinches A and E had learnt to sing, although
218
ANIMAL BEHAVIOUR . VI,
abnormal, were more effective in eliciting song when played back than was normal song . Thus the process of learning a song type determines not only what song will be sung, but also what will be effective in inducing singing. While the learning of the motor pattern, and the acquisition of the mechanism whereby a stimulus song is responded to, could be independent processes, this suggests that they depend on the same initial stage-namely the development of a selective responsiveness to the stimulus song . This is in harmony with what happens in the development of full song, which Thorpe (1954) describes as "so to speak `crystallising out' of the amorphous subsong," the transformation of subsong into song consisting largely "in the gradual dropping out of the extreme frequencies ." What "crystallises out" is determined by what the bird has heard in the past, which must be retained in some way as a pattern towards which the song gradually develops . Indeed, some characteristics of the song are learnt in the bird's youth, before it is itself able to sing . Thus, as Thorpe points out, the learning is not in the first place the acquisition merely of a motor pattern, but of a receptory mechanism responsive to the song which is being acquired . (iii) Functional Aspects In nature, song attracts females and repels males : it plays an important role in the defence of the territory (Marler, 1956) . Since song is more likely to evoke a response from another Chaffinch if it resembles that Chaffinch's own song (p . 216), there will be a selective advantage in developing a song type like that of one's neighbours . Since each territory-owning male is likely to have several neighbours, there will be an advantage in having several songs and in replying to a song of one type with a similar one . Further, it will be disadvantageous to develop a song markedly different from the normal . All this, however, assumes an initial variability between the songs of individuals given variability, there is a selective advantage to individual males in developing songs like those of their neighbours . The significance of the initial variability is another question, but is presumably related to the role of song in permitting individual recognition at a distance : this is especially likely to be important in pair formation and the maintenance of the pair bond .
3-4
Summary 1 . When a Chaffinch has more than one song type in its repertoire, each song outburst consists of a sequence of one song type followed by a sequence of another, and so on . Data concerning various aspects of the succession of song sequences in an outburst are presented . It is suggested that the uttering of each song is associated with both inhibitory and facilitative effects on the repetition of that type . and that differences in the decay constants of the effects govern the alternation of song types . 2. When songs are played back to a Chaffinch, those song types which it utters most frequently itself are most effective in evoking singing . irrespective of whether they resemble normal song . Further, the frequency of the song type played tends to increase in the bird's own singing . This supports the view that song-learning consists primarily in the acquisition of a selective responsiveness to a particular song type (or range of types) . Acknowledgments I am grateful to Dr . W . H . Thorpe for making available birds previously trained by him for use in this experiment, and to Dr . Thorpe and Dr . Marler for their comments on the manuscript . REFERENCES Collard, J . & Grevendal, L. (1946) . Etude sur les characteres sexuels des Pinsons Fringilla coelebs and F. ntontifringilla. Gerfaut, 2, 89-107 .
Marler, P. (1952) . Variation in the song of the Chaffinch (Fringilla coelebs) . Ibis, 94, 458-472 .
Marler, P . (1956) . The behaviour of the Chaffinch . Behaviour Supplement, No . 5, 1-178 . Poulsen, H . N . (1951) . Inheritance and learning in the song of the Chaffinch . Behaviour, 3 . 216-227 . Promptoff, A . (1930) . Die geographische Variabilitat des Buchfinkenschlags (Fringilla coelehs) L . in zusammenhang mit etlichen allegemeinen Fragen der Saisonvogelzuge. Bio . Zbl., 50, 478-503 . Thorpe, W . H . (1954) . The process of song-learning in the Chaffinch as studied by means of the sound spectograph. Nature (Lond.), 173, 465 . Thorpe, W . H . (1956) . Learning and instinct in animals. London : Methuen . Thorpe, W . H. (1958) . The learning of song patterns by birds, with special reference to the song of the Chaffinch. Ibis, 100, in press . Accepted for publication 3rd March . 1958 .