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Serial order in wood thrush song
Anirn. Behav., 1985, 33, 1250-1265
Serial order in wood thrush song C A R L L. W H I T N E Y *
Rockefeller University FieM Research Center, Tyrrel Road, Millbrook, New York 12545, U.S.A.
Abstract. In a study of two captive male wood thrushes (Hylocichla rnustelina), I found that each bird had a preferred serial order of songs when it sang in isolation. This order could be disrupted by playback. When the stimulus was one of the subject's own songs, the bird often answered with the song that followed the stimulus song in the preferred order. This result supports the following hypothesis: the preferred serial order of songs delivered by a wood thrush is based, in part, on a mechanism by which one song facilitates, via a loop involving audition, the production of the next song in the sequence. I gained further insight into this mechanism by analysing the response of the birds to each other's songs and to experimentally altered songs.
Serial order in behaviour, to which Lashley (1951) drew attention, is one of the classic problems in the study of behavioural mechanisms. Finding bird song to be a convenient subject for analysis, ethologists have studied a number of species in which individual birds possess repertoires of two or more versions of the territorial advertising song. The emphasis has been on descriptive studies of undisturbed song (Isaac & Marler 1963; Beck 1971; Lemon & Chatfield 1971, 1973; Nelson 1973; Kroodsma 1975; Dobson & Lemon 1977, 1979; Hansen 1981; Whitney 1981; Slater 1983). We know that birds may alter the serial order of their songs in response to the song of other birds or to playback of recorded song, but most studies have been more concerned with the functional significance of vocal interactions between birds than with underlying behavioural mechanisms (Lemon 1968a, b; Bertram 1970; Kroodsma 1971, 1979; Verner 1975; Krebs et al. 1981; Todt 1981; Falls et al. 1982; Falls & d'Agincourt 1983; Schroeder & Wiley 1983). Two notable exceptions are Hinde (1958) and Todt (1975). In this paper I describe an experimental study of serial order in the song of two captive male wood thrushes (Hylocichla rnustelina). I present data showing how each bird responds to broadcast of the ongoing song of the other bird and to playback of various programmes of recorded song. A typical wood thrush song is composed of three phrases, labelled A, B and C (Fig. 1). The A phrase consists of one or more low-pitched sounds that resemble one of the call notes of the species (R. M. * Present address: 3744 West 12th Avenue, Vancouver. BC V6R 2N6, Canada.
Beck, personal communication). This paper is concerned only with the B and C phrases, which are the more complex parts of the song. The B phrase consists of loud flute-like notes, and the C phrase is usually a trill. B phrases are learned from conspecitics and can be classified into discrete types, while C phrases appear to be invented and are not amenable to classification (Whitney et al., unpublished data). Males have repertoires of 2-8 B phrases, several of which may be different versions of the same type, and 6-12 C phrases. In the songs of an individual bird, a given B phrase may be followed by different Cs at different times, giving a total of up to 25 different BC combinations (Beck 1971). In normal singing, each song has a different B and C phrase from the preceding one, and transitions between successive songs are non-random (Dobson & Lemon 1979). In an earlier study I found that when wood thrushes are presented with recorded song, they alter their singing to avoid matching B phrases that are identical or very similar to their own (Whitney & Miller 1983). A possible explanation for this response is that these stimuli activate an inhibitory mechanism that, in normal singing, prevents a given B phrase from being repeated in successive songs (Whitney & Miller 1983). An alternative explanation is that the stimuli activate mechanisms that directly facilitate transitions between given B phrases. The 'self-inhibition' hypothesis does not predict which B phrase will occur in the song immediately following the stimulus, but the 'direct-connection' hypothesis predicts that this phrase will be the one that, in normal singing, follows the B phrase that is identical, or very similar, to the stimulus. A major purpose of this paper is to test this prediction.
1250
Whitney." Serial order in wood thrush song
kHz 5-
kHz] 1,
-
t
L t ,tJ
3-
A
B
C
Figure l. Sonagram of a typical wood thrush song, showing A, B and C phrases.
METHODS
-.
Rlb
W2by
->5'
_-,.-,. W2bx
kHz
!1--=
Rab
The subjects (Red and White) were two of the three birds used in an earlier study (Whitney & Miller 1983). They were taken as nestlings in June 1980 and tutored at age 20-80 days with recorded B phrases. They were housed together during tutoring but were kept separately in acoustic isolation chambers during the period of song development in spring, 1981. The tutor tape contained 16 B phrases consisting of four synthetic variants each, of four previously defined types (Whitney et al., unpublished data). The variants were created with a computer system described by Zoloth et al. (1980). A single phrase of each type was altered to yield variants that were 0, 312, 624 and 936 Hz higher in frequency. Both birds developed a repertoire of five B phrases, copied from the tutor tape (Whitney & Miller, unpublished data). Red developed one version each of three types and two versions of the fourth type; White developed two versions each of two types and a single version of a third type (Fig. 2). Red developed seven C phrases, and White developed eight (Fig. 3), All are structurally normal, despite the lack of tutoring with C phrases (Whitney & Miller, unpublished data). The experiments were performed from 17 May to 12 July 1982, and from 29 January to 3 February 1983. Singing was induced during the latter period by subcutaneous implants of testosterone. Each bird was housed alone in an acoustic chamber and was confined to a cage with dimensions of 35 x 50 x 40 cm (width x length x height). A U t a h 10-cm loudspeaker was placed facing the cage, 10 cm from the shorter side. A Tandberg series-15 tape recorder was used to broadcast song (either recorded or live from the other bird) at a peak intensity of about 75 dB (re 20 N/m), 30 cm directly in fi-ont of the speaker.
1251
kHz.
R4bx
-----
W3b
W4bx
kHz
!1"-'": R4by
"-= W4by
Figure 2. Sonagrams of B phrasesof the two subjects, Red and White. Labels for B phrases of Red begin with an R, and those for B phrases of White begin with a W. The second symbol in each label indicates the phrase type. Thus, for example, phrases R3b and W3b are of the same type. The b in all labels indicates that the sounds are B phrases. Different versions of a given phrase type within a bird's repertoire are indicated by an 'x" or a 'y' at the end of the label.
The experiments with live broadcasts had three treatments: (1) Red could hear White, (2) White could hear Red, and (3) each bird could heat the other. The treatments, each lasting 10 rain, were conducted in random order on each of five different days. For the experiments with recorded song, each playback was of a single song and occurred with a latency of 0-5-2-0 s after the subject had completed one of its own songs. In one experimental design the subjects were allowed to sing a randomly determined number (3, 4, 5 or 6) of songs between each playback. In the other design all playbacks occurred after songs containing a specified B phrase. In some experiments a coin flip determined whether each repetition of the phrase would be followed by a stimulus or would be designated a control: in the others a coin flip determined which of two stimuli would be presented.
1252
Animal Behaviour 33, 4
kHz 97.-
tilltltLtL~,,
5-
pPq fr
1"
Rlc
R2c
Rae
R5c
R4c
97Rnlml
5-
lil '/ltlt,r,~
~
,
0"5 S
wilmeme~m, .,,,
31-
R7e
R6c 9-
,///,
Wlc
ffff!rrr,
75-
!1 tl I,
W2c 1
p
,
31-
i,J
I Pf~T~r,, II
II,
W3c
W4c
W5c
W6c
WTe
W8c
Figure 3. Sonagrams of C phrases of the two subjects, Red and White. In contrast to the labels for B phrases (Fig. 2), the second symbol is intended only to distinguish among the phrases within each bird's repertoire and not to indicate a phrase type (C phrases cannot be classified into discrete types).
For the experiments using recorded stimuli the data were taken down by hand; for the live broadcasts the two birds were recorded on separate channels of a Sony TC-D5M cassette recorder, and the recording was filmed using a Princeton Applied Research 4512 F F T real time spectrum analyser. Sonagrams were made with a Kay Elemetrics Corp. 7092A sound spectrograph, using the 8-8000-Hz frequency range and the flat shape and wide band settings.
RESULTS
Normal Serial Order In the live broadcast experiments (conducted from 17 to 24 May 1982), each subject was unable to hear the other bird during one of the three
treatments. The first-order transitions of B phrases for each bird during this 50-rain period (10 m i n x 5 days) are shown in Tables Ia and IIa. No statistical analysis is necessary to show that each bird had strong first-order preferences. For Red, 63-89~ of the transitions from each B phrase were to a single one of the other phrases. White showed even stronger preferences, with 95-100~ of the transitions from four of its five B phrases (W4by, W4bx, W2by, W3b) being to a single other phrase~ There were two common transitions from the fifth B phrase (W2bx). Inspection of the sequences showed that White typically sang several cycles of W3b W4by W 4 b x - W 2 b y - W 2 b x , then sang W4bx (instead of W3b) and carried on from that point in the usual cycle. Although Red was less predictable, he often sang several cycles of R 4 b x - R4by R3b R l b R2b before deviating. The deviations may have
Whitney." Serial order in wood thrush song Table I. First-order transitions of B phrases for Red
Table II. First-order transitions of B phrases for White
Following B phrase Preceding Bphrase
R4bx
R4by
Following B phrase
Rib
R2b
Preceding Bphrase
t0 83 0 l 3
16 4 83 0 18
6 1 6 Ill 0
W4by W4bx W2by W2bx W3b
52 147 1 18 27
53 17 160 3 114
27 14 53 276 0
R3b
(a) Not able to hear song of White
R4bx R4by R3b Rlb R2b
1 9 4 10 69
78 0 6 3 20
0 7 17 31 164
82 3 14 17 66
W4by
W4bx
W2by
W2bx
W3b
1 50 0 0 0
0 0 59 0 0
0 0 2 29 0
5 91 4 4 13
0 7 98 0 0
2 5 6 55 0
(a) Not ab~ to hear song of Red
(b) Able to hear song of White*
R4bx R4by R3b Rlb R2b
1253
0 0 1 0 32
31 0 0 16 0
(b) Able to hear song of Red
* But White not able to hear Red.
followed a pattern, but I did not investigate higherlevel transitions. Live B r o a d c a s t s
The serial order of B phrases became less stereotyped in each subject when the other bird could be heard singing (Tables Ib, IIb). The preferred transitions (Tables Ia, IIa) remained more c o m m o n than other transitions, but in all cases they declined as a percentage of the total transitions. F o r White, the number of cells in the transition table with non-zero entries increased dramatically from 9 to 21; for Red the increase was only from 21 to 23. More specific information about the disruption of normal serial order can be gained from the firstorder transitions between the B phrases of the two birds. F o r the treatments in which only one bird could hear the other, the observed transitions (from the independent singer to the bird that could hear) deviated significantly from the random expectation (Tables IIIa, IVa). An explanation for the deviations in certain cells is that the bird altered its normal serial order to avoid matching a B phrase very similar to one of its own (Whitney & Miller 1983). Before I began these experiments, I had determined that R2b was very similar to W2bx, R3b to W3b, R4bx to W4bx, and R4by to W4by. Although the phrases differed in details of structure (Fig. 2), they were similar in overall frequency, and I found them difficult to distinguish by ear. When Tables IIIa and IVa are condensed about the ceils
W4by W4bx W2by W2bx W3b
1 3 3 4 43
47 5 9 27 12
* But Red not able to hear White.
of interest, significant deviations (P < 0-05) occur in six out of eight cells. Red avoided matching W2bx, W3b, and W4bx (Z2=13.16, 6.66 and 12.20, respectively), and White avoided matching the counterparts of these three phrases (Z2 = 11.05, 8.69 and 13.29, respectively). It follows that the birds favoured answering with non-matching phrases. But they did not seem to choose at random from non-matching phrases. For example, White showed a marked preference for answering R2b with W4bx rather than with W2by, W3b or W4by (Table IVa). Similarly, Red favoured answering W2by, a phrase for which he had no counterpart, with R4by, yet avoided answering with R l b (Table IIIa). The first-order B phrase transitions for the treatment in which each bird could hear the other are shown in Tables IIIb and IVb. Overall, the observed values deviated from the random expectation, but deviations due to avoidance of matching were less predominant than in the treatments in which only one bird could hear the other. Red avoided matching W3b and W4bx; White did not avoid matching any of Red's B phrases. The deviations in other cells tended to be consistent with those in Tables IIIa and IVa. P l a y b a c k of the O t h e r Bird's S o n g
In an attempt to manipulate serial order more systematically, I presented playbacks of recorded song. Each subject was presented with the B phrases, each with an associated C phrase, of the
Animal Behaviour, 33, 4
1254
Table III. First-order transitions from the B phrases of White
to the B phrases of Red* Preceding B phrase of White
Following B phrase of Red Rl b
R2b
R3b
R4bx
R4by
(a) Red able to hear song of White, but White not able to hear Red
W2bx
10 4 (12.92) (14-36) W2by 6 13 (14.54) (16.15) W3b 10 16 (7-62) (8.46) W4bx 27 9 (12.23) (13.59) W4by 1 18 (6.69) (7.44) Difference between observed and df= 16, P<
10 11 21 (8.38) (11.73) (8.62) 15 28 1 (9.42) (13.19) (9-69) 0 2 5 (4.94) ( 6 - 9 1 ) (5.08) 7 2 8 (7.93) (11.10) (8.15) 3 6 1 (4-34) (6.07) (4.46) expected values: )( = 125.24, 0.001.
(b) Red able to hear song of White, and White able to hear Red
W2bx
3 ll 9 7 19 (10.70) (13.48) (8"56) (7.92) (8.34) W2by 0 20 25 22 1 (14.85) (18-71) (11.88) (10.99) (11.58) W3b 4 9 0 7 10 (6.55) (8.25) (5-24) (4.85) (5.11) W4bx 43 5 2 0 8 (12.66) (15-96) (10.13) (9.37) (9.88) W4by 0 18 4 l 1 (5-24) (6.60) (4.19) (3.88) (4.09) Difference between observed and expected values: Z2= 207.7 l, df= 16, P<0.001. * Expected values shown in parentheses.
other subject. By allowing the subjects to sing a randomly determined number of songs before each playback, I established the expectation that by chance alone the number of playbacks answered with a given B phrase should be proportional to the overall frequency of occurrence of that B phrase. The experiments were first conducted on 3-8 June 1982, and then repeated on 9-14 June. In both sets of experiments the results for Red are largely consistent with those obtained in the live broadcasts. Red's observed use of different B phrases to answer the stimuli differed in every case from the random expectation (Table V). As before, he avoided matching W2bx (though the results were statistically significant only in the first replicate), W3b and W4bx; he also avoided matching W4by, a trend that did not reach statistical significance in the live broadcasts. Finally, the results
were consistent with the earlier ones in cases where deviations from expected values could not be explained as avoidance of matching (compare Tables III and V). By contrast, White's observed use of different B phrases to answer the stimuli differed in only two cases from the random expectation (Table VI). White matched R2b, R3b and R4bx slightly less often than expected in each replicate, and R4by slightly more often than expected. N o n e of the results reached significance. Further analysis shows that White was more likely to deviate from his preferred sequences immediately following a stimulus than at other times (Table VII). This occurred even in the treatment where the stimulus was a B phrase type that was not in White's repertoire (Rlb). In the four treatments where the stimulus was very similar
Whitney." Serial order in wood thrush song
1255
Table IV. First-order transitions from the B phrases of Red to
the B phrases of White* Preceding B phrase of Red
Following B phrase of White W2bx
W2by
W3b
W4bx
W4by
(a) White able to hear song of Red, but Red not able to hear White
Rib
14 5 8 13 2 (8.37) (12.29) (6.15) (10.07) (5-12) R2b 2 13 9 26 3 (10.56) (15-51) (7.76) (12.71) (6-46) R3b 10 13 0 5 14 (8-37) (12.29) (6.15) (10.07) (5.12) R4bx 8 31 3 2 5 (9.76) (14.34) (7.17) (11.75) (5.98) R4by 15 10 16 13 6 (11.95) (17.56) (8.78) (14.39) (7-32) Difference between observed and expected values: Z2= 100.42, df= 16, P <0.001. (b) White able to hear song of Red, and Red able to hear White
Rlb
22 10 4 7 5 (10.36) (13.96) (6-34) (12-90) (4.44) R2b 6 21 11 35 I (10-15) (21.52) (9'78) (t9.89) (6-85) R3b 7 12 4 9 8 (8.63) (11.63) (5.29) (10-75) (3.70) R4bx 8 19 2 4 4 (7.99) (10.76) (4-89) (9-94) (3-42) R4by 6 4 9 6 3 (6.04) (8.14) (3.70) (7"52) (2.59) Difference between observed and expected values: Z2= 63.54, d f - 16, P < 0.001. * Expected values shown in parentheses.
to one of White's own B phrases, the deviations tended to occur when the normal serial order would have resulted in matching (Table VII). Playback of Own Song
When presented with the other bird's songs, both in the live broadcasts and in the playbacks, each subject tended to avoid matching B phrases that were very similar to its own, and to favour answering with certain other phrases. In this section I test the prediction of the direct-connection hypothesis that the birds should favour answering one of their own songs with the B phrase that in normal singing follows the stimulus B phrase. The stimuli were the same BC combinations used in the above experiments. By random choice among each bird's B phrases, all stimuli for Red were presented
after songs containing R3b, and all stimuli for White after songs containing W2by. Each trial involving a given stimulus continued until the subject had sung 50 songs containing the specified phrase. A coin flip decided whether each song would be followed by the stimulus or would be designated a control. The experiments were conducted first in June 1982, and then repeated in January and February 1983. The results for Red gave only partial and inconsistent support for the hypothesis (Table VIII). In the controls, R3b was followed by R l b 73-100% of the time. In the first replicate of the experiment, Red made a significant switch away from R l b to answer with another B phrase only when the stimulus was R l b . As predicted by the hypothesis, it switched to the phrase (R2b) that
Animal Behaviour, 33, 4
1256
Table V. Response of Red to random playbacks of White's songs Number of answers Stimulus
Replicate Obs:
Rlb
R2b
R3b
R4bx
R4by
10
5
15
12
33
1 Exp:
)~2
p
23.62
<0-001
26.49
<0.001
56.12
<0.001
37-68
<0.001
24.12
<0.001
35.00
<0.001
13.44
<0.01
21.19
<0.001
38.29
<0.001
56.93
<0.001
1 5 . 9 3 13.72 14.60 13.94 16.81
W2bx W7c Obs:
6
7
16
14
32
2 Exp: Obs:
1 7 . 4 6 12.76 15.00 13.88 15.90 1
12
16
41
5
1 Exp:
14-55 15-45 15.22 16.12 13.66
W2by-W 1c Obs:
3
28
18
24
2
2 Exp: Obs:
16.01 14.86 15.09 15.32 13.72 14
35
6
6
14
1 Exp:
1 7 . 0 9 19-08 13-09 13-76 11.98
W3b W3c Obs:
15
36
7
5
12
2 Exp: Obs:
15.81 16.04 13.55 14.68 14.91 20
15
19
0
5
8.36
5.65
6
15
1 Exp:
17.18 16.05 11.75
W4bx-W5c Obs:
14
30
10
2 Exp: Obs:
16-92 15.09 14.86 13.72 14.41 2
37
11
19
5
1 Exp:
16.13 18.33 14.36 13.25 11.93
W4by W4c Obs:
1
40
10
22
2
2 Exp:
1 7 . 9 3 17.36 13.89 15.05 11.57
followed R i b in normal sequences. The results were similar for the second replicate o f this treatment. Interestingly, in the first replicate o f the R3b treatment, Red answered the stimulus even more often t h a n expected with R l b . This might be interpreted as s u p p o r t for the hypothesis, supposing that the stimulus reinforced the facilitative connection to R l b by providing an additional sensory dose o f R3b. In the second replicate o f this treatment there was no possibility o f a switch
toward answers with R l b since this phrase always followed R3b in the controls. The results for the R2b treatment support the hypothesis in the second replicate but not in the first. Finally, the results for the second replicate of the R4by treatment show an inexplicable switch to anwers with a phrase (R2b) that only rarely followed R4by in normal sequences (Table Ia). With only a single exception, the results for White clearly support the hypothesis (Table IX).
Whitney." Ser&l order in wood thrush song
1257
Table V|. Response of White to random playbacks of Red's songs Number of answers Stimulus
Replicate
W2bx
W2by
W3b
W4bx
W4by
Obs:
23
13
9
18
12
Exp:
16.01
16.01
Obs:
19
15
Exp:
15-69
Obs:
14
Exp:
15-39
1 13-58 15.81
X~
P
5-65
> 0.20
5.99
>0-20
9-65
<0-05
9,05
>0.05
4.62
> 0.30
4,71
>0.30
3-84
>0-30
5,39
>0.20
11.52
<0.05
6.00
>0.10
13-58
R 1I~R4c 20
10
11
15-90
14.18
I4
6
16.04
13,22
2 1 5 . 0 4 14.18 26
15
1 16"69 1 3 . 6 6
R21~R5c Obs:
1[
Exp:
15.27
Obs:
15
Exp:
15-94
Obs:
10
Exp:
15-84
24
9
21
10
2 16.37 I4-16 15.93 14
10
15
13.27 21
1 1 6 . 3 9 12-57 1 6 . 1 7
13.92
R3b-R7c 18
11
17
19
2 Obs:
16.06 13.86 14.74
20
17
16
14.52
13
9
16-04
13-55
11
17
14.26
13-80
1 Exp:
15"57
16"27 13.55
Obs:
12
Exp:
16"10
Obs:
5
17
Exp:
16-04
15.81
Obs:
15
25
Exp:
16-74
R4bx-R6c 23
12
2 1 6 . 5 6 14.26 14
22
17
1 14-01 1 5 . 8 1
13.33
R4by R3c 10
11
14
2 17,20 1 4 . 2 2 1 4 . 4 5
The exception is the second replicate o f the W4by treatment, in which White did not deviate from his normal sequence.
I m p o r t a n c e o f B and C P h r a s e s
The stimuli in the above experiments contained both B and C phrases. In this section I show how these two parts o f the song, presented separately and in natural and synthetic combinations, affect serial order.
12,39
Table X gives the results o f three experiments with White. The stimuli in each case were presented after songs containing W2bx. In the first experiment, the stimuli were two o f White's songs that differed only in the C phrase. The first song (W2bx W7c) was usually followed in normal sequences by W3b, and the second (W2bx-WSc) was followed by W4bx. Both transitions were c o m m o n (Table IIa). As predicted by the direct-connection hypothesis, significantly m o r e answers with W4bx occurred in response to the second song. Presentation o f the C
Animal Behaviour, 33, 4
1258
Table VII. Further analysis of White's response to random playback of Red's songs Number of deviations immediately Incidence of normal and following the abnormal ordering of B phrases stimulus that resulted in Not immediately avoidance following Immediately following of the stimulus the stimulus matching Stimulus R 1l~R4c R21~R5c R31~R7c R4bx-R6c R4b~R3c
Normal
Abnormal
Normal
Abnormal
Observed
Expected
567 533 521 504 507
0 0 2 2 0
144 140 137 140 137
6 10 13 10 13
-6 9 7 t1
2.20 2.76 1-82 2.44
'Abnormal ordering of B phrases, immediately following the stimulus' refers to all occasions when the first song after the stimulus deviated from the preferred order; 'abnormal ordering not immediately following the stimulus' refers to all other deviations. The expected number of deviations immediately following the stimulus that resulted in avoidance of matching was calculated as follows: (overall proportion of stimuli that were immediately followed by a deviation from the preferred order) x (number of stimuli that would have been matched if no deviation had occurred).
phrases alone, in the next experiment, led to similar results. The final experiment shows that the response to songs containing a very similar B phrase (R2b), of Red, also varied with C phrase. In a set of four experiments, the response of Red to his own B phrase and associated C phrase ( R 2 b R6c) versus that to a very similar B phrase and its associated C phrase (W2bx WSc) of White was explored in detail (Table XI). All stimuli were presented after songs containing R2b. The results for the first experiment show that Red answered R 2 b - R 6 c mostly with R4bx, as would be expected from its preferred B-phrase transitions (Table Ia), but answered W 2 b x - W 8 c mostly with R4by. This response to White's song is similar to that given in earlier experiments (Table VI). Removal of the C phrases from the stimuli, in the second experiment, had little effect on the response. Removal of the B phrases, leaving just the Cs, may have had some effect, but the responses to the two stimuli remained significantly different. In the final experiment each B phrase was combined with the C phrase of the other bird (yielding R2b W8c and W2bx-R6c). Red responded to both artificial songs by answering mostly with R4bx. Thus the response normally given to the bird's own B and C phrases,
presented either separately or together, appeared to override that given to the other bird's phrases. A similar set of five experiments with Red was conducted using the songs R 4 b y - R 3 c and W 4 b y W4c (Table XII). The results of the first experiment show that the response was significantly different to the complete songs. Red answered R 4 b y - R 3 c with R3b and R l b , and answered W 4 b y - W 4 c with R2b and R3b. The tendency to answer White's song with R2b is consistent with the results of earlier experiments (Tables IVa, V). In the second experiment the B phrases were presented alone, and Red continued to answer W4by more with R2b. Interestingly, removal of the C phrase from R4by appeared to diminish the response with R1. In contrast to the results of the previous series of experiments (Table XI), there was no difference in response to the isolated C phrases. Red favoured answering both phrases with R3b, and did not answer at all with R2b. In the fourth experiment, however, presentation of the synthetic song, R 4 b y W4c, resulted in a partial reinstatement of the response with R2b. Taken together, the results of the third and fourth experiments indicate that, to induce a response with R2b, the C phrase, W4c, must be presented in combination with a B phrase.
Whitney." Serial order in wood thrush song
1259
Table VIII. Response of Red to playback of his own song (presented after R3b) Percentage of answers Stimulus
Replicate
N
Rlb
R2b
R3b
R4bx
R4by
23
Playback:
95"7
27
Control:
23
Playback:
27
Control:
100-0
22
Playback:
72.7
28
Control:
92-9
20
Playback:
45-0
55.0
30
Control:
93'3
3.3
3-3
28
Playback:
100.0
22
Control:
72.7
13.6
9-1
25
Playback:
100.0
25
Control:
100.0
26
Playback:
96.2
24
Control:
75.0
22
Playback:
81.8
28
Control:
96.4
29
Playback:
86.2
21
Control:
100-0
22
Playback:
27.3
28
Control:
96.4
4.3
1
<0.001 92.6
3.7
3.7
R i1~R4c 95.7
4.3
2
<0.001 13.6
13.6
1
NS
3.6
3.6
R2b-R5c 2
<0.001
1
<0.05 4.5
R31~R7c 2
NS
3.8
1
NS
16.7
8.3
R4bx-R6c 4-5
13.6
2
NS
3.6 3.4
6.9
1
3.4 NS
R4by-R3c 59.1
13.6
2
<0.001 3.6
Probability values are based on Fisher's test, one-tailed. For application of the test, response data were lumped into two categories: (1) R I b (the phrase that most commonly followed R3b in normal sequences), and (2) all other phrases.
Both synthetic songs ( R 4 b y - W 4 c and W 4 b y - R 3 c ) were presented in the fifth experiment. The response to R 4 b y - W 4 c included an even larger p r o p o r t i o n o f answers with R2b than in the previous experiment. The response to W 4 b y - R 3 c was almost evenly divided a m o n g answers with R l b , R3b and R4bx. I c a n n o t account for the tendency to answer with R4bx, but the answers with R l b may have been induced by the C phrase
R3c. Recall that removal o f this phrase from R4by completely eliminated the response with R l b in the second experiment.
Self-inhibition
of B P h r a s e s
Self-inhibition has been invoked to account for the m a n n e r in which wood thrushes cycle through
Animal Behaviour, 33, 4
1260
Table IX. Response of White to playback of his own song (presented after W2by) Percentage of answers Stimulus
Replicate
N
W2bx
22
Playback:
28
Control:
100.0
25
Playback:
40.0
25
Control:
100.0
23
Playback:
100-0
27
Control:
100'0
27
Playback:
100"0
23
Control:
100.0
24
Playback:
54.2
26
Control:
100.0
26
Playback:
57-7
24
Control:
100.0
30
Playback:
70-0
20
Control:
100-0
24
Playback:
33 '3
26
Control:
100"0
29
Playback:
34.5
21
Control:
100.0
25
Playback:
100.0
25
Control:
100.0
W2by
W3b
W4bx
W4by
P
36.4
63-6
<0'001
1
W2bx-W7c 60'0 <0"001
2
N8
l
W2by-W 1c NS
2 12"5
8"3
25.0 <0.01
1
W3b-W3c 3-8
38.5 <0.001
2 30.0
<0.01
1
W4bx-W5c 66.7 <0-00l
2 65"6
< 0.001
1
W4by-W4c NS
2
Statistics as in Table VIII, with the first response category being W2bx (the phrase that almost invariably followed W2by in normal sequences).
their B a n d C phrase repertoires (Beck 1971). Successive utterances o f a given phrase are generally separated by several songs c o n t a i n i n g other phrases. To test for self-inhibition o f B phrases, I did a series of five experiments with Red. In each experiment the stimulus song ( R l b - R 4 c ) was presented after a different one of the bird's five B phrases. I reasoned t h a t if self-inhibition dissipates gradually after p r o d u c t i o n o f a phrase, the tendency to answer the stimulus B phrase with the B
phrase t h a t followed it in n o r m a l sequences (R2b) should vary systematically across the treatments. The predicted trend a n d the results are s h o w n in Table XIII. W h e n the stimulus was presented after R2b the bird never answered with R2b. In each of the o t h e r four treatments it answered mostly with R2b, but, c o n t r a r y to the prediction, the percentage of the playbacks answered with this phrase did n o t increase as a function of the n u m b e r of o t h e r B phrases p r o d u c e d since the last utterance of R2b.
Whitney." Serial order in wood thrush song
1261
Table X. Response of White to playback of different combinations of B and C phrases
(stimuli presented over W2bx) Percentage of answers Experiment
Stimulus
N
W2bx-W7c
22
W2bx W8c
28
no B-W7c
21
no B-W8c
W2bx
W2by
W3b
W4bx
18"2
77-3
4.5
42.9
57.1
90.5
4'8
29
65-5
34.5
R2b-R5c
25
64-0
36.0
R2t~R6c
25
100.0
W4by
P <0"001
1
4.8
< 0"02
2
<0.01
3
Probability values are based on Fisher's test, one-tailed for experiments 1 and 2 and twotailed for experiment 3. The test was applied only to the data for W3b and W4bx, the two phrases that followed W2bx in normal sequences.
Table XI. Response of Red to playback of different combinations of B and C phrases
(stimuli presented after R2b) Percentage of answers Experiment
Stimulus
N
Rlb
R2b-R8c
20
5.0
W2bx-WSc
R2b
R3b
R4bx
R4by
80.0
15-0
30
23.3
76.7
R2b-no C
22
90'9
9' 1
W2bx-no C
28
25.0
75-0
no B-R8c
27
11.1
77-8
3.7
no B-W8c
23
8,7
56.5
34-8
R21>W8c
25
84.0
16,0
W2bx-R8c
25
80.0
20-0
I
P <0.001
2
<0.001 7.4
3
<0-01
4
NS
Probability values are based on Fisher's test, two-tailed for experiments 1 and 4 and one-tailed for experiments 2 and 3. The test was applied only to the data for R4bx and R4by, the two phrases that most commonly followed R2b in the experiments.
DISCUSSION In summary, the results show that when each subject sang in isolation it had a preferred order o f B phrases (Tables Ia, IIa). This order was disrupted
when the subject could hear the ongoing song o f the other bird (Tables Ib, lib). A partial explanation for the disruption is that each bird tended to avoid matching B phrases that were very similar to its own. This, however, does not account for the
Animal Behaviour, 33, 4
1262
Table XIL Response of Red to playback of different combinations of B and C phrases (stimuli presented after R4by) Experiment
Stimulus
N
Rlb
R2b
R3b
R4bx
R4by-R3c
23
34.8
56.5
8-7
W4by W4c
27
55-6
44.4
R4by no C
24
4.2
95.8
W4by-no C
26
38.5
61-5
no B-R3c
29
6.9
93" 1
no B W4c
21
4.8
95.2
R4by-R3c
25
48.0
52-0
R4by-W4c
25
4.0
2 4 . 0 72.0
R4by-W4c
31
3.2
5 1 . 6 45.2
W4by R3c
19
R4by
1
P <0.001
2
<0.01
3
NS
4
<0.01
5
<0.001 31"6 1 0 . 5 2 6 . 3
31.6
Probability values for experiments 2 and 3 are based on Fisher's test, one-tailed. Probability values for experiments 1, 4 and 5 are based on the ;(2 test. Categories were combined as necessary to ensure sufficiently large expected values, except for experiment 4, where this would have rendered the test meaningless. For experiments 1 and 5 the categories were R2b, R3b, and all other phrases combined (X2= 89.56; Z2 - 22.90, respectively). Note that for experiment 4 two expected values were less than 5.0 (Zz= 12.21).
Table XIII. Response of Red to playback of a stimulus song (Rib R4c) at different points in his normal sequence of songs B phrase of song immediately preceding stimulus
N
Average number of songs since last utterance of R2b
R 1b R3b R4by R4bx R2b
31 21 21 23 29
3-70 3-57 3-25 2.23 0
consistently large deviations from expected firstorder transitions between certain other B phrases. The same general patterns o f disruption occurred when Red was presented, at r a n d o m intervals~ with recorded songs o f White (Table V). In the converse experiments, White's response was much more subtle (Table VI), and additional analysis was necessary to reveal a tendency to avoid matching very similar B phrases (Table VII).
Predicted response with R2b
~ Answers with R2b
Greatest
93.5 66.7 71-4 95.7 0
. Least
The self-inhibition hypothesis can account for avoidance o f matching but not for the other consistent patterns of answering shown by the two birds in the live broadcasts and r a n d o m playbacks. The direct-connection hypothesis is m o r e comprehensive. It predicts that the B phrase used to answer the other bird's song will be the one that, in normal singing, follows the B phrase that is very similar to the stimulus. This prediction is clearly not upheld
Whitney: Serial order in wood thrush song
in the results of the live broadcasts and random playbacks of the other bird's songs (Tables III, IV, V, VI). For example, Red favoured answering W3b with R2b, yet in undisturbed sequences he usually sang R l b after R3b, a phrase very similar to W3b (Table Ia). The direct-connection hypothesis received mixed support when the stimulus was one of the bird's own songs. Except for one replicate of one experimental treatment (W4by), White always showed a significant tendency to answer with the B phrase that followed the stimulus phrase in normal sequences (Table IX). For Red the only results that supported the hypothesis in both replicates were for the R 1b treatment (Table VIII). Note, however, that R l b was presented immediately before that phrase would have occurred in the normal sequence, and that Red responded by skipping ahead just one song in the normal sequence. One could argue that this response is also consistent with an elaboration of the self-inhibition hypothesis: following stimulus-induced inhibition, the B phrase that has the highest level of causal factors, and therefore will be sung next, is the one that follows the inhibited phrase in normal sequences. In the second replicate of the R2b treatment Red did, however, respond in a way consistent with only the direct-connection hypothesis. He answered mainly with the phrase (R4bx) that followed R2b in normal sequences. Similar results were obtained in two experiments not shown in Table XI. In one experiment the stimulus R l b (with R4c) was presented after R4bx and in the other it was presented after R4by. In both cases Red answered mainly with the phrase (R2b) that followed R1 b in normal sequences (first experiment: 22/23 answers with R2b versus 1/27 in control; second experiment: 15/21 answers with R2b versus 0/27 in control). In these experiments the birds may have responded to either the B phrase or the C phrase of the stimulus song, or to both. The results of further experiments indicate that both phrases are important (Tables X, XI, XII). An interesting case of direct connections based on C phrases is shown for White in Table X. Consistent with the transitions observed in normal sequences, the experimental results show that the response was different to two C phrases, both when the phrases were presented alone and when they were combined with a B phrase. The two sets of experiments with Red, in which
1263
both birds' B and C phrases were used as stimuli, show that the response depends on both types of phrases, but that the details may differ. In the first set of experiments the difference in response to two very similar B phrases, each with an associated C phrase, persisted when the B phrases were presented alone and also when the C phrases were presented alone (Table XI). By contrast, in the second set, the difference in response to the BC combinations was altered when the B phrases were presented alone, and eliminated when the C phrases were presented alone (Table XII). Thus the C phrases had an effect only when combined with B phrases. Overall, the results bearing on the direct-connection hypothesis may be summarized as follows. When presented with his own song, White nearly always responded in a way consistent with the hypothesis. In the only case where he did not, his normal order of B phrases was unaffected by the stimulus (Table IX). Red was less consistent, but again, most of the results that were contrary to those predicted by the hypothesis indicate a lack of any response to the stimulus (Table VIII). In the only exception, Red made a significant switch to answers with a B phrase that did not follow the stimulus B phrase in normal sequences. For both birds the results varied in some treatments between the first and second replicates. I conclude that normal serial order of B phrases in the two birds depended, at least in part, on direct facilitative connections. From the results of the later experiments it is clear that these connections involved C phrases as well as B phrases (Tables X, XI, XII). The fact that transitions between some B phrases were not disrupted by playback need not be taken as evidence against direct connections. One possibility is that such mechanisms underlie these transitions but do not depend upon auditory feedback. The difference between the results of the first and second replicates of some treatments would then imply that the role of audition is not constant. Now consider the direct-connection hypothesis in light of the responses given by each subject to the other bird's song. Both birds avoided matching B phrases very similar to their own, and favoured answering with certain other phrases. But these phrases were often not the ones predicted by the direct-connection hypothesis. For example, Red consistently avoided matching W2bx with R2b and instead favoured answering with R4by (Table III,
1264
Animal Behaviour, 33, 4
V). This is in contrast to his tendency to answer R2b with R4bx, the B phrase that followed R2b in normal sequences. The difference in response to the two B phrases persisted even when they were presented alone, without C phrases (Table X1). The mechanism that controls transitions between B phrases cannot be as simple as previously implied. One part of the mechanism appears to treat very similar B phrases as equivalent, resulting in avoidance of matching, but another part discriminates between the phrases and facilitates different transitions. Facilitative connections are not the only type of mechanism underlying serial order in wood thrush song. Self-inhibition also appears to be important. The results of experiments with Red indicate a quickly-dissipating form of self-inhibition, sufficient to account for the immediate switches between different B phrases (Table XIII). The question remains, however, as to why the bird typically repeated a particular B phrase only after having sung all four of his other phrases. Perhaps a longer lasting form of self-inhibition operated during the development of a stable serial order, which was then maintained by facilitative connections. A result obtained in one of the earlier experiments can also be interpreted as evidence for selfinhibition. When White was presented with W4bx (and W5c) after he sang W2by, he sometimes answered with W2by, thus singing this phrase twice in succession (Table IX). This supports the directconnection hypothesis, since W2by followed W4bx in normal sequences. In the first replicate of the experiment, however, I noticed that the answer was often an incomplete song. The second repetition of the trill in W2by, and the entire C phrase were deleted. I kept a record of such songs in the second replicate and found that 9 of the 16 answers with W2by were incomplete. N o n e of the songs immediately preceding playbacks was incomplete. Thus the artificial facilitation of W2by was opposed by self-inhibition, with neither mechanism prevailing. It appears that the mechanisms underlying serial order in wood thrush song include both facilitative connections and self-inhibition. Slater (1983) came to a similar conclusion in a non-experimental study of chaffinch (Fringilla coelebs) song. He suggested that the relative importance of these two mechanisms may vary between individual birds. I have not investigated self-inhibition in detail, but the results presented in this paper indicate that the
importance of facilitative connections, at least where they are mediated by audition, varies not only between individual wood thrushes but between the phrases within the repertoire of a single bird.
ACKNOWLEDGMENTS I thank A. Dufty, P. Marler, J, Miller, P. Slater and R. Suter for commenting on earlier versions of the manuscript. The research was supported by an N I M H postdoctoral fellowship (MH08291) to the author and by an N I H grant to Rockefeller University (RR07065-15). The birds were collected and held in captivity in accordance with Federal scientific collecting permit P R T 2 - 1 3 9 4 N Y and State of New Y o r k scientific collector's licence SC 1916.
REFERENCES Beck, R. M. 1971. Sequence patterning of wood thrush song. Am. Zool., II, 66 (Abstract). Bertram, B. C. R. 1970. The vocal behaviour of the Indian hill mynah, Gracula religiosa. Anim. Behav. Monogr., 3, 79 102. Dobson, C. W. & Lemon, R. E. 1977. Markovian versus rhomboidal patterning in the song of Swainson's thrush. Behaviour, 62, 276-297. Dobson, C. W. & Lemon, R. E. [977. Markov sequences in songs of American thrushes. Behaviour, 68, 86-105. Falls, J. B. & d'Agincourt, L. G. 1983. Why do meadowlarks switch song types? Can. J. Zool., 60, 3400-3408. Falls, J. B., Krebs, J. R. & McGregor, P. K. 1982. Song matching in the great tit (Parus major): the effect of similarity and familiarity. Anita. Behav., 30, 997--1009. Hansen, P. 1981. Song organization in a chaffinch (Fringilla eoelebs). Natura Jutland., 19, 107 120. Hinde, R. A. 1958. Alternative motor patterns in chaffinch song. Anim. Behav., 6, 211 218. Isaac, D. & Marler, P. 1963. Ordering of sequences of singing behaviour of mistle thrushes in relationship to timing. Anim. Behav., 11, 179-188. Krebs, J. R., Ashcroft, R. & van Orsdol, K. 1981. Song matching in the great tit Parus major L. Anim. Behav., 29, 918-923. Kroodsma, D. E. 1971. Song variations and singing behavior in the rufous-sided towhee, Pipilo erythrophthalmus oregonus. Condor, 73, 303 308. Kroodsma, D. E. 1975. Song patterning in the rock wren. Condor, 77, 294-303. Kroodsma, D. E. 1979. Vocal dueling among male marsh wrens: evidence for ritualized expressions of dominance/subordinance. Auk, 96, 506-515. Lashley, K. 1951. The problem of serial order in behavior. In: Cerebral Mechanisms in Behavior (Ed. by L. A. Jeffress), pp. 112-136. New York: Wiley.
Whitney: Serial order in wood thrush song Lemon, R. E. 1968a. Coordinated singing by blackcrested titmice. Can. J. Zool., 46, 1163-1167. Lemon, R. E. 1968b. The relationship between organization and function of song in cardinals. Behaviour, 32, 158-178. Lemon, R. E. & Chatfield, C. 1971. Organization of song in cardinals. Anim. Behav., 19, 1 17. Lemon, R. E. & Chatfield, C. 1973. Organization of song of rose-breasted grosbeaks. Anim. Behav., 21, 2 8 4 4 . Nelson, K. 1973. Does the holistic study of behavior have a future? In: Perspectives' in Ethology (Ed. by P. P. G. Bateson & P. H. Klopfer), pp. 281 328. New York: Plenum Press. Schroeder, D. J. & Wiley, R. H. 1983. Communication with shared song themes in tufted titmice. Auk, 100, 414424. Slater, P. J. B. 1983. Sequences of song in chaffinches. Anim. Behav., 31, 2 7 ~ 2 8 1 . Todt, D. 1975. Short term inhibition of outputs occurring in the vocal behaviour of blackbirds (Turdus merula m.
1265
L.). J. comp. Physiol., 98, 28%306. Todt, D. 1981. On functions of vocal matching: effect of counter-replies on song post choice and singing. Z. Tierpsychol., 57, 73 93. Verner, J. 1975. Complex song repertoire o f male longbilled m a r s h wrens in eastern Washington. Living Bird, 14, 263-300. Whitney, C. L. 1981. Patterns of singing in the varied thrush II. A model of control. Z. Tierpsychol., 57, 141 162. Whitney, C. L. & Miller, J. 1983. Song matching in the wood thrush (Hylociehla mustelina): a function of song dissimilarity. Anita. Behav., 31, 4 5 7 4 6 1 . Zoloth, S., Dooling, R. J., Miller, R. & Peters, S. 1980. A minicomputer system for the synthesis of animal vocalizations. Z. Tierpsychol., 54, 151-162.
(Received 19 June 1984; revised 29 October 1984; MS. number." A4328)
Serial order in wood thrush song C A R L L. W H I T N E Y *
Rockefeller University FieM Research Center, Tyrrel Road, Millbrook, New York 12545, U.S.A.
Abstract. In a study of two captive male wood thrushes (Hylocichla rnustelina), I found that each bird had a preferred serial order of songs when it sang in isolation. This order could be disrupted by playback. When the stimulus was one of the subject's own songs, the bird often answered with the song that followed the stimulus song in the preferred order. This result supports the following hypothesis: the preferred serial order of songs delivered by a wood thrush is based, in part, on a mechanism by which one song facilitates, via a loop involving audition, the production of the next song in the sequence. I gained further insight into this mechanism by analysing the response of the birds to each other's songs and to experimentally altered songs.
Serial order in behaviour, to which Lashley (1951) drew attention, is one of the classic problems in the study of behavioural mechanisms. Finding bird song to be a convenient subject for analysis, ethologists have studied a number of species in which individual birds possess repertoires of two or more versions of the territorial advertising song. The emphasis has been on descriptive studies of undisturbed song (Isaac & Marler 1963; Beck 1971; Lemon & Chatfield 1971, 1973; Nelson 1973; Kroodsma 1975; Dobson & Lemon 1977, 1979; Hansen 1981; Whitney 1981; Slater 1983). We know that birds may alter the serial order of their songs in response to the song of other birds or to playback of recorded song, but most studies have been more concerned with the functional significance of vocal interactions between birds than with underlying behavioural mechanisms (Lemon 1968a, b; Bertram 1970; Kroodsma 1971, 1979; Verner 1975; Krebs et al. 1981; Todt 1981; Falls et al. 1982; Falls & d'Agincourt 1983; Schroeder & Wiley 1983). Two notable exceptions are Hinde (1958) and Todt (1975). In this paper I describe an experimental study of serial order in the song of two captive male wood thrushes (Hylocichla rnustelina). I present data showing how each bird responds to broadcast of the ongoing song of the other bird and to playback of various programmes of recorded song. A typical wood thrush song is composed of three phrases, labelled A, B and C (Fig. 1). The A phrase consists of one or more low-pitched sounds that resemble one of the call notes of the species (R. M. * Present address: 3744 West 12th Avenue, Vancouver. BC V6R 2N6, Canada.
Beck, personal communication). This paper is concerned only with the B and C phrases, which are the more complex parts of the song. The B phrase consists of loud flute-like notes, and the C phrase is usually a trill. B phrases are learned from conspecitics and can be classified into discrete types, while C phrases appear to be invented and are not amenable to classification (Whitney et al., unpublished data). Males have repertoires of 2-8 B phrases, several of which may be different versions of the same type, and 6-12 C phrases. In the songs of an individual bird, a given B phrase may be followed by different Cs at different times, giving a total of up to 25 different BC combinations (Beck 1971). In normal singing, each song has a different B and C phrase from the preceding one, and transitions between successive songs are non-random (Dobson & Lemon 1979). In an earlier study I found that when wood thrushes are presented with recorded song, they alter their singing to avoid matching B phrases that are identical or very similar to their own (Whitney & Miller 1983). A possible explanation for this response is that these stimuli activate an inhibitory mechanism that, in normal singing, prevents a given B phrase from being repeated in successive songs (Whitney & Miller 1983). An alternative explanation is that the stimuli activate mechanisms that directly facilitate transitions between given B phrases. The 'self-inhibition' hypothesis does not predict which B phrase will occur in the song immediately following the stimulus, but the 'direct-connection' hypothesis predicts that this phrase will be the one that, in normal singing, follows the B phrase that is identical, or very similar, to the stimulus. A major purpose of this paper is to test this prediction.
1250
Whitney." Serial order in wood thrush song
kHz 5-
kHz] 1,
-
t
L t ,tJ
3-
A
B
C
Figure l. Sonagram of a typical wood thrush song, showing A, B and C phrases.
METHODS
-.
Rlb
W2by
->5'
_-,.-,. W2bx
kHz
!1--=
Rab
The subjects (Red and White) were two of the three birds used in an earlier study (Whitney & Miller 1983). They were taken as nestlings in June 1980 and tutored at age 20-80 days with recorded B phrases. They were housed together during tutoring but were kept separately in acoustic isolation chambers during the period of song development in spring, 1981. The tutor tape contained 16 B phrases consisting of four synthetic variants each, of four previously defined types (Whitney et al., unpublished data). The variants were created with a computer system described by Zoloth et al. (1980). A single phrase of each type was altered to yield variants that were 0, 312, 624 and 936 Hz higher in frequency. Both birds developed a repertoire of five B phrases, copied from the tutor tape (Whitney & Miller, unpublished data). Red developed one version each of three types and two versions of the fourth type; White developed two versions each of two types and a single version of a third type (Fig. 2). Red developed seven C phrases, and White developed eight (Fig. 3), All are structurally normal, despite the lack of tutoring with C phrases (Whitney & Miller, unpublished data). The experiments were performed from 17 May to 12 July 1982, and from 29 January to 3 February 1983. Singing was induced during the latter period by subcutaneous implants of testosterone. Each bird was housed alone in an acoustic chamber and was confined to a cage with dimensions of 35 x 50 x 40 cm (width x length x height). A U t a h 10-cm loudspeaker was placed facing the cage, 10 cm from the shorter side. A Tandberg series-15 tape recorder was used to broadcast song (either recorded or live from the other bird) at a peak intensity of about 75 dB (re 20 N/m), 30 cm directly in fi-ont of the speaker.
1251
kHz.
R4bx
-----
W3b
W4bx
kHz
!1"-'": R4by
"-= W4by
Figure 2. Sonagrams of B phrasesof the two subjects, Red and White. Labels for B phrases of Red begin with an R, and those for B phrases of White begin with a W. The second symbol in each label indicates the phrase type. Thus, for example, phrases R3b and W3b are of the same type. The b in all labels indicates that the sounds are B phrases. Different versions of a given phrase type within a bird's repertoire are indicated by an 'x" or a 'y' at the end of the label.
The experiments with live broadcasts had three treatments: (1) Red could hear White, (2) White could hear Red, and (3) each bird could heat the other. The treatments, each lasting 10 rain, were conducted in random order on each of five different days. For the experiments with recorded song, each playback was of a single song and occurred with a latency of 0-5-2-0 s after the subject had completed one of its own songs. In one experimental design the subjects were allowed to sing a randomly determined number (3, 4, 5 or 6) of songs between each playback. In the other design all playbacks occurred after songs containing a specified B phrase. In some experiments a coin flip determined whether each repetition of the phrase would be followed by a stimulus or would be designated a control: in the others a coin flip determined which of two stimuli would be presented.
1252
Animal Behaviour 33, 4
kHz 97.-
tilltltLtL~,,
5-
pPq fr
1"
Rlc
R2c
Rae
R5c
R4c
97Rnlml
5-
lil '/ltlt,r,~
~
,
0"5 S
wilmeme~m, .,,,
31-
R7e
R6c 9-
,///,
Wlc
ffff!rrr,
75-
!1 tl I,
W2c 1
p
,
31-
i,J
I Pf~T~r,, II
II,
W3c
W4c
W5c
W6c
WTe
W8c
Figure 3. Sonagrams of C phrases of the two subjects, Red and White. In contrast to the labels for B phrases (Fig. 2), the second symbol is intended only to distinguish among the phrases within each bird's repertoire and not to indicate a phrase type (C phrases cannot be classified into discrete types).
For the experiments using recorded stimuli the data were taken down by hand; for the live broadcasts the two birds were recorded on separate channels of a Sony TC-D5M cassette recorder, and the recording was filmed using a Princeton Applied Research 4512 F F T real time spectrum analyser. Sonagrams were made with a Kay Elemetrics Corp. 7092A sound spectrograph, using the 8-8000-Hz frequency range and the flat shape and wide band settings.
RESULTS
Normal Serial Order In the live broadcast experiments (conducted from 17 to 24 May 1982), each subject was unable to hear the other bird during one of the three
treatments. The first-order transitions of B phrases for each bird during this 50-rain period (10 m i n x 5 days) are shown in Tables Ia and IIa. No statistical analysis is necessary to show that each bird had strong first-order preferences. For Red, 63-89~ of the transitions from each B phrase were to a single one of the other phrases. White showed even stronger preferences, with 95-100~ of the transitions from four of its five B phrases (W4by, W4bx, W2by, W3b) being to a single other phrase~ There were two common transitions from the fifth B phrase (W2bx). Inspection of the sequences showed that White typically sang several cycles of W3b W4by W 4 b x - W 2 b y - W 2 b x , then sang W4bx (instead of W3b) and carried on from that point in the usual cycle. Although Red was less predictable, he often sang several cycles of R 4 b x - R4by R3b R l b R2b before deviating. The deviations may have
Whitney." Serial order in wood thrush song Table I. First-order transitions of B phrases for Red
Table II. First-order transitions of B phrases for White
Following B phrase Preceding Bphrase
R4bx
R4by
Following B phrase
Rib
R2b
Preceding Bphrase
t0 83 0 l 3
16 4 83 0 18
6 1 6 Ill 0
W4by W4bx W2by W2bx W3b
52 147 1 18 27
53 17 160 3 114
27 14 53 276 0
R3b
(a) Not able to hear song of White
R4bx R4by R3b Rlb R2b
1 9 4 10 69
78 0 6 3 20
0 7 17 31 164
82 3 14 17 66
W4by
W4bx
W2by
W2bx
W3b
1 50 0 0 0
0 0 59 0 0
0 0 2 29 0
5 91 4 4 13
0 7 98 0 0
2 5 6 55 0
(a) Not ab~ to hear song of Red
(b) Able to hear song of White*
R4bx R4by R3b Rlb R2b
1253
0 0 1 0 32
31 0 0 16 0
(b) Able to hear song of Red
* But White not able to hear Red.
followed a pattern, but I did not investigate higherlevel transitions. Live B r o a d c a s t s
The serial order of B phrases became less stereotyped in each subject when the other bird could be heard singing (Tables Ib, IIb). The preferred transitions (Tables Ia, IIa) remained more c o m m o n than other transitions, but in all cases they declined as a percentage of the total transitions. F o r White, the number of cells in the transition table with non-zero entries increased dramatically from 9 to 21; for Red the increase was only from 21 to 23. More specific information about the disruption of normal serial order can be gained from the firstorder transitions between the B phrases of the two birds. F o r the treatments in which only one bird could hear the other, the observed transitions (from the independent singer to the bird that could hear) deviated significantly from the random expectation (Tables IIIa, IVa). An explanation for the deviations in certain cells is that the bird altered its normal serial order to avoid matching a B phrase very similar to one of its own (Whitney & Miller 1983). Before I began these experiments, I had determined that R2b was very similar to W2bx, R3b to W3b, R4bx to W4bx, and R4by to W4by. Although the phrases differed in details of structure (Fig. 2), they were similar in overall frequency, and I found them difficult to distinguish by ear. When Tables IIIa and IVa are condensed about the ceils
W4by W4bx W2by W2bx W3b
1 3 3 4 43
47 5 9 27 12
* But Red not able to hear White.
of interest, significant deviations (P < 0-05) occur in six out of eight cells. Red avoided matching W2bx, W3b, and W4bx (Z2=13.16, 6.66 and 12.20, respectively), and White avoided matching the counterparts of these three phrases (Z2 = 11.05, 8.69 and 13.29, respectively). It follows that the birds favoured answering with non-matching phrases. But they did not seem to choose at random from non-matching phrases. For example, White showed a marked preference for answering R2b with W4bx rather than with W2by, W3b or W4by (Table IVa). Similarly, Red favoured answering W2by, a phrase for which he had no counterpart, with R4by, yet avoided answering with R l b (Table IIIa). The first-order B phrase transitions for the treatment in which each bird could hear the other are shown in Tables IIIb and IVb. Overall, the observed values deviated from the random expectation, but deviations due to avoidance of matching were less predominant than in the treatments in which only one bird could hear the other. Red avoided matching W3b and W4bx; White did not avoid matching any of Red's B phrases. The deviations in other cells tended to be consistent with those in Tables IIIa and IVa. P l a y b a c k of the O t h e r Bird's S o n g
In an attempt to manipulate serial order more systematically, I presented playbacks of recorded song. Each subject was presented with the B phrases, each with an associated C phrase, of the
Animal Behaviour, 33, 4
1254
Table III. First-order transitions from the B phrases of White
to the B phrases of Red* Preceding B phrase of White
Following B phrase of Red Rl b
R2b
R3b
R4bx
R4by
(a) Red able to hear song of White, but White not able to hear Red
W2bx
10 4 (12.92) (14-36) W2by 6 13 (14.54) (16.15) W3b 10 16 (7-62) (8.46) W4bx 27 9 (12.23) (13.59) W4by 1 18 (6.69) (7.44) Difference between observed and df= 16, P<
10 11 21 (8.38) (11.73) (8.62) 15 28 1 (9.42) (13.19) (9-69) 0 2 5 (4.94) ( 6 - 9 1 ) (5.08) 7 2 8 (7.93) (11.10) (8.15) 3 6 1 (4-34) (6.07) (4.46) expected values: )( = 125.24, 0.001.
(b) Red able to hear song of White, and White able to hear Red
W2bx
3 ll 9 7 19 (10.70) (13.48) (8"56) (7.92) (8.34) W2by 0 20 25 22 1 (14.85) (18-71) (11.88) (10.99) (11.58) W3b 4 9 0 7 10 (6.55) (8.25) (5-24) (4.85) (5.11) W4bx 43 5 2 0 8 (12.66) (15-96) (10.13) (9.37) (9.88) W4by 0 18 4 l 1 (5-24) (6.60) (4.19) (3.88) (4.09) Difference between observed and expected values: Z2= 207.7 l, df= 16, P<0.001. * Expected values shown in parentheses.
other subject. By allowing the subjects to sing a randomly determined number of songs before each playback, I established the expectation that by chance alone the number of playbacks answered with a given B phrase should be proportional to the overall frequency of occurrence of that B phrase. The experiments were first conducted on 3-8 June 1982, and then repeated on 9-14 June. In both sets of experiments the results for Red are largely consistent with those obtained in the live broadcasts. Red's observed use of different B phrases to answer the stimuli differed in every case from the random expectation (Table V). As before, he avoided matching W2bx (though the results were statistically significant only in the first replicate), W3b and W4bx; he also avoided matching W4by, a trend that did not reach statistical significance in the live broadcasts. Finally, the results
were consistent with the earlier ones in cases where deviations from expected values could not be explained as avoidance of matching (compare Tables III and V). By contrast, White's observed use of different B phrases to answer the stimuli differed in only two cases from the random expectation (Table VI). White matched R2b, R3b and R4bx slightly less often than expected in each replicate, and R4by slightly more often than expected. N o n e of the results reached significance. Further analysis shows that White was more likely to deviate from his preferred sequences immediately following a stimulus than at other times (Table VII). This occurred even in the treatment where the stimulus was a B phrase type that was not in White's repertoire (Rlb). In the four treatments where the stimulus was very similar
Whitney." Serial order in wood thrush song
1255
Table IV. First-order transitions from the B phrases of Red to
the B phrases of White* Preceding B phrase of Red
Following B phrase of White W2bx
W2by
W3b
W4bx
W4by
(a) White able to hear song of Red, but Red not able to hear White
Rib
14 5 8 13 2 (8.37) (12.29) (6.15) (10.07) (5-12) R2b 2 13 9 26 3 (10.56) (15-51) (7.76) (12.71) (6-46) R3b 10 13 0 5 14 (8-37) (12.29) (6.15) (10.07) (5.12) R4bx 8 31 3 2 5 (9.76) (14.34) (7.17) (11.75) (5.98) R4by 15 10 16 13 6 (11.95) (17.56) (8.78) (14.39) (7-32) Difference between observed and expected values: Z2= 100.42, df= 16, P <0.001. (b) White able to hear song of Red, and Red able to hear White
Rlb
22 10 4 7 5 (10.36) (13.96) (6-34) (12-90) (4.44) R2b 6 21 11 35 I (10-15) (21.52) (9'78) (t9.89) (6-85) R3b 7 12 4 9 8 (8.63) (11.63) (5.29) (10-75) (3.70) R4bx 8 19 2 4 4 (7.99) (10.76) (4-89) (9-94) (3-42) R4by 6 4 9 6 3 (6.04) (8.14) (3.70) (7"52) (2.59) Difference between observed and expected values: Z2= 63.54, d f - 16, P < 0.001. * Expected values shown in parentheses.
to one of White's own B phrases, the deviations tended to occur when the normal serial order would have resulted in matching (Table VII). Playback of Own Song
When presented with the other bird's songs, both in the live broadcasts and in the playbacks, each subject tended to avoid matching B phrases that were very similar to its own, and to favour answering with certain other phrases. In this section I test the prediction of the direct-connection hypothesis that the birds should favour answering one of their own songs with the B phrase that in normal singing follows the stimulus B phrase. The stimuli were the same BC combinations used in the above experiments. By random choice among each bird's B phrases, all stimuli for Red were presented
after songs containing R3b, and all stimuli for White after songs containing W2by. Each trial involving a given stimulus continued until the subject had sung 50 songs containing the specified phrase. A coin flip decided whether each song would be followed by the stimulus or would be designated a control. The experiments were conducted first in June 1982, and then repeated in January and February 1983. The results for Red gave only partial and inconsistent support for the hypothesis (Table VIII). In the controls, R3b was followed by R l b 73-100% of the time. In the first replicate of the experiment, Red made a significant switch away from R l b to answer with another B phrase only when the stimulus was R l b . As predicted by the hypothesis, it switched to the phrase (R2b) that
Animal Behaviour, 33, 4
1256
Table V. Response of Red to random playbacks of White's songs Number of answers Stimulus
Replicate Obs:
Rlb
R2b
R3b
R4bx
R4by
10
5
15
12
33
1 Exp:
)~2
p
23.62
<0-001
26.49
<0.001
56.12
<0.001
37-68
<0.001
24.12
<0.001
35.00
<0.001
13.44
<0.01
21.19
<0.001
38.29
<0.001
56.93
<0.001
1 5 . 9 3 13.72 14.60 13.94 16.81
W2bx W7c Obs:
6
7
16
14
32
2 Exp: Obs:
1 7 . 4 6 12.76 15.00 13.88 15.90 1
12
16
41
5
1 Exp:
14-55 15-45 15.22 16.12 13.66
W2by-W 1c Obs:
3
28
18
24
2
2 Exp: Obs:
16.01 14.86 15.09 15.32 13.72 14
35
6
6
14
1 Exp:
1 7 . 0 9 19-08 13-09 13-76 11.98
W3b W3c Obs:
15
36
7
5
12
2 Exp: Obs:
15.81 16.04 13.55 14.68 14.91 20
15
19
0
5
8.36
5.65
6
15
1 Exp:
17.18 16.05 11.75
W4bx-W5c Obs:
14
30
10
2 Exp: Obs:
16-92 15.09 14.86 13.72 14.41 2
37
11
19
5
1 Exp:
16.13 18.33 14.36 13.25 11.93
W4by W4c Obs:
1
40
10
22
2
2 Exp:
1 7 . 9 3 17.36 13.89 15.05 11.57
followed R i b in normal sequences. The results were similar for the second replicate o f this treatment. Interestingly, in the first replicate o f the R3b treatment, Red answered the stimulus even more often t h a n expected with R l b . This might be interpreted as s u p p o r t for the hypothesis, supposing that the stimulus reinforced the facilitative connection to R l b by providing an additional sensory dose o f R3b. In the second replicate o f this treatment there was no possibility o f a switch
toward answers with R l b since this phrase always followed R3b in the controls. The results for the R2b treatment support the hypothesis in the second replicate but not in the first. Finally, the results for the second replicate of the R4by treatment show an inexplicable switch to anwers with a phrase (R2b) that only rarely followed R4by in normal sequences (Table Ia). With only a single exception, the results for White clearly support the hypothesis (Table IX).
Whitney." Ser&l order in wood thrush song
1257
Table V|. Response of White to random playbacks of Red's songs Number of answers Stimulus
Replicate
W2bx
W2by
W3b
W4bx
W4by
Obs:
23
13
9
18
12
Exp:
16.01
16.01
Obs:
19
15
Exp:
15-69
Obs:
14
Exp:
15-39
1 13-58 15.81
X~
P
5-65
> 0.20
5.99
>0-20
9-65
<0-05
9,05
>0.05
4.62
> 0.30
4,71
>0.30
3-84
>0-30
5,39
>0.20
11.52
<0.05
6.00
>0.10
13-58
R 1I~R4c 20
10
11
15-90
14.18
I4
6
16.04
13,22
2 1 5 . 0 4 14.18 26
15
1 16"69 1 3 . 6 6
R21~R5c Obs:
1[
Exp:
15.27
Obs:
15
Exp:
15-94
Obs:
10
Exp:
15-84
24
9
21
10
2 16.37 I4-16 15.93 14
10
15
13.27 21
1 1 6 . 3 9 12-57 1 6 . 1 7
13.92
R3b-R7c 18
11
17
19
2 Obs:
16.06 13.86 14.74
20
17
16
14.52
13
9
16-04
13-55
11
17
14.26
13-80
1 Exp:
15"57
16"27 13.55
Obs:
12
Exp:
16"10
Obs:
5
17
Exp:
16-04
15.81
Obs:
15
25
Exp:
16-74
R4bx-R6c 23
12
2 1 6 . 5 6 14.26 14
22
17
1 14-01 1 5 . 8 1
13.33
R4by R3c 10
11
14
2 17,20 1 4 . 2 2 1 4 . 4 5
The exception is the second replicate o f the W4by treatment, in which White did not deviate from his normal sequence.
I m p o r t a n c e o f B and C P h r a s e s
The stimuli in the above experiments contained both B and C phrases. In this section I show how these two parts o f the song, presented separately and in natural and synthetic combinations, affect serial order.
12,39
Table X gives the results o f three experiments with White. The stimuli in each case were presented after songs containing W2bx. In the first experiment, the stimuli were two o f White's songs that differed only in the C phrase. The first song (W2bx W7c) was usually followed in normal sequences by W3b, and the second (W2bx-WSc) was followed by W4bx. Both transitions were c o m m o n (Table IIa). As predicted by the direct-connection hypothesis, significantly m o r e answers with W4bx occurred in response to the second song. Presentation o f the C
Animal Behaviour, 33, 4
1258
Table VII. Further analysis of White's response to random playback of Red's songs Number of deviations immediately Incidence of normal and following the abnormal ordering of B phrases stimulus that resulted in Not immediately avoidance following Immediately following of the stimulus the stimulus matching Stimulus R 1l~R4c R21~R5c R31~R7c R4bx-R6c R4b~R3c
Normal
Abnormal
Normal
Abnormal
Observed
Expected
567 533 521 504 507
0 0 2 2 0
144 140 137 140 137
6 10 13 10 13
-6 9 7 t1
2.20 2.76 1-82 2.44
'Abnormal ordering of B phrases, immediately following the stimulus' refers to all occasions when the first song after the stimulus deviated from the preferred order; 'abnormal ordering not immediately following the stimulus' refers to all other deviations. The expected number of deviations immediately following the stimulus that resulted in avoidance of matching was calculated as follows: (overall proportion of stimuli that were immediately followed by a deviation from the preferred order) x (number of stimuli that would have been matched if no deviation had occurred).
phrases alone, in the next experiment, led to similar results. The final experiment shows that the response to songs containing a very similar B phrase (R2b), of Red, also varied with C phrase. In a set of four experiments, the response of Red to his own B phrase and associated C phrase ( R 2 b R6c) versus that to a very similar B phrase and its associated C phrase (W2bx WSc) of White was explored in detail (Table XI). All stimuli were presented after songs containing R2b. The results for the first experiment show that Red answered R 2 b - R 6 c mostly with R4bx, as would be expected from its preferred B-phrase transitions (Table Ia), but answered W 2 b x - W 8 c mostly with R4by. This response to White's song is similar to that given in earlier experiments (Table VI). Removal of the C phrases from the stimuli, in the second experiment, had little effect on the response. Removal of the B phrases, leaving just the Cs, may have had some effect, but the responses to the two stimuli remained significantly different. In the final experiment each B phrase was combined with the C phrase of the other bird (yielding R2b W8c and W2bx-R6c). Red responded to both artificial songs by answering mostly with R4bx. Thus the response normally given to the bird's own B and C phrases,
presented either separately or together, appeared to override that given to the other bird's phrases. A similar set of five experiments with Red was conducted using the songs R 4 b y - R 3 c and W 4 b y W4c (Table XII). The results of the first experiment show that the response was significantly different to the complete songs. Red answered R 4 b y - R 3 c with R3b and R l b , and answered W 4 b y - W 4 c with R2b and R3b. The tendency to answer White's song with R2b is consistent with the results of earlier experiments (Tables IVa, V). In the second experiment the B phrases were presented alone, and Red continued to answer W4by more with R2b. Interestingly, removal of the C phrase from R4by appeared to diminish the response with R1. In contrast to the results of the previous series of experiments (Table XI), there was no difference in response to the isolated C phrases. Red favoured answering both phrases with R3b, and did not answer at all with R2b. In the fourth experiment, however, presentation of the synthetic song, R 4 b y W4c, resulted in a partial reinstatement of the response with R2b. Taken together, the results of the third and fourth experiments indicate that, to induce a response with R2b, the C phrase, W4c, must be presented in combination with a B phrase.
Whitney." Serial order in wood thrush song
1259
Table VIII. Response of Red to playback of his own song (presented after R3b) Percentage of answers Stimulus
Replicate
N
Rlb
R2b
R3b
R4bx
R4by
23
Playback:
95"7
27
Control:
23
Playback:
27
Control:
100-0
22
Playback:
72.7
28
Control:
92-9
20
Playback:
45-0
55.0
30
Control:
93'3
3.3
3-3
28
Playback:
100.0
22
Control:
72.7
13.6
9-1
25
Playback:
100.0
25
Control:
100.0
26
Playback:
96.2
24
Control:
75.0
22
Playback:
81.8
28
Control:
96.4
29
Playback:
86.2
21
Control:
100-0
22
Playback:
27.3
28
Control:
96.4
4.3
1
<0.001 92.6
3.7
3.7
R i1~R4c 95.7
4.3
2
<0.001 13.6
13.6
1
NS
3.6
3.6
R2b-R5c 2
<0.001
1
<0.05 4.5
R31~R7c 2
NS
3.8
1
NS
16.7
8.3
R4bx-R6c 4-5
13.6
2
NS
3.6 3.4
6.9
1
3.4 NS
R4by-R3c 59.1
13.6
2
<0.001 3.6
Probability values are based on Fisher's test, one-tailed. For application of the test, response data were lumped into two categories: (1) R I b (the phrase that most commonly followed R3b in normal sequences), and (2) all other phrases.
Both synthetic songs ( R 4 b y - W 4 c and W 4 b y - R 3 c ) were presented in the fifth experiment. The response to R 4 b y - W 4 c included an even larger p r o p o r t i o n o f answers with R2b than in the previous experiment. The response to W 4 b y - R 3 c was almost evenly divided a m o n g answers with R l b , R3b and R4bx. I c a n n o t account for the tendency to answer with R4bx, but the answers with R l b may have been induced by the C phrase
R3c. Recall that removal o f this phrase from R4by completely eliminated the response with R l b in the second experiment.
Self-inhibition
of B P h r a s e s
Self-inhibition has been invoked to account for the m a n n e r in which wood thrushes cycle through
Animal Behaviour, 33, 4
1260
Table IX. Response of White to playback of his own song (presented after W2by) Percentage of answers Stimulus
Replicate
N
W2bx
22
Playback:
28
Control:
100.0
25
Playback:
40.0
25
Control:
100.0
23
Playback:
100-0
27
Control:
100'0
27
Playback:
100"0
23
Control:
100.0
24
Playback:
54.2
26
Control:
100.0
26
Playback:
57-7
24
Control:
100.0
30
Playback:
70-0
20
Control:
100-0
24
Playback:
33 '3
26
Control:
100"0
29
Playback:
34.5
21
Control:
100.0
25
Playback:
100.0
25
Control:
100.0
W2by
W3b
W4bx
W4by
P
36.4
63-6
<0'001
1
W2bx-W7c 60'0 <0"001
2
N8
l
W2by-W 1c NS
2 12"5
8"3
25.0 <0.01
1
W3b-W3c 3-8
38.5 <0.001
2 30.0
<0.01
1
W4bx-W5c 66.7 <0-00l
2 65"6
< 0.001
1
W4by-W4c NS
2
Statistics as in Table VIII, with the first response category being W2bx (the phrase that almost invariably followed W2by in normal sequences).
their B a n d C phrase repertoires (Beck 1971). Successive utterances o f a given phrase are generally separated by several songs c o n t a i n i n g other phrases. To test for self-inhibition o f B phrases, I did a series of five experiments with Red. In each experiment the stimulus song ( R l b - R 4 c ) was presented after a different one of the bird's five B phrases. I reasoned t h a t if self-inhibition dissipates gradually after p r o d u c t i o n o f a phrase, the tendency to answer the stimulus B phrase with the B
phrase t h a t followed it in n o r m a l sequences (R2b) should vary systematically across the treatments. The predicted trend a n d the results are s h o w n in Table XIII. W h e n the stimulus was presented after R2b the bird never answered with R2b. In each of the o t h e r four treatments it answered mostly with R2b, but, c o n t r a r y to the prediction, the percentage of the playbacks answered with this phrase did n o t increase as a function of the n u m b e r of o t h e r B phrases p r o d u c e d since the last utterance of R2b.
Whitney." Serial order in wood thrush song
1261
Table X. Response of White to playback of different combinations of B and C phrases
(stimuli presented over W2bx) Percentage of answers Experiment
Stimulus
N
W2bx-W7c
22
W2bx W8c
28
no B-W7c
21
no B-W8c
W2bx
W2by
W3b
W4bx
18"2
77-3
4.5
42.9
57.1
90.5
4'8
29
65-5
34.5
R2b-R5c
25
64-0
36.0
R2t~R6c
25
100.0
W4by
P <0"001
1
4.8
< 0"02
2
<0.01
3
Probability values are based on Fisher's test, one-tailed for experiments 1 and 2 and twotailed for experiment 3. The test was applied only to the data for W3b and W4bx, the two phrases that followed W2bx in normal sequences.
Table XI. Response of Red to playback of different combinations of B and C phrases
(stimuli presented after R2b) Percentage of answers Experiment
Stimulus
N
Rlb
R2b-R8c
20
5.0
W2bx-WSc
R2b
R3b
R4bx
R4by
80.0
15-0
30
23.3
76.7
R2b-no C
22
90'9
9' 1
W2bx-no C
28
25.0
75-0
no B-R8c
27
11.1
77-8
3.7
no B-W8c
23
8,7
56.5
34-8
R21>W8c
25
84.0
16,0
W2bx-R8c
25
80.0
20-0
I
P <0.001
2
<0.001 7.4
3
<0-01
4
NS
Probability values are based on Fisher's test, two-tailed for experiments 1 and 4 and one-tailed for experiments 2 and 3. The test was applied only to the data for R4bx and R4by, the two phrases that most commonly followed R2b in the experiments.
DISCUSSION In summary, the results show that when each subject sang in isolation it had a preferred order o f B phrases (Tables Ia, IIa). This order was disrupted
when the subject could hear the ongoing song o f the other bird (Tables Ib, lib). A partial explanation for the disruption is that each bird tended to avoid matching B phrases that were very similar to its own. This, however, does not account for the
Animal Behaviour, 33, 4
1262
Table XIL Response of Red to playback of different combinations of B and C phrases (stimuli presented after R4by) Experiment
Stimulus
N
Rlb
R2b
R3b
R4bx
R4by-R3c
23
34.8
56.5
8-7
W4by W4c
27
55-6
44.4
R4by no C
24
4.2
95.8
W4by-no C
26
38.5
61-5
no B-R3c
29
6.9
93" 1
no B W4c
21
4.8
95.2
R4by-R3c
25
48.0
52-0
R4by-W4c
25
4.0
2 4 . 0 72.0
R4by-W4c
31
3.2
5 1 . 6 45.2
W4by R3c
19
R4by
1
P <0.001
2
<0.01
3
NS
4
<0.01
5
<0.001 31"6 1 0 . 5 2 6 . 3
31.6
Probability values for experiments 2 and 3 are based on Fisher's test, one-tailed. Probability values for experiments 1, 4 and 5 are based on the ;(2 test. Categories were combined as necessary to ensure sufficiently large expected values, except for experiment 4, where this would have rendered the test meaningless. For experiments 1 and 5 the categories were R2b, R3b, and all other phrases combined (X2= 89.56; Z2 - 22.90, respectively). Note that for experiment 4 two expected values were less than 5.0 (Zz= 12.21).
Table XIII. Response of Red to playback of a stimulus song (Rib R4c) at different points in his normal sequence of songs B phrase of song immediately preceding stimulus
N
Average number of songs since last utterance of R2b
R 1b R3b R4by R4bx R2b
31 21 21 23 29
3-70 3-57 3-25 2.23 0
consistently large deviations from expected firstorder transitions between certain other B phrases. The same general patterns o f disruption occurred when Red was presented, at r a n d o m intervals~ with recorded songs o f White (Table V). In the converse experiments, White's response was much more subtle (Table VI), and additional analysis was necessary to reveal a tendency to avoid matching very similar B phrases (Table VII).
Predicted response with R2b
~ Answers with R2b
Greatest
93.5 66.7 71-4 95.7 0
. Least
The self-inhibition hypothesis can account for avoidance o f matching but not for the other consistent patterns of answering shown by the two birds in the live broadcasts and r a n d o m playbacks. The direct-connection hypothesis is m o r e comprehensive. It predicts that the B phrase used to answer the other bird's song will be the one that, in normal singing, follows the B phrase that is very similar to the stimulus. This prediction is clearly not upheld
Whitney: Serial order in wood thrush song
in the results of the live broadcasts and random playbacks of the other bird's songs (Tables III, IV, V, VI). For example, Red favoured answering W3b with R2b, yet in undisturbed sequences he usually sang R l b after R3b, a phrase very similar to W3b (Table Ia). The direct-connection hypothesis received mixed support when the stimulus was one of the bird's own songs. Except for one replicate of one experimental treatment (W4by), White always showed a significant tendency to answer with the B phrase that followed the stimulus phrase in normal sequences (Table IX). For Red the only results that supported the hypothesis in both replicates were for the R 1b treatment (Table VIII). Note, however, that R l b was presented immediately before that phrase would have occurred in the normal sequence, and that Red responded by skipping ahead just one song in the normal sequence. One could argue that this response is also consistent with an elaboration of the self-inhibition hypothesis: following stimulus-induced inhibition, the B phrase that has the highest level of causal factors, and therefore will be sung next, is the one that follows the inhibited phrase in normal sequences. In the second replicate of the R2b treatment Red did, however, respond in a way consistent with only the direct-connection hypothesis. He answered mainly with the phrase (R4bx) that followed R2b in normal sequences. Similar results were obtained in two experiments not shown in Table XI. In one experiment the stimulus R l b (with R4c) was presented after R4bx and in the other it was presented after R4by. In both cases Red answered mainly with the phrase (R2b) that followed R1 b in normal sequences (first experiment: 22/23 answers with R2b versus 1/27 in control; second experiment: 15/21 answers with R2b versus 0/27 in control). In these experiments the birds may have responded to either the B phrase or the C phrase of the stimulus song, or to both. The results of further experiments indicate that both phrases are important (Tables X, XI, XII). An interesting case of direct connections based on C phrases is shown for White in Table X. Consistent with the transitions observed in normal sequences, the experimental results show that the response was different to two C phrases, both when the phrases were presented alone and when they were combined with a B phrase. The two sets of experiments with Red, in which
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both birds' B and C phrases were used as stimuli, show that the response depends on both types of phrases, but that the details may differ. In the first set of experiments the difference in response to two very similar B phrases, each with an associated C phrase, persisted when the B phrases were presented alone and also when the C phrases were presented alone (Table XI). By contrast, in the second set, the difference in response to the BC combinations was altered when the B phrases were presented alone, and eliminated when the C phrases were presented alone (Table XII). Thus the C phrases had an effect only when combined with B phrases. Overall, the results bearing on the direct-connection hypothesis may be summarized as follows. When presented with his own song, White nearly always responded in a way consistent with the hypothesis. In the only case where he did not, his normal order of B phrases was unaffected by the stimulus (Table IX). Red was less consistent, but again, most of the results that were contrary to those predicted by the hypothesis indicate a lack of any response to the stimulus (Table VIII). In the only exception, Red made a significant switch to answers with a B phrase that did not follow the stimulus B phrase in normal sequences. For both birds the results varied in some treatments between the first and second replicates. I conclude that normal serial order of B phrases in the two birds depended, at least in part, on direct facilitative connections. From the results of the later experiments it is clear that these connections involved C phrases as well as B phrases (Tables X, XI, XII). The fact that transitions between some B phrases were not disrupted by playback need not be taken as evidence against direct connections. One possibility is that such mechanisms underlie these transitions but do not depend upon auditory feedback. The difference between the results of the first and second replicates of some treatments would then imply that the role of audition is not constant. Now consider the direct-connection hypothesis in light of the responses given by each subject to the other bird's song. Both birds avoided matching B phrases very similar to their own, and favoured answering with certain other phrases. But these phrases were often not the ones predicted by the direct-connection hypothesis. For example, Red consistently avoided matching W2bx with R2b and instead favoured answering with R4by (Table III,
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Animal Behaviour, 33, 4
V). This is in contrast to his tendency to answer R2b with R4bx, the B phrase that followed R2b in normal sequences. The difference in response to the two B phrases persisted even when they were presented alone, without C phrases (Table X1). The mechanism that controls transitions between B phrases cannot be as simple as previously implied. One part of the mechanism appears to treat very similar B phrases as equivalent, resulting in avoidance of matching, but another part discriminates between the phrases and facilitates different transitions. Facilitative connections are not the only type of mechanism underlying serial order in wood thrush song. Self-inhibition also appears to be important. The results of experiments with Red indicate a quickly-dissipating form of self-inhibition, sufficient to account for the immediate switches between different B phrases (Table XIII). The question remains, however, as to why the bird typically repeated a particular B phrase only after having sung all four of his other phrases. Perhaps a longer lasting form of self-inhibition operated during the development of a stable serial order, which was then maintained by facilitative connections. A result obtained in one of the earlier experiments can also be interpreted as evidence for selfinhibition. When White was presented with W4bx (and W5c) after he sang W2by, he sometimes answered with W2by, thus singing this phrase twice in succession (Table IX). This supports the directconnection hypothesis, since W2by followed W4bx in normal sequences. In the first replicate of the experiment, however, I noticed that the answer was often an incomplete song. The second repetition of the trill in W2by, and the entire C phrase were deleted. I kept a record of such songs in the second replicate and found that 9 of the 16 answers with W2by were incomplete. N o n e of the songs immediately preceding playbacks was incomplete. Thus the artificial facilitation of W2by was opposed by self-inhibition, with neither mechanism prevailing. It appears that the mechanisms underlying serial order in wood thrush song include both facilitative connections and self-inhibition. Slater (1983) came to a similar conclusion in a non-experimental study of chaffinch (Fringilla coelebs) song. He suggested that the relative importance of these two mechanisms may vary between individual birds. I have not investigated self-inhibition in detail, but the results presented in this paper indicate that the
importance of facilitative connections, at least where they are mediated by audition, varies not only between individual wood thrushes but between the phrases within the repertoire of a single bird.
ACKNOWLEDGMENTS I thank A. Dufty, P. Marler, J, Miller, P. Slater and R. Suter for commenting on earlier versions of the manuscript. The research was supported by an N I M H postdoctoral fellowship (MH08291) to the author and by an N I H grant to Rockefeller University (RR07065-15). The birds were collected and held in captivity in accordance with Federal scientific collecting permit P R T 2 - 1 3 9 4 N Y and State of New Y o r k scientific collector's licence SC 1916.
REFERENCES Beck, R. M. 1971. Sequence patterning of wood thrush song. Am. Zool., II, 66 (Abstract). Bertram, B. C. R. 1970. The vocal behaviour of the Indian hill mynah, Gracula religiosa. Anim. Behav. Monogr., 3, 79 102. Dobson, C. W. & Lemon, R. E. 1977. Markovian versus rhomboidal patterning in the song of Swainson's thrush. Behaviour, 62, 276-297. Dobson, C. W. & Lemon, R. E. [977. Markov sequences in songs of American thrushes. Behaviour, 68, 86-105. Falls, J. B. & d'Agincourt, L. G. 1983. Why do meadowlarks switch song types? Can. J. Zool., 60, 3400-3408. Falls, J. B., Krebs, J. R. & McGregor, P. K. 1982. Song matching in the great tit (Parus major): the effect of similarity and familiarity. Anita. Behav., 30, 997--1009. Hansen, P. 1981. Song organization in a chaffinch (Fringilla eoelebs). Natura Jutland., 19, 107 120. Hinde, R. A. 1958. Alternative motor patterns in chaffinch song. Anim. Behav., 6, 211 218. Isaac, D. & Marler, P. 1963. Ordering of sequences of singing behaviour of mistle thrushes in relationship to timing. Anim. Behav., 11, 179-188. Krebs, J. R., Ashcroft, R. & van Orsdol, K. 1981. Song matching in the great tit Parus major L. Anim. Behav., 29, 918-923. Kroodsma, D. E. 1971. Song variations and singing behavior in the rufous-sided towhee, Pipilo erythrophthalmus oregonus. Condor, 73, 303 308. Kroodsma, D. E. 1975. Song patterning in the rock wren. Condor, 77, 294-303. Kroodsma, D. E. 1979. Vocal dueling among male marsh wrens: evidence for ritualized expressions of dominance/subordinance. Auk, 96, 506-515. Lashley, K. 1951. The problem of serial order in behavior. In: Cerebral Mechanisms in Behavior (Ed. by L. A. Jeffress), pp. 112-136. New York: Wiley.
Whitney: Serial order in wood thrush song Lemon, R. E. 1968a. Coordinated singing by blackcrested titmice. Can. J. Zool., 46, 1163-1167. Lemon, R. E. 1968b. The relationship between organization and function of song in cardinals. Behaviour, 32, 158-178. Lemon, R. E. & Chatfield, C. 1971. Organization of song in cardinals. Anim. Behav., 19, 1 17. Lemon, R. E. & Chatfield, C. 1973. Organization of song of rose-breasted grosbeaks. Anim. Behav., 21, 2 8 4 4 . Nelson, K. 1973. Does the holistic study of behavior have a future? In: Perspectives' in Ethology (Ed. by P. P. G. Bateson & P. H. Klopfer), pp. 281 328. New York: Plenum Press. Schroeder, D. J. & Wiley, R. H. 1983. Communication with shared song themes in tufted titmice. Auk, 100, 414424. Slater, P. J. B. 1983. Sequences of song in chaffinches. Anim. Behav., 31, 2 7 ~ 2 8 1 . Todt, D. 1975. Short term inhibition of outputs occurring in the vocal behaviour of blackbirds (Turdus merula m.
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L.). J. comp. Physiol., 98, 28%306. Todt, D. 1981. On functions of vocal matching: effect of counter-replies on song post choice and singing. Z. Tierpsychol., 57, 73 93. Verner, J. 1975. Complex song repertoire o f male longbilled m a r s h wrens in eastern Washington. Living Bird, 14, 263-300. Whitney, C. L. 1981. Patterns of singing in the varied thrush II. A model of control. Z. Tierpsychol., 57, 141 162. Whitney, C. L. & Miller, J. 1983. Song matching in the wood thrush (Hylociehla mustelina): a function of song dissimilarity. Anita. Behav., 31, 4 5 7 4 6 1 . Zoloth, S., Dooling, R. J., Miller, R. & Peters, S. 1980. A minicomputer system for the synthesis of animal vocalizations. Z. Tierpsychol., 54, 151-162.
(Received 19 June 1984; revised 29 October 1984; MS. number." A4328)