ORIGINAL PAPER

Human melody singing by bullfinches (Pyrrhula pyrrula)gives hints about a cognitive note sequence processing

Jurgen Nicolai • Christina Gundacker •

Katharina Teeselink • Hans Rudolf Guttinger

Received: 6 November 2012 / Revised: 23 April 2013 / Accepted: 20 May 2013

� Springer-Verlag Berlin Heidelberg 2013

Abstract We studied human melody perception and pro-

duction in a songbird in the light of current concepts from the

cognitive neuroscience of music. Bullfinches are the species

best known for learning melodies from human teachers. The

study is based on the historical data of 15 bullfinches, raised

by 3 different human tutors and studied later by Jurgen

Nicolai (JN) in the period 1967–1975. These hand-raised

bullfinches learned human folk melodies (sequences of

20–50 notes) accurately. The tutoring was interactive and

variable, starting before fledging and JN continued it later

throughout the birds’ lives. All 15 bullfinches learned to sing

alternately melody modules with JN (alternate singing). We

focus on the aspects of note sequencing and timing studying

song variability when singing the learned melody alone and

the accuracy of listening-singing interactions during alter-

natively singing with JN by analyzing song recordings of 5

different males. The following results were obtained as

follows: (1) Sequencing: The note sequence variability

when singing alone suggests that the bullfinches retrieve the

note sequence from the memory as different sets of note

groups (=modules), as chunks (sensu Miller in Psychol Rev

63:81–87, 1956). (2) Auditory–motor interactions, the

coupling of listening and singing the human melody:

Alternate singing provides insights into the bird’s brain

melody processing from listening to the actually whistled

part of the human melody by JN to the bird’s own accurately

singing the consecutive parts. We document how variable

and correctly bullfinches and JN alternated in their singing

the note sequences. Alternate singing demonstrates that

melody-singing bullfinches did not only follow attentively

the just whistled note contribution of the human by auditory

feedback, but also could synchronously anticipate singing

the consecutive part of the learned melody. These data

suggest that both listening and singing may depend on a

single learned human melody representation (=coupling

between perception and production).

Keywords Songbird �Melody perception and production �Sequencing and timing � Auditory–motor interactions �Feedback between hearing and singing � Internal

representation

Introduction

In this manuscript, we analyze human melody and alternate

singing in bullfinches in terms of current concepts from the

cognitive neurobiology of music perception and production

in humans (e.g. Janata and Grafton 2003; Sakai et al. 2004;

Brown et al. 2004, 2006; Zatorre et al. 2007; Chen et al.

2009; Tierney et al. 2011). Music performance is currently

considered to be one of the most complex and demanding

cognitive challenges that human mind can undertake. It

offers a view of the brain in which acoustic perceptual and

motor systems are coupled across multiple levels of pro-

cessing. Melody singing requires precise timing of several

hierarchically organized actions as well as accurate control

over different pitches and durations of consecutive notes.

Several cortical and subcortical regions including the basal

ganglia, the supplementary motor area and the cerebellum

Jurgen Nicolai: Deceased in 2006.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10071-013-0647-6) contains supplementarymaterial, which is available to authorized users.

J. Nicolai � C. Gundacker � K. Teeselink � H. R. Guttinger (&)

Abteilung fur Allgemeine Zoologie, FB Biologie, Universitat

Kaiserslautern, P.B. 3049, 67653 Kaiserslautern, Germany

e-mail: guett@biologie.uni-kl.de

123

Anim Cogn

DOI 10.1007/s10071-013-0647-6

have been implicated in the learning and production of note

sequences in humans.

Until recently, comparative neuroanatomy did not rec-

ognize cortex-like structures and functions in the avian

forebrain. However, the Avian Brain Nomenclature Con-

sortium (Jarvis et al. 2005) disproved this classical thinking

about avian brain. In the songbird, neural coding of syn-

tactic structure in learned vocalizations has been detected,

suggesting that individual neurons can acquire syntactic

attributes in the course of vocal learning (Fujimoto et al.

2011). Thus, the bird’s brain is neither a precursor nor a

primitive form of the mammalian brain but a highly and

differently organized structure. Given the new under-

standing of avian brain organization and function, which

demonstrates similarities to mammalian sensory and motor

cortices, our study on human melody singing in bullfinches

promises insights into whether a similar cognitive pro-

cessing may also occur in songbird’s brain.

We focus on the following two aspects:

1. Sequencing and timing (rhythm), studying the vari-

ability (errors) of singing the melody solo, without a

human partner.

We studied whether the bullfinches memorized and

recall the note sequence of the melodies as a coherent,

linear chain or, as humans do (Janata and Grafton 2003), in

smaller sub-sequences (or modules), in chunks. We use

‘‘module’’ here to refer to the objective breakdown of a

melody into sub-melodies and ‘‘chunking’’ for the inferred

cognitive processes of correct memorizing and recalling

the note sequence.

The significance of chunking derives from the ability to

overcome objections to linear models of serially organized

behavior by augmenting linear with hierarchical structures.

Chunking is regarded as a basic cognitive process. It pro-

vides a window onto cognitive processes that guide or

interrupt otherwise automatic processes (Sakai et al. 2004).

Processing beyond the boundary of a chunk requires a

cognitive selection of the next chunk, whereas processing

within chunks is carried out more automatically. Chunks

can be identified by long variable pauses and elevated

transitional error probabilities after these pauses (Terrace

2001). Phrasing by inserting pauses into a sequence can

either facilitate or retard serial learning for humans and

animals (Wallace et al. 2008).

For songbirds, organizing songs in chunks has already

been reported for the Zebrafinch (Taeniopygia guttata)

(Williams and Staples 1972), for Nightingales (Luscinia

megarhynchos) (Hultsch and Todt 1989) and the Bengalese

finch (Lonchura striata) (Suge and Okanoya 2010).

We studied whether the bullfinches retrieve the learned

human melodies in sub-melodies (modules) separated by

pauses according to the note pattern whistled by the human

tutor and how bullfinches assemble modules into a correct

melody.

2. Auditory–motor interaction, that is, coupling between

listening, perceiving and singing melody parts of

bullfinches during alternate singing with its human

partner.

We analyzed the accuracy of the bullfinch’s choices and

how a bird continues after the human partner pauses,

focusing on whether the bird chooses the appropriate note

pattern. We studied the precision of the bird’s responses to

a variable challenge, that is, to the group of notes that had

just been whistled by its human partner. When faced with a

variety of possible entry points into a melody, the bird must

choose the correct note sequence and the exact time to cue

into continue the melody where the human partner just

ended. Alternate singing, when various entry sites are

possible, that is whenever the human stops, provides

information about how the bullfinch acoustically processes

the note sequence whistled by the human and thus how

auditory–motor interactions in the bird’s brain retrieve the

still remaining parts of the notes sequence. It requires a

departure from routinely singing the sequence from the

beginning to the end, to cope with challenges that are not

precisely predictable. Does the bird compare the notes, or

note groups, just heard with its mental representation of the

learned human melody stored in its memory? To be able to

choose the correct consecutive melody module, the bird

probably has to engage in short-range planning.

In order to understand our approach, Melody 1 in the

original recording (Electronic Supplementary Mate-

rial = ESM, S1) and the note sequences of the visual

display both spectrograms and the musical notation (Fig. 1)

should be followed simultaneously. Listening to the mel-

ody and simultaneously following its notation in notes and

spectrograms enables a more stringent recognition of the

phrasing into smaller sub-melodies and better detection of

sequential errors than does examining the visualized pre-

sentations by themselves.

To determine where the bullfinch starts singing after the

human partner stops, the notes uttered by the bullfinch or

whistled by JN must be distinguished with high reliability.

This distinction can be accomplished both by listening and

by analyzing spectrograms (Fig. 2, ESM: S4): The notes of

the bullfinches sound more sonorous and vary far less in their

dynamics. On the visual display, the bird’s notes consist of a

fundamental, which determines the pitch, and a row of

overtones that are responsible for their flute-like timbre.

Teaching birds to imitate human melodies was a popular

hobby in the 18th and 19th centuries and the bullfinch was the

favorite species (e.g. Hamersley 1717; Pernau 1768; Brehm

1832; Holden 1895; Naumann 1900). In his pioneering song

study, ‘‘Family tradition in the song development of the

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bullfinch’’ Nicolai (1959) stated that the bullfinch’s indi-

vidual bonding to its father or to its foster parent (canary or

human tutors) is the crucial factor in focusing the attention of

the juvenile bullfinches and enabling them to learn their song

patterns. He noted later (Nicolai 1969) that his human mel-

ody-singing bullfinches would sometimes omit sections and

if JN began whistling the omitted parts, the birds would begin

singing again, completing the missing modules correctly. All

15 human melody-singing bullfinches could produce con-

secutive modules in the correct-order chronological order

during alternate singing.

Alternate singing has never been reported in wild bull-

finches, but in other species, duets between pair partners

occur regularly, especially in the tropics (e.g. Thorpe 1972;

Seibt and Wickler 2000).

Materials and methods

Animals, melody tutoring program

The study is based on the historical data of 15 bullfinches,

hand-raised by 5 different human tutors kept and studied by

JN within 1967–1975 at the Max Planck-Institut fur Ver-

haltensphysiologie at Seewiesen. All 15 bullfinches learned

to sing melody modules alternately with JN. The five

bullfinches used in this study were bought at the age of

6 months, from 3 different tutors (Christian Grosch, Karl

Moller and Karl Dorr) at Angersbach, near Fulda, a former

center for tutoring bullfinches to sing human melodies

(Lichau 1989).

Melody tuition started before fledging, generally in June

of the birds’ hatching year. The tutors did not tune their

whistling for absolute pitch (frequency). Pitches of their

entire melody performances recorded at different days

varied within the range of 3 semitones. Their performances

were defined by relative pitches. Unlike the humans, the

bullfinches sang the melodies at high-pitch constancy

(Guttinger et al. 2002).

By December, after daily training for 5–6 months, the

bullfinches often sang the tutored note sequence with

excellent accuracy. However, even birds that were excel-

lent melody singers during their first winter often stopped

singing the entire note sequence correctly after the molt

and started to repeat single melody parts (modules) again

and again without completing the entire melody as

Fig. 1 Melody 1, ‘‘Der Jager aus Kurpfalz,’’ sung by Bullfinch 1

shown as spectrogram and in musical notation, using Helmholtz

notation for the names of notes. The notes are numbered according to

their position within the melody; numbers with primes identify notes

sung by the bullfinch, and numbers without primes those whistled by

JN. The beginning of a new module is indicated by an arrow. Note

that each module has a characteristic contour, e.g. rising and falling

pitch: module 1, 2, 3, 5 and 7. Note also that modules 2 and 3 are

followed by extended pauses that act as separators. In addition,

compare the Melody 1 depicted in spectrograms and notes by

listening to the original sound recording of Bullfinch 1 on S1. Notes 4

and 5 are at ‘‘critical positions’’ defined in the text

Anim Cogn

123

documented for Bullfinch 4 by ESM S5e acoustically, by

S5f schematically and by S5g with spectrograms. There-

fore, in an attempt to maintain the birds’ accuracy as

adults, JN continued to whistle the melody to the birds each

day. In Figs. 1, 2 and 4, the notes whistled by human tutors

are numbered without primes and notes sung by bullfinches

by numbers with primes.

Instead of repeating the entire melody as did the tutors

who had hand raised the birds, JN evaluated and tried to

correct each bird’s individual deficiencies. For example,

when a bird did not continue the note sequence, JN spe-

cifically whistled the continuing modules again and again.

We document a training session with Bullfinch 3, recorded

on May 13, 1971, in a film with a sound track (Haanstra

Fig. 2 Alternate singing of the Melody 2 ‘‘Im tiefen Bohmerwald’’ between JN and Bullfinch 4. Notes with primes were sung by Bullfinch 4,

those without primes by JN. Notes of the birds are framed by light gray whereas those of JN are dark

Anim Cogn

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1972) (ESM S2). ESM S3 is a schematic documentation of

7 repetitions of Melody 3 by Bullfinch 5, based on a

recording of a training session showing the mutual module

contributions for Bullfinch 5 and JN. Note that as Bullfinch

5 often did not continue after note 31 (from module 4–5),

JN repeated the consecutive note group from 32 to 40

(module 5) again and again.

Characterizations of the learned melodies

Studying a cross-cultural data base on folk songs, Tierney

et al. (2011) concluded that segmenting folk songs into

sub-melodies called modules, phrases or chunks (Zatorre

et al. 2007) are a widespread human song feature. One can

generally discern these sub-melodies by the following 3

characteristics: (1) separation from the other sub-units by

lengthened pauses; (2) differences in the melodic shape; (3)

the final note of the modules is usually particularly long.

Segmentation into sub-melodies is a particular promi-

nent acoustic feature of melodies. Therefore, in the Elec-

tronic Supplementary Material, we document the songs

analyzed both acoustically, by the original recordings and

also visually, by spectrograms. Thus, one can simulta-

neously gauge acoustically the temporal organizations of

the note sequence by pauses, the differences in the melodic

shape (contour) and the sequential errors of melody singing

and compare it to its pictorial displays on the spectrograms.

By listening to Melody 1 (ESM S1) and by following the

note sequence simultaneously on the notation and on the

spectrograms (Fig. 1), one can perceive unambiguously the

3 main criteria for modules:

1. Lengthened pauses between modules: On the spectro-

grams, the sequence of 26 notes is segmented into 4

modules by pauses varying between 0.1 and 1 s.

2. Differences in the melodic shape (=contour): Module 1

has rising pitch, modules 2 and 4 have descending

pitch, and module 3 has both rising and falling pitch.

3. Lengthened duration of the module’s terminal notes:

note 6, 20 and 26.

The three learned human melodies differ substantially in

melodic characteristics, in numbers of modules (note

groups separated by longer pauses) and in numbers of

different pitches and durations of notes (see Table 1).

Melody 1 (‘‘Der Jager aus Kurpfalz’’), learned by

Bullfinches 1, 2 and 3, is documented in parallel by sound

spectrograms, in musical notes (Fig. 1, for Bullfinch 1

singing alone) and as a sound file (S1). Alternate singing

between Bullfinch 1 and JN and versatility of entries at

critical position is shown schematically on Fig. 3.

Melody 2 (‘‘Im tiefen Bohmerwald’’ and ‘‘Abend wird

es wieder’’), learned by Bullfinch 4, is documented in

musical notes (S5a), acoustically, as audio files (S5b):

whistled by tutor Moller, S5c: sung correctly by Bullfinch 4

and by the corresponding spectrograms (S5d). Errors and

module repetitions are documented on S5e-h. Alternate

singing with JN is documented by Fig. 2 and S6a.

Melody 3 (‘‘In einem kuhlen Grunde’’), learned by

Bullfinch 5, is documented while alternate singing with JN

in spectrograms on Fig. 3 and as notation on S8.

Recording and analyses

JN recorded the singing using a NAGRA III b tape recor-

der. We analyzed the songs with Avisoft-SASLab Pro

software (Specht 2000).

Data Analysis

1. How accurately do bullfinches sing the sequence of

notes solo?

We start by investigating whether the bullfinches retrieve

the learned note sequences from memory in the same way

as humans, in sub-sequences separated by noticeable pau-

ses (Zatorre et al. 2007), or as a single linear chain.

In order to focus on flexibility, we selected, based on our

acoustic impression, song parts where deviating sequences,

particularly repeats of preceding modules, occurred. For

birds 4 and 5, we analyzed five different sets of melody

performances, each lasting from 20 to 50 s. Note that for

solo singing with correct temporal and sequential organi-

zation, we have previously documented the concordance

between the note sequences of the human teacher and the

songs of Bullfinch 4 for the note sequence from note 1 to

note 15 (Guttinger et al. 2002).

Bird 4 repeated particular modules multiple times and

made sequential errors in singing, as documented by S5d-h.

Table 1 Characterization of the three learned melodies

Melody

number

Number of

notes

Number of

chunks

Duration

in s

1 26 4 17

2 45 7 18

3 50 6 15

Segmenting the note sequence into sub-melodies (modules) by pauses

is a particular prominent acoustic feature of melodies. Listen to

Melody 1 (ESM S1) and simultaneously follow up its notation in

notes and spectrograms (Fig. 1). Additionally, in the electronic sup-

plementing material Melody 2 is documented both acoustically

whistled by the human tutor (S5b), sung by Bullfinch 4 (S5c) and

visually, by spectrograms (S5d) of the song documented acoustically

(S5c) and in the musical notation (5a). Melody 3 is depicted in

musical notation (S8)

Musical notation gives additional information on differences in the

melodic shapes (contour) of modules, on the characteristics of notes

(note duration in relation to other notes, its pitches and intervals

between notes)

Anim Cogn

123

Bird 5 only repeated module 4, but did not make any

detectable errors in the note sequence.

Using the solo singing of Melody 2 by Bird 4, we

investigated the following questions:

1.1 Did the bird phrase the sequence into melodic sub-

units (modules) by lengthened pauses where the

human teacher did (Table 2)?

1.2 Temporal organization of modules by different note

durations (Table 3).

1.3 Characterization of errors (schematic documentation

of errors S5f).

1.4 Are errors disproportionally located at the beginning

and ending of module (Table 2), a criterion for

chunks?

1.5 Did Birds 4 and 5, by repeating modules, enhance the

accuracy of those modules adjusting the pitches and

durations of notes to those of the human model

(Table 3)?

2. Alternate singing

We focus on the correct entries and continuations, dis-

tinguishing between correct and incorrect choices, deter-

mining the rhythmical, sequential order and versatility of

the two partners’ contributions. To produce the specific

note subsequence at the appropriate time in response to the

antecedent melody part, the bullfinch has both to perceive

the antecedent melody part of JN and at the same time to

anticipate its own entry and select the correct continuation.

In the analysis of the recordings of alternate singing, we

asked the following questions (Table 4):

2.1 Did the birds start singing only when JN stopped

(parallel singing), or also while he was still whistling?

2.2 Did the birds enter only at the beginnings of modules,

or also in the middle of modules (Table 4)?

2.3 Did they continue singing at random, beginning at

any note of the melody (H0), or from any point in the

Fig. 3 Versatility of entries at

critical positions for Melody 1

by Bullfinch 1 and JN.

Schematic documentations of

modules whistled by JN are

framed in light gray and the

entry and continuation of

Bullfinch 1 in white. Note that in

repetition 5, the correct entry

and continuation are at the

critical position 5

Table 2 Did bullfinch 4 segment Melody 2 by pauses into modules only where the human teacher did? Points of transitional errors, an

operational criterion for chunking?

Pauses Duration of pauses Errors

Number of

the pause

Between

notes

Tutor

N = 5

Bullfinch 4

N = 5

Singing with repeats

Duration of pause Singing accurately Singing with repeats (errors) Between

modules

Within

modulesM SD M SD M SD

1 6/7 0.35 0.10 0.17 0.04 0.27 0.15 3 0

2 12/13 0.95 0.15 0.53 0.08 1.18 0.82 2 0

3 24/25 1.15 0.07 0.24 0.06 0.53 0.33 1 1

4 30/31 0.35 0.21 0.12 0.02 0.32 0.24 0 0

5 35/36 0.96 0.13 0.67 0.27 1.29 0.44 1 0

6 41/42 0.56 0.11 0.28 0.05 0.46 0.23 9 1

The phrasing into modules by pauses in the songs whistled by the human teacher Karl Moller and by Bullfinch 4 shows that the bird left pauses

only where the human tutor did. With respect whether these pauses may define boundaries of chunks: Sixteen of 18 errors occurred at the

boundaries between modules. Thus, the elevated occurrences of errors closely match the criterion for chunking

Anim Cogn

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melody, where an identical note (critical position)

that JN had just whistled occurred, or from the correct

point (H1) by continuing the sequence correctly (e.g.

at note 25 after JN just had whistled note 24, as

documented in Fig. 2?

2.4 As regards the bullfinches’ correct choice of consec-

utive note groups we assessed how variably and

flexibly the bullfinches and JN chose the positions of

their entries (Table 4).

2.5 To determine whether the bullfinch is merely

responding to JN’s last note or to longer groups of

notes (syntactical information processing), we focus

on the following two situations, which we define as

‘‘critical positions:’’

• Successive notes, identical in pitch and duration

• Identical notes that recur at different positions within

the melody.

If the bird responded only according to the last note and

did not take into account earlier notes of the melody it had

just heard, the continuation should often be not correct.

Abe and Watanabe (2011) showed that a songbird, the

Bengalese finch (L. striata), can use syntactical informa-

tion processing to discriminate songs.

3. Statistics

To study the relation between pauses and sequential

errors statistically, a criterion for chunking was tested by

binomial test. Do sequential errors occur at random from

any position within the note sequence (H0) or preferentially

at the borders between modules selectively at the first note

of modules (H1)?

To investigate whether, when alternate singing, the

bullfinches entered at random at any note within a melody

having N notes (H0), or selectively at the next note (H1), we

again used a binomial test.

Results

General remarks on the natural songs of bullfinches

The songs of free-living bullfinches are soft and contain

syllables that are similar to the whistled notes human

melodies, but the birds also sing ‘‘squeaking’’ syllables

(Guttinger et al. 2001, 2002). The bullfinches’ natural

Table 3 How did Bullfinch 4 copy the rhythmical organization by

different note values within modules from its human teacher Karl

Moller?

Number

of note

Tutor

N = 5

Bullfinch 4

N = 4

M SD M SD

1 0.32 0.03 0.32 0.01

2 0.39 0.07 0.36 0.01

3 0.18 0.01 0.15 0.01

4 0.27 0.00 0.30 0.01

5 0.33 0.07 0.23 0.00

6 0.71 0.07 0.66 0.02

7 0.25 0.01 0.26 0.00

8 0.21 0.03 0.25 0.00

9 0.26 0.02 0.20 0.01

10 0.42 0.02 0.40 0.03

The first 10 notes of Melody 2 include 5 different note values, from

semiquaver to dotted crochet in musical notation (S5). Bullfinch 4

copied these temporal differences accurately. It sang notes with an

identical pitch, but with different durations (e.g. Note 1 and 6, E flat),

corresponding to its human model firstly at point 1 as eight with

duration of 0.32 s and at point 6 as a dotted crochet with duration of

0.71 s

Table 4 Comparison of the flexibility in the entry points between the bullfinches and JN while they were engaged in alternate singing

Entries of JN Entries of the bullfinch

With the

bullfinch

number

On the

beginning

of a module

Within a

module

Correct on the

beginning of

a module

Incorrect on the

beginning of

a module

Correct within

a module

(parallel singing)

Incorrect within

a module

(parallel singing)

1 13 3 8 0 10 1

2 4 0 7 0 1 0

3 10 1 5 1 1 9

4 15 0 8 1 4 0

5 24 1 15 3 4 3

Sum 66 5 43 5 19 13

The bullfinches entered the melody after JN stopped whistling, but also while he was still whistling (parallel singing). Bullfinches 1, 2, 4 and 5

made a total of 62 correct and 21 incorrect entries. Bullfinch 3, however often confused the similar modules 1 and 3 of Melody 1 which both end

with the note A as a crotchet (see Fig. 1). It entered incorrectly 10 times, compared to only 7 correct entries

In addition, flexibility in the choice of entries of JN and the 5 bullfinches is documented. Note particularly that JN mostly whistled entire modules

as song units, whereas the birds started flexibly and correctly not only after modules, but also when he was still whistling notes within modules

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repertoire size varies between 42 and 52 different syllable

types and is thus similar to the note number in the human

melodies they learned.

How accurately do bullfinches sing the learned melody

alone?

1. Did the bird phrase the note sequence into modules

like the human model?

The segmenting of the 45 notes of Melody 2 into modules

(sub-melodies) by pauses is documented acoustically in

ESM S5b, whistled by the human tutor Karl Moller, and in

ESM S5c, sung by Bullfinch 4. The positions and different

durations of pauses can be examined visually on spectro-

grams (ESM S5d). The temporal segmenting by pauses

whistled by the tutor and sung by Bullfinch 4 was assessed

by measuring the pauses’ durations (Table 2). Both by

listening and by analyzing spectrograms, we can recognize

distinctly three longer pauses (around 1 s) and some shorter

ones. By measuring these pauses on the spectrograms, we

analyze whether Bullfinch 4 leaves long pauses only or

disproportionally often where its tutor did. We examined

two different recordings, one containing correct melody

repetitions and one with songs repeating a single-module

again and including errors (S5e). The positions of the bird’s

pauses and also the differences in the durations of its

pauses correspond closely to those of the human model:

three longer pauses—often longer than 1 s—between notes

12 and 13 (boundary between module 2 and 3), between

note 24 and 25 (the boundary between module 4 and 5) and

between notes 35 and 36 (boundary between module 6 and

7), and 3 shorter ones (in the range of 0.3–0.5 s). Note that,

when singing with errors, the bird pauses at identical

points, but by segmenting into modules by often extended

and much more variable pauses (S5h).

2. Temporal organization of modules by different dura-

tions of notes.

The temporal patterning of the sequence by notes is

documented for Bullfinch 4 by a spectrogram of the entire

melody (S5d) and in more detail for module 6, notes

36–41, in S5g. Compared to the distinct pauses between

modules, the pauses within modules are so short that we

can scarcely perceive them acoustically or measure them in

the spectrograms (a supplementary criterion for a module).

However, we can discern 45 consecutive notes and rec-

ognize their durations and pitches. The musical notation of

this performance (S5a) uses 6 categories on note values for

the ranging from semiquaver (sixteenth note) to minim

(half note) and 9 different pitches. Learning to sing a folk

song is an extraordinary challenging sequencing task. In

order to sing each of the 45 notes which are substantially

determined in duration and pitch, the bird has to time

precisely the execution of a specific motor pattern at a

particular location in the sequence.

We assessed how precisely the Bullfinch 4 copied dif-

ferent note values by comparing the measured values of the

first 10 notes between the teacher and this bird (Table 3):

These values correspond as well between the human and

the bullfinch as they do to the indicated value in musical

notation (e.g.: note 1, notated as a quaver, 0. 32 s and note

6, notated as a dotted crotchet, 0. 71/0.66 s).

Characterizations of errors

We recognized the following irregularities in the repeti-

tions of Melody 2 by Bullfinch 4, documented as Audio

Files in the Electronic Supplementary Material S5e, as

spectrograms in S5g and S5h and schematically depicted in

S5f:

• Repetitions of antecedent note groups, by starting again

after an extended pause at the first note of antecedent

modules, as depicted in sonograms (S5h).

• Skipping ahead, omitting notes, but continuing the

melody correctly at later positions after a lengthened

pause in relation to the duration of the omitted melody

part (S5g and S5h). Correct continuation after omission

is of particular interest, since it appears to indicate

hierarchical representation (see ‘‘Discussion’’).

• Repetition of the antecedent note (S5h).

We counted as follows: 11 repetitions of antecedent note

groups, 7 occurrences of skipping ahead omitting notes and

two repetitions of a note. Furthermore, we could not detect

any other categories of errors.

Skipping ahead, omitting notes but continuing correctly

after lengthened pauses, is documented by spectrograms in

ESM S5g, and S5h. It occurred at 3 different positions: At

the boundary between modules 1 and 2, having skipped

from note 5–7 (S5g), from the middle of module 3 (note

20) to the first note of module 4 (note 25) and at the

boundary between modules 41/42, from note 41 to note 43.

Are errors disproportionally higher located at the

beginnings and endings of modules?

To assess whether the melody modules might be com-

parable to chunks, we studied the positions of errors in note

choices in relation to pauses between modules (Table 2).

Sixteen of 18 observed errors documented acoustically

(S5e), graphically (S5f), and as spectrograms (S5g)

occurred at endings of modules (H1). Melody 2 has 45

notes and includes 7 modules, so the probability that an

error occurs at the end of a module by chance is 7/45, that

is, 0.156; a binomial test against this null hypothesis shows

that the observed tendency for errors to occur at the end of

modules is highly significant (P = 1.3 9 10-11). All 11

Anim Cogn

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repeats restarted not from any random positions but at the

first note of a module (and there were 6 restarts at note 36,

from the beginning of module 5 to notes 41 or 45). A

similar binomial test shows that this tendency for restarts to

happen at the beginning of a module is again highly sig-

nificant (P = 1.3 9 10-9). The extremely elevated occur-

rence of errors at the border between modules closely

matches the operational criterion for chunking (Terrace

2001).

Finally, we studied whether the Bullfinches 4 and 5 were

trying to enhance the accuracy of the copy, by measuring

the variation of the notes structure (frequency and dura-

tions). The variations of notes values are documented for

the human teacher and Bird 4 on Table 3, (frequencies are

not shown,) for the notes of particular modules repeated

again and again. Because both bullfinches repeated these

notes with high constancy its note values and in its pitches

(not shown), we suggest that these repetitions (used instead

of progressions) were caused by an actual memory

blockage.

In summary, analysis of the bird’s solo singing, specif-

ically the phrasing in sub-melodies marked by pauses,

indicates that the bullfinch did not retrieve the learned

melody as one coherent unit—as a linear chain of notes—

but as modules, containing of much smaller sub-sequences

containing 4–12 notes.

Alternate singing

We focus on the entries and on the consequent continua-

tions, distinguishing between correct and false choices and

continuations, analyzing sequential, rhythmic orders and

assessing the versatility of the two partners’ contributions.

For Bullfinch 4 and JN, correct and incorrect entries for

a single sequence (the notes of Melody 2) are depicted in

spectrograms (Fig. 2) as audio files (S6) and schematically

the variable points of entry (S7). In the spectrograms, the

notes sung by bullfinches can be distinguished from those

whistled by JN by the pronounced overtones, which are

nearly absent in the human’s whistled notes (S4).

In the spectrogram of Fig. 2, JN started and whistled the

first module of the melody (notes 1–6). Bullfinch 4 entered

at position 4 sang notes 4–6 (parallel singing) with its

human partner until the end of module 1 where JN stopped

while the bullfinch continued alone until position 12. JN

took over correctly at note 13 and continued up to position

24. The bird entered again, at position 24 slightly (30 ms)

too early, but with the correct note (note 25)—not con-

sidered as an error—and continued singing until note 35.

From this position, JN continued up to note 41. Instead of

finishing the melody, which contained a total of 45 notes,

Bullfinch 4 then, after a pause of 1 s, started again from the

beginning, which we rated as incorrect. The bird continued

singing up to note 12, when JN took over. S6a documents

additionally the temporal variation of the bird’s entries at

position 24/25 in 3 repetitions of the melody and as audio

files (S6b-S6c).

Data on entries of the 5 bullfinches and JN are given in

Tables 4 and 5. As regards the birds’ choices of the point of

entry, all bullfinches sometimes entered the melody while

JN was still whistling (parallel singing), not only when he

had stopped. They tended to start by correctly singing the

first note of the next module (43 occurrences) or the next

note within a module (19 occurrences). Table 4 shows that

Bullfinches 1, 2, 4 and 5 made a total of 62 correct and 21

incorrect entries. Bullfinch 3, however, often confused the

similar modules 1 and 3 of Melody 1, which end with the

identical note (see Fig. 1) and entered incorrectly 10 times,

compared to 7 correct entries. We assessed the accuracies

of the entries for each bird separately. In a melody of N

notes, the probability of entering at the correct point by

chance is 1/N. The significance of the number of correct

entries made can be assessed by a binomial test. The data

and the corresponding significance levels are shown in

Table 5; it can be seen that even for the least accurate bird

(Bird 3), the probability of the observed number of correct

entries occurring by chance is vanishingly small.

We continue by studying the flexibility of the entry

positions for JN and the birds, documented here in sche-

matic tabular sequences (Bullfinch 1, Melody 1: Fig. 3,

Bullfinch: 4, Melody 2: S7, Bullfinch 5 S3) based on

spectrograms of recorded alternate singing repetitions. The

birds were not only correct with respect to their entries, but

were also flexible in their behavior, as can be seen on S7

and on in Table 4. The beginnings and endings of the note

contributions vary much more in the songs of the bull-

finches than in those whistled by JN. He whistled the entire

modules, whereas the bullfinches started flexibly and cor-

rectly not only at the end of a module (38 times) when JN

stopped, but also when he was still whistling (parallel

singing: 18 times). In this context, the high flexibility in the

choice of entries of Bird 1 (documented in Fig. 3) is par-

ticularly notable. While JN constantly whistled module 1,

from note 1 to 6, the bullfinch entered at 3 different notes

Table 5 Binomial tests for significance for correct entries

Bird N n ce ic Bi

1 26 16 18 01 6.2 9 10-25

2 26 04 08 00 4.8 9 10-12

3 26 08 06 10 1.1 9 10-10

4 45 07 12 01 1.8 9 10-19

5 50 09 19 06 6.0 9 10-21

N = number of notes of the melody, n = number of melody repeats

studied, N n(=the number of positions to enter at random),

ce = number of correct and ic = number of incorrect entries

Anim Cogn

123

within the module by parallel singing and at note 7 by

alternate singing. Thus, given that flexibility is a criterion

for distinguishing decisions and choices based on cognition

from those based on conditioning (Griffin and Speck 2004),

so we exclude inflexibly programmed conditioning as the

main explanation for the birds’ correct choices of entries.

Finally, we determine whether the bullfinch is merely

responding to JN’s last note or to a group of notes by

discriminating syntactic rules of the note sequence (Abe

and Watanabe 2011). We focused on the following two

aspects, which we call critical positions:

1. Successive notes, identical in pitch and duration,

within a melody module: Consider, in the musical

notation of Melody 1 (Fig. 1), positions 3–6 sung as

a’’’. If Bullfinch 1 responded only according to the last

note a’’’ without considering what are preceded in the

note sequence, its singing would deviate substantially

from the melody.

If the bird responds only according to the last note, its

continuation should often be incorrect. However, as

Fig. 3 shows, Bullfinch 1 was able to accurately take

up the melody at four different positions with no

observed errors. This degree of accuracy requires that

the bird attend to pitch, duration and rhythmical timing

of several preceding notes.

2. Identical notes that recur at different positions within the

melody: If the bird considers only the last note when

deciding upon its entries, deviating note sequences

would accumulate at these positions. The most instruc-

tive examples showing that Bullfinch 5 could not only

perceive melody parts, but was also capable of short-

range planning, occurred when JN did not continue the

melody (spectrograms on Fig. 4 and tabular documen-

tation of the contributions of JN and the bird on S3), but

went to an antecedent part, (from position 40 to 32) and

repeated the sequence 11 times again until note 40.

Bullfinches 5 waited until position 40 and entered cor-

rectly with note 40, or later at note 41.

These data show that the decision on entry is at least

based on previously heard note groups, not just on the

last note.

Discussion

Aspects of memorization and recall of the melody (solo

singing)

For bullfinches, learning the long note sequences of human

folk melodies is a most demanding task, achieved by only a

subset of tutored individuals. Holden (1895), who imported

and sold melody-singing bullfinches in America, described

their performances in detail. He listed about 50 different

German, British and American popular tunes. The best

singers sang 2–3 melodies, containing at the maximum

about 50 notes. But only about one-third sang the entire

Fig. 4 Parallel singing of Bullfinch 5 (notes with primes) of Melody

3 with JN (notes without primes). JN repeats the module 5 (notes

32–40) twice. Bullfinch 5 entered correctly twice at position 40 and

finally it started again accurately at the end of module 6 at note 49 and

sang the continuing terminal notes in parallel with JN

Anim Cogn

123

tutored sequence accurately. Another third copied only

about half of the tutored sequence, and the remaining birds

did not sing more than one or two fragments (modules).

JN’ s birds, as a group, performed significantly better,

probably because of the continuing long-lasting individu-

alized interactive tutoring that JN provided. These suc-

cessful birds provide considerable data on studying melody

learning with respect to sequencing.

We distinguish the following 3 hierarchical levels of

organization (Fig. 1) in the songs: Single notes, at the

lowest level; coherent groups of notes as a module at the

intermediate level; and the entire melody, the correct

sequence of modules, at the top level. To sing a melody,

accurately the bird must learn at least the following three

hierarchically organized motor control functions:

1. To sing each note at the pitch and duration of the

corresponding note within the melody.

2. To sing consecutive notes of a module in the specific

temporal pattern (rhythm) for this melody.

3. To assemble single modules into the entire sequence of

the melody: In a melody consisting of 4–7 modules,

each module must be sung in its correct position in the

sequence.

The bullfinches retrieved the melody whistled by the

human model by reorganizing it into much smaller mod-

ules separated from one another by pauses, a criterion for

chunking (Terrace 2001). After chunking individual notes

into modules, the birds merged the modules into the

higher-order level of a hierarchically organized melody.

Hierarchical storage and recall from several levels is much

more demanding than performing a linear chain of

responses. However, chunking, unlike linear storage,

ensures that small sequential errors do not prevent the bird

from continuing correctly: Omitting a note within a module

on the intermediate level should not block retrieval of notes

of the next consecutive module. We counted 7 instances in

which a bird omitted a note or note group (S5h) but then

performed the next module accurately—hinting at hierar-

chical storage. An additional indication that temporal

organization may be represented at a higher level is given

by the durations of the pauses after the bird omitted parts of

the melody. Pauses before continuing correspond to the

length of the omitted part: The pauses were short (in the

range of 2 s) when just one note was omitted (S5h) and

much longer (5 s) when a note sequence (20–25) was

omitted.

We assume that, as the initial step, the bullfinches

started to memorize and to practice just a single-module

containing 4–12 notes and as their performance progressed,

they learned to sing more of the melody, but still as isolated

modules. As a final step, in order to sing the entire, much

longer note sequence correctly, they had to assemble the

modules together in the correct temporal and melodic

order. As untutored bullfinches do not emit songs con-

taining long coherent sequences, and because even the

tutored birds reported by Holden (1895) often failed to

learn an entire melody, we supposed that the final step, the

coupling of the modules to form a sequence of 25–50 notes,

is the upper limit for sequential learning and requires more

than what is required by song learning in nature. Such

extraordinary success seems to be achieved by the

continuing intensive individual, daily tuition by JN

throughout the birds’ lives.

Other species may respond similarly. Note that for

Nightingales (L. megarhynchos), learning of the pattern

structure (at the lower hierarchical organizational level)

and of sequencing different pattern structures (at the higher

level) are two different aspects of song acquisition. ‘‘Low’’

exposure frequencies (10–30 compared to 100 times) lim-

ited learning of sequential orders on the higher level, but

did not influence the number and the accuracy of the copies

of the subordinated patterns (Hultsch and Todt 1989,

1992). Rose et al. (2004) used data from the White-

crowned Sparrow (Zonotrichia leucophrys) to test a con-

ceptual model of a mechanism in which motor programs

link song parts together. Early, in song development, while

still perfecting single-module structures, the birds began to

combine modules; first, primarily into pairs, then into

longer sequences. Their model posits that only module

pairs that match the tutor model are reinforced maximally

over time and refined into final form.

Alternate singing gives insights into how the bird’s brain

processes a melody

We now consider the cognitive processes that allow the

bullfinch to continue to sing the correct melody part when

its human partner stops. To continue singing appropriately,

the birds had to switch from attentive listening to singing,

as an immediate response to the antecedent notes whistled

by JN. As discussed above, the bird’s behavior—appro-

priate entries at critical positions (identical notes which

occur at several positions within the note sequence, e.g.,

Fig. 3—reveals that their choices are not based entirely on

the last note but at least on the preceding note groups, or

even on much longer parts of the melody.

What mechanism is responsible for this behavior? We

consider ‘‘inner singing’’ (imagined) to be a prerequisite

for correct entries. As soon as the human starts, the birds

can match the note sequences it hears to its memorized

representation in the brain. At the point of changeover,

from perception (sensory side) to vocalization (motor side),

cognitive processing is required. Listening attentively to

the note group just whistled by the human may simulta-

neously activate the appropriate motor program to sing the

Anim Cogn

123

consecutive notes together with the human (parallel sing-

ing), but may, as long its human partner whistles, suppress

the transformation into motor commands to sing. The

bird’s brain may compare the currently perceived notes

from its partner with its memorized note sequence repre-

sentation. This comparison can establish ‘‘the inner world’’

that one associates with awareness: As soon as the human

ceases to whistle, the already-activated motor program

(‘‘imagined singing’’) can be translated into motor com-

mands to sing the consecutive notes aloud. In this way,

accurate entry and continuation may be assured. We

interpret the occasional occurrence of parallel singing as

the inability (perhaps because of incomplete learning) to

suppress its own execution during the partner’s singing.

For the bird to cue in accurately, its ability to listen to

the partner’s contributions and its ability to control its own

singing must become tightly coupled by learning. Prather

et al. (2008) identified auditory–motor mirror neurons in

the songbird with properties similar to the visual-motor

mirror neurons first observed in the monkey frontal cortex

(Rizzolatti and Craighero 2004). The songbird auditory–

motor mirror neurons fired both when a song was per-

formed by the bird and when the same song was heard. It

has been suggested that such properties in mirror neurons

suit them for the perception of visual and auditory com-

munication, including both gestures and speech (Koehler

et al. 2002). Activation of auditory mirror neurons of a

bullfinch hearing its human partner whistle may allow the

bird to use the neurons that have already been activated by

listening to continue the note sequence with the corre-

sponding motor commands.

Alternate singing by bullfinches with conspecifics, with

other bird species or with humans, has previously only

been reported as a single anecdote with a canary (Henschel

1903). Thus, this newly observed behavior may have

resulted from the supplementary daily interactive training

by JN provided to individual birds. He specifically tried to

perfect the bird’s performance by repeating missing

continuing modules again and again immediately after a

bird did not continue the melody to the end (see Supple-

mentary Material, S2: film and sound track (Haanstra 1972)

and S3: tabular documentation of the reciprocal song

modules whistled by JN and sung by Bullfinch 5). It was a

kind of ‘‘action-based’’ teaching (Nelson and Marler 1994).

Direct singing interactions between tutor and bird are

considered important for song learning (Burt et al. 2007).

The additional interactive melody rehearsal might have

specifically tuned the auditory–motor neurons in the song

circuit to switch rapidly between auditory following of the

melody and active singing.

Melody learning and alternative singing demonstrate

that as follows: (1) Bullfinches can represent a sequence of

vocal patterns as a set of modules, or ‘‘chunks’’ (Miller

1956) and (2). They have an internal representation of it.

They can cope with the complex and demanding cognitive

challenges of perceiving a human melody in its rhythmic

and melodic complexities and learning to sing it accurately.

Acknowledgments We thank Christina Meier for very helpful and

encouraging comments to improve the presentation of the results. Dr.

Jean–Pierre Stockis from the department of mathematics of TU Ka-

iserslautern gave advices and did the statistical analyses. Thanks are

also due to Tim R. Birkhead, Jessica Boffo, Manfred Gahr, Irene M.

Pepperberg and Jeffry Tesselink for constructive comments on the

earlier drafts and for correcting the English, and to three anonymous

referees.

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