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Dialects in pygmy marmosets Population variation in call structure.

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American Journal of Primatology 71:333–342 (2009)
RESEARCH ARTICLE
Dialects in Pygmy Marmosets? Population Variation in Call Structure
STELLA DE LA TORRE1 AND CHARLES T. SNOWDON2
1
College of Biological and Environmental Sciences, Department of Ecology, Universidad San Francisco de Quito, CumbayáQuito, Ecuador
2
Department of Psychology, University of Wisconsin, Madison, Wisconsin
Population variation in primate vocal structure has been rarely observed. Here, we report significant
population differences in the structure of two vocalizations in wild pygmy marmosets (Trills and
J calls). We studied 14 groups of pygmy marmosets Callithrix (Cebuella) pygmaea pygmaea from five
populations in northeastern Ecuador. We analyzed the acoustic structure of Trills and J calls recorded
from two adult animals in each group through focal samples. Although individuals and groups within a
population differed in call structure, we found consistent structural differences at a population level for
Trills and J calls. Pair-wise comparisons for the two call types point to San Pablo and Amazoonico as
the populations that differed the most, whereas Hormiga and Zancudococha showed the least
differences. Discriminant function analysis indicates that calls from each population could be classified
accurately at rates significantly above chance. Habitat acoustics, social factors and genetic drift may
explain interpopulation vocal differences. This is the first evidence of within-subspecies vocal
differences, or dialects, in wild populations of a neotropical primate species. Am. J. Primatol.
71:333–342, 2009. r 2009 Wiley-Liss, Inc.
Key words: vocal variability; pygmy marmoset; Callithrix (Cebuella) pygmaea; Ecuadorian
Amazon; dialects
INTRODUCTION
Bird song has long fascinated those interested in
the development of communication because the
variability seen in different populations of the same
species (or subspecies) suggests that song might be
learned from others [reviewed by Catchpole & Slater,
1995]. However, less evidence exists of similar
processes in nonhuman primates [Egnor & Hauser,
2004; Janik & Slater, 1997]. Variation in vocal
structure between populations has been described
only in few primate species, wild chimpanzees Pan
troglodytes [Crockford et al., 2004; Marshall et al.,
1999; Mitani & Brandt, 1994; Mitani et al., 1999],
wild silvery gibbons Hylobates moloch [Dallmann &
Geissmann, 2001], captive Barbary macaques Macaca sylvanus [Fischer et al., 1998], provisioned
Japanese macaques M. fuscata [Green, 1975; Masataka, 1992] and between subspecies of squirrel
monkeys Saimiri oerstedi and of saddle-back
tamarins Saguinus fuscicollis [Boinski & Newman,
1988; Hodun et al., 1981]. This raises the question of
what has led to such flexible communication in birds
and in humans in contrast to the relatively inflexible
vocal development of nonhuman primates. Snowdon
et al. [1997] argued that this perceived lack of vocal
variability could be an artifact of the lack of
appropriate quantitative data for this order. In this
study, we present evidence to support their argu-
r 2009 Wiley-Liss, Inc.
ment, documenting interpopulation differences in
the physical structure of two separate vocalizations
of the pygmy marmoset Callithrix (Cebuella)
pygmaea pygmaea. We discuss how habitat acoustics,
vocal learning and genetic drift could be influencing
the reported differences.
The pygmy marmoset is an arboreal primate
restricted to river-edge forests in the Upper Amazon
basin [de la Torre, 2000; Hershkovitz, 1977; Soini,
1988]. Visibility in these forests is generally poor,
therefore, pygmy marmosets, as other arboreal
primates, are likely to be highly dependent on vocal
communication [Marler, 1965; Seyfarth, 1987]. Like
other callitrichines, pygmy marmosets are cooperative breeders that live in stable, heterosexual groups
varying in size from two to nine individuals,
with small home range areas from 0.1 to 1.2 ha
Contract grant sponsor: USPHS Grant; Contract grant number:
MH029775; Contract grant sponsor: National Geographic
Society; Contract grant number: 5806-96.
Correspondence to: Stella de la Torre, Universidad San
Francisco de Quito, Av. Interoceanica y Jardines del Este,
Cumbayá-Quito, Ecuador. E-mail: stella@usfq.edu.ec
Received 18 July 2008; revised 25 November 2008; revision
accepted 25 November 2008
DOI 10.1002/ajp.20657
Published online 8 January 2009 in Wiley InterScience (www.
interscience.wiley.com).
334 / de la Torre and Snowdon
[Ferrari & Lopes Ferrari, 1989; Soini, 1988; Yépez
et al., 2005]. Group cooperation in the care of young
requires close coordination between group members,
and this is mainly achieved through vocal communication [de la Torre & Snowdon, 2002; de la Torre
et al., 2000; Snowdon & Cleveland, 1984; Soini,
1988].
Captive and wild pygmy marmosets use Trills
and J calls (Fig. 1) to maintain short-range contact
and to mediate interactions between group members
[Elowson & Snowdon, 1994; Elowson et al., 1992;
Pola & Snowdon, 1975; Snowdon & Elowson, 1999;
Snowdon & Hodun, 1981]. These contact calls are
variants of a sinusoidally frequency modulated tone
(Trills and J calls lower frequency: above 7 kHz; peak
frequency: approx. 12 kHz) and have a pulsatile
temporal structure (Trills: 32–38 cycles/sec, J calls:
17–23 cycles/sec). Trills are usually emitted when
animals are no more than 10 m apart while they are
feeding on exudates, foraging for insects, traveling or
resting, whereas J calls are emitted at caller–receiver
distances between 11 to 20 m. When J calls are
produced at distances less that 5 m of a potential
receiver, the calling animal either begins to travel
within 5 min after emitting the call, or approaches an
exudate source, or responds to a bout of babbling of
an infant [de la Torre & Snowdon, 2002; Snowdon &
Hodun, 1981]. The relationship between the use of
these call types and the distance between the calling
animal and the potential receivers suggests that
pygmy marmosets vary the use of these calls in a way
appropriate to the effects of habitat acoustics [de la
Torre & Snowdon, 2002; Snowdon & Hodun, 1981].
Yépez et al. [2005] found that each of four
populations of pygmy marmosets in northeastern
Ecuador had distinct preferences for tree species
used for exudate feeding that were unrelated to the
abundance of each species in that population. These
results are an indication of population differences in
behavior and, coupled with preliminary indications
of differences in vocal structure, led us to hypothesize
that each population would differ from the others in
the structure of Trills and J calls.
METHODS
Study Area
We gathered data in five areas in northeastern
Ecuador in an east–west transect of approximately
300 km and a north–south transect of approximately
100 km. La Hormiga population is located in
the margins of the Laguna Grande of the Cuyabeno
hydrographic system. The Zancudococha population
is located on the edges of the Zancudococha
Lake. The San Pablo population is located in
the margins of the Aguarico River. The Sacha
population is located in the margins of the Napo
River. The Amazoonico population is located in
the margins of the Arajuno River (Fig. 2). Each
population is separated from the others by at least
30 km; large rivers and large extensions of open
areas or terra firme forests, not used by
the marmosets, are natural boundaries for all
populations.
These areas have an altitude of 230–360 m above
sea level. The habitats of San Pablo, Sacha and
Amazoonico are varzea forests, seasonally flooded
by white-water rivers, with different degrees of human
alteration caused by agriculture and selective logging.
The areas of Zancudococha and La Hormiga are
edge habitats between terra firme and igapo forests
seasonally flooded by black-water rivers. These
habitats have not been affected by agricultural
Fig. 1. Spectrograms of pygmy marmoset vocalizations. (a) Trill and (b) J call from La Hormiga (H) and Amazoonico (A) populations.
FFT size: 256, Hanning window.
Am. J. Primatol.
Vocal Variability in Pygmy Marmosets / 335
activities but the area of La Hormiga had a high rate of
tourism during the years when our research was
carried out at that site (1996–1998) [de la Torre et al.,
2000].
Fig. 2. Location of the studied populations of pygmy marmosets
in Ecuadorian Amazonia (1, La Hormiga; 2, Zancudococha; 3,
San Pablo; 4, Sacha; 5, Amazoonico).
Data Collection
We observed 14 groups of pygmy marmosets in
the five populations for a total of 1,722 hr of direct
observation. All observations were carried out in the
rainy season (March through August) (Table I). Body
lengths of adult and subadult individuals in all
groups ranged from 13 to 15 cm and did not differ
among populations. Group size varied from three to
eight individuals, and the home-range size varied
from 0.15 to 1.2 ha (Table I). Distances between
neighboring groups varied from 30 m (groups 1 and 2
at Zancudococha) to 1,000 m (groups 1 and 2 at La
Hormiga). All the research methods were reviewed
and approved by the Ecuadorian Ministry of the
Environment, which gave us the legal permit to
conduct the research.
Vocalizations
Two to three field workers observed the 14
groups of pygmy marmosets. We classified marmosets in each group by size and other morphological
characters (e.g., presence of whitish nasal stripe)
into approximate age classes [Soini, 1988]. Sex
determination was possible in adults and in most of
the subadult animals based on the scrotal pigmentation of males. The vocalizations of the marmosets in
a group were recorded using focal samples, each
sample lasting a total of 5 min. At least two focal
samples of the adult (male and female) members of
the groups were carried out per day of observation in
TABLE I. Population Coordinates (UTM), Months and Hours of Observation, Group Size Range, and Home Range
Size of all Studied Groups
UTM
coordinatesa
Months of
observation
Group
Hours of
observationb
Group size
rangec
Home range size
(ha)d
Amazoonico
219290E,
9883728N
July 2003
June 2004
A1
A2
114
80
4–5
3–4
0.15
0.40
San Pablo
341767E,
9969737N
July 2001
July 2002
June 2003
July 2004
P2
P4
P5
126
107
110
5–7
4–6
4–7
0.45
0.22
0.31
Sacha
337296E,
9946861N
August 2001
June 2002
August 2003
S1
S2
S3
153
143
159
4–6
5–8
5–7
0.37
1.20
0.40
La Hormiga
368315E,
3685N
April, May 1997
G1
G2
G3
105
100
105
6
4
6
0.90
1.09
0.53
Zancudococha
445459E,
9933749N
June, July,
August
1997
Z1
Z2
Z3
140
140
140
6–7
7
5–6
0.73
0.40
0.78
Population
a
Zone 18, Datum PSAD56.
Hours of observation rounded to the nearest hour, rainy season only.
Variance in group size is the result of differences in group sizes among field seasons.
d
Home range size was estimated by connecting the extreme location points of group members during the study period; the periphery that enclosed all points
was considered as the home range perimeter and the area inside the perimeter was calculated [Yépez et al., 2005].
b
c
Am. J. Primatol.
336 / de la Torre and Snowdon
each group. These samples were evenly distributed
throughout the day.
The vocalizations of the focal individuals
were recorded with a high fidelity stereo recorder
(Marantz PMD 222, Marantz, frequency response:
40–14,000 Hz) and a unidirectional microphone
(Sennheiser ME66, Sennheiser, Germany, frequency
response: 40–20,000 Hz72.5 dB) at a recording volume that optimized the recording of the calls. In all
groups the recording distances ranged from 1 to
10 m. We annotated the vocalizations emitted by the
focal animals on the tape. Focal recordings were done
only when animals were visible and could be clearly
identified.
Acoustic analysis
We used Signal 2.29 (Engineering Design) and
SoundEdit (Macromedia) to construct spectrograms
of calls (FFT size: 256, Hanning window). We
selected 15 Trills and 15 J calls with high sound
clarity, emitted by the adult male and the adult
female in each of the groups. These vocalizations
were selected from at least five focal samples carried
out on different days throughout a sampling period
and were evenly distributed throughout the day (in
those groups that were observed in different years
we used the vocalizations recorded in only 1 year for
each focal animal to avoid the possibility of changes
in group composition between years). We analyzed a
total of 420 Trills and 420 J calls.
We measured the acoustical variables with the
cursors of the display screen and recorded four
variables: (1) total call duration (in ms); (2) number
of cycles (for Trills) or notes (for J calls)/sec, obtained
by dividing the number of complete cycles or notes by
the total duration of the call (in sec); (3) minimum
frequency (in kHz); (4) upper or maximum frequency
(in kHz). We also calculated the frequency bandwidth (maximum minus minimum frequency in kHz)
of each call.
Data Analyses
We used each of the 15 calls from the adult male
and female in a group to evaluate inter-individual
variability with unpaired t-tests for each acoustic
variable within each group. For analyzing population
differences, we averaged all the acoustic measurements for a given call type to obtain a single value for
each variable per subject; thus, degrees of freedom in
our interpopulation analyses were based on the
number of focal animals (N 5 28 animals) and not
the number of individual calls. We carried out two
complementary statistical analyses of the acoustic
variables of Trills and J calls, after confirming that
the data set met the conditions of normality,
independence and homoscedasticity. Nested ANOVAs
(SuperAnova 1.11, Abacus Concepts for MacIntosh)
were used to determine interpopulation differences
Am. J. Primatol.
after taking into account group and individual
variability, with population as the main factor, group
as the factor nested within population and individuals nested within group. Significant differences
between pairs of populations were determined with
the Fisher’s PLSD test (P 5 0.05). We also used
discriminant function analyses (SPSS version16.0)
to complement ANOVA results for individual acoustic variables to determine which variables
contributed most to differentiation of populations
with Wilks’ lambda. The resulting discriminant
functions were used to classify Trills and J calls by
population and the proportion of correctly classified
calls was tested against the expected values (20% for
each population for each call type), using a w2 test.
Sex differences were evaluated with unpaired t-tests
(StatView SE; Abacus Concepts for MacIntosh).
RESULTS
Individual and Sex Differences
Within each group the Trills and J calls of the
individual animals differed significantly in at least
one of the variables that we measured, but across the
entire sample (14 males and 14 females) we found no
consistent or significant pattern of differences
between sexes in either Trills and J calls
(Appendix A).
Interpopulation Differences
After controlling for group and individual
variability, we found significant interpopulation
differences in all of the acoustic variables of Trills
and J calls.
Trills
The results of the nested ANOVAs showed that
Trill structure differed significantly among all
populations (Table II). Marmosets at Amazoonico
emitted the shortest Trills with the narrowest
bandwidth and the highest number of cycles/sec
whereas marmosets at Sacha emitted the longest
Trills. Marmosets at La Hormiga and Zancudococha
emitted Trills with the lowest number of cycles/sec.
The lowest minimum frequency was recorded in the
Trills of La Hormiga and Zancudococha. The highest
maximum frequency was recorded in the Trills of
San Pablo. In the discriminant function analysis,
cycles per second, minimum frequency and duration
were the main variables in statistically differentiating Trills from the five populations. Trills were
correctly classified to the population of the caller in
71.4% of the cases, compared with the expected 20%
for each population (w216 ¼ 59:1, Po0.0001). Using
the cross-validation, leave-one-out method, classification was correct in 50.0% of the cases (w216 ¼ 47:5,
Po0.0001).
Vocal Variability in Pygmy Marmosets / 337
TABLE II. Interpopulation Differences in Trill Acoustic Parameters (Mean 7 SE; Populations With Different
Letters Differ Significantly—Fisher’s PSLD Tests—on That Variable; F and P Values From Nested ANOVAs)
Population
Amazoonico
Sacha
San Pablo
Zancudococha
Hormiga
F4,11
P
Duration (ms)
Cycles/sec
211.25710a
348.17717b
277.33723c
283.57718c
310.3776c,b
5.86
0.009
38.5270.6a
33.9370.6b
33.2770.6b
31.1070.7c
31.1770.7c
30.57
0.0001
Max. freq (kHz)
10.5370.3a
11.9470.3b,c
12.2370.4b
11.2270,1a,c
11.4070.2a,b,c
4.53
0.02
Min. freq (kHz)
8.0270.2b,c
8.7170.2a,c
8.7270.2a
7.8170.1b
7.7370.1b
5.88
0.009
Bandwidth (kHz)
2.5170.2a
3.2370.2b
3.5170.2b
3.4170.1b
3.6670.3b
4.92
0.02
TABLE III. Interpopulation Differences in J Call Acoustic Parameters (Mean 7 SE; Populations With Different
Letters Differ Significantly—Fisher’s PSLD Tests—on That Variable; F and P Values From Nested ANOVAs)
Population
Amazoonico
Sacha
San Pablo
Zancudococha
Hormiga
F4,11
P
Duration (ms)
590.50728a
582.50719a
730.67730b
751.83720b
705.17727b
7.32
0.004
Notes/sec
17.3370.8a
18.4070.7a,b
18.5871.4a,b
17.7171.0a
20.4270.8b
3.96
0.03
J calls
The results of the nested ANOVAs showed that
there was significant variation among populations in
all the acoustic parameters of this call type
(Table III). Marmosets at Sacha and Amazoonico
emitted the shortest J calls. The highest number of
notes/sec and the lowest minimum frequency were in
J calls at La Hormiga. The highest maximum
frequency was in J calls at San Pablo. The narrowest
bandwidth was in J calls of Amazoonico. In the
discriminant function analysis, maximum frequency
and duration were the main variables in statistically
differentiating J calls from the five populations.
J calls were correctly classified to the population of
the caller in 78.6% of the cases, compared with the
expected 20% for each population (w216 ¼ 70:4,
Po0.0001). Using the cross-validation, leave-oneout method, classification was correct in 57.1% of the
cases (w216 ¼ 42:6, P 5 0.0003).
DISCUSSION
The structure of the Trills and J calls recorded
from the wild groups of pygmy marmosets is within
the range of variation recorded in captive colonies
[Elowson & Snowdon, 1994; Pola & Snowdon, 1975;
Snowdon, 1993; Snowdon & Cleveland, 1980].
Significant differences in at least one acoustic
variable of Trills and of J calls make possible
individual recognition between the focal animals in
each of the study groups in a similar manner as was
Max. freq (kHz)
Min. freq (kHz)
Bandwidth (kHz)
10.4270.2a
12.3670.3b
13.5870.4c
12.3970.2b
11.8270.1b
11.36
0.0007
7.970.2b,c
8.3370.1b
8.8970.3a
7.9270.1c
7.6270.1c
15.8
0.0002
2.4870.1a
4.0370.3b
4.6970.4b
4.4670.1b
4.2070.2b
6.16
0.008
reported in captive pygmy marmosets by Snowdon
and Cleveland [1980]. However, we did not find any
consistent differences in the whole data set that
could be attributable to sex only.
Trills and J calls had significantly different
structures in different populations. These differences exist despite the presence of some intrapopulation variability, as shown by the results of the nested
ANOVAs and in the discriminant function analyses.
Pair-wise comparisons for variables of the two
call types indicated that only La Hormiga and
Zancudococha populations did not differ from each
other except for notes/sec in J calls, but they differed
from all other populations (Tables II and III). Based
on the similar body sizes of the marmosets in all the
groups and populations, we believe that the potential
effect of body size on the frequency differences found
in the two call types among populations is negligible.
Recording distances were similar for all groups and
were within the range of minimum distortion for
Trills and J calls [de la Torre & Snowdon, 2002] so
we also feel confident that the observed differences
were not an artifact of sampling acoustic differences
among populations.
Some of the differences we found in Trills and
J calls could be related to differences in the acoustic
characteristics of the habitats. The ‘‘local adaptation
hypothesis’’ states that the acoustic characteristics of
the environment through which a signal is normally
transmitted have selectively influenced the form of a
signal to reduce distortion [Gish & Morton, 1981].
Am. J. Primatol.
338 / de la Torre and Snowdon
When we quantitatively evaluated the ambient noise
levels and the reverberation properties of the
habitats of the groups [de la Torre & Snowdon,
2002, de la Torre & Snowdon, in preparation] we
found that La Hormiga had the greatest ambient
noise and Amazoonico the least. Longer duration and
wider bandwidth may increase the detectability of
the calls because of temporal summation [Aubin &
Mathevon, 1995; Zwicker et al., 1957] and are
expected in calls from noisier habitats. Additionally,
the frequency of a call may be adapted to be above
the upper range of ambient noise [Snowdon &
Hodun, 1981]. Thus, calls from populations with a
lower range of ambient noise should be lower in
frequency than those from populations with a
broader range of ambient noise. However, although
the calls from Amazoonico did have the shortest
duration and smallest bandwidth as predicted, the
calls from La Hormiga were not the longest calls;
Trills, but not J calls, had the widest bandwidth and
there was no relationship across populations between ambient noise range and lower minimum
frequency of calls. Slower repetition rates (fewer
number of cycles or notes per second) and lower
frequencies reduce the distorting effects that sound
reverberation has on the transmission of signals with
fast repetition rates and high frequencies
[Brenowitz, 1986; Richards & Wiley, 1980; Wiley,
1991; Wiley & Richards, 1978]. Zancudococha,
Amazoonico and Sacha habitats had the greatest
reverberation compared with the other two sites;
however, although the calls from Zancudococha had
lowest repetition rates as predicted, Trills from
Amazoonico and Sacha had the highest repetition
rates and none of the calls from these three
populations had the lowest minimum frequency.
Thus, although some predictions about call structure
based on habitat acoustics were supported, several
others were not. It is possible that other habitat
acoustic variables, such as amplitude fluctuations
specific to one population or another, may have
influenced call structure [Brenowitz, 1986; Richards
& Wiley, 1980; Wiley & Richards, 1978]. However,
we currently have no data to evaluate this. The
presence of different predator assemblages in different populations may also drive changes in vocal
structure [Marler, 1955; Zimmermann et al., 2000]
but our observations do not suggest variation in
predators among populations.
Social influences may play a role in the differences in vocal structure. Studies with captive pygmy
marmosets and Wied’s black tufted-ear marmosets
C. kuhlii have provided evidence of plasticity in
acoustic structure that allow them to adjust their
vocalizations through subtle changes in frequency
and temporal parameters, in response to changes in
their social environment (e.g., the presence of a novel
companion) [Elowson & Snowdon, 1994; Rukstalis
et al., 2003; Snowdon & Elowson, 1999]. As Trills
Am. J. Primatol.
and J calls are emitted during interactions between
individuals under fluid environmental conditions, we
view vocal plasticity as a functional adaptation of the
marmosets to cope with their changing environment
where individuals may adapt their call structure to
match that of a new mate or social group [de la Torre
& Snowdon, 2002; Elowson & Snowdon, 1994;
Elowson et al., 1992]. Natural changes in the social
environment of wild pygmy marmoset groups include changes in group size and composition owing to
migrations (e.g., presence of novel companions) [de la
Torre et al., 2000; Soini, 1988]. These environmental
changes are not unique for pygmy marmosets so we
expect vocal plasticity to be reported in other
primates as more detailed studies are carried out
on multiple populations of the same species. Vocal
plasticity is considered a basis for learning processes
[Egnor & Hauser, 2004; Snowdon et al., 1997] known
to be related to dialects in some bird species [e.g.,
Marler, 1970; Nottebohm, 1972], whales [Noad et al.,
2000], bats [Boughman, 1998] and primates
[Crockford et al., 2004], and might account for some
of the population differences we have reported, but
this hypothesis is difficult to test in the field.
Interpopulation differences in the acoustic structure
of vocalizations in the five studied marmoset
populations are consistent with independent interpopulation differences found in exudate feeding
preferences in the same populations [Yépez et al.,
2005]. Genetic variation owing to river barriers
promoting separation between populations and the
low mobility of marmosets could account for some of
the observed differences but at present we have no
data to test this hypothesis.
This study provides the first evidence for
natural population variation in vocal structure in a
neotropical primate and one of the few demonstrations in the whole order. These variations can
be partially explained by differences in habitat
acoustics. Mechanisms of social learning and
genetic isolation of different populations may account for the remaining differences. Given the
documented interpopulation variability in vocal
production in this study coupled with the variability
in exudate feeding in pygmy marmosets [Yépez et al.,
2005], the loss of even one population may imply the
loss of a unique behavioral variation. This consideration needs to be taken into account while planning
future conservation actions in Ecuadorian Amazon
and in other areas of the distribution of pygmy
marmosets.
ACKNOWLEDGMENTS
All the research reported in this manuscript
adhered to the American Society of Primatologists
Principles for the ethical treatment of nonhuman
primates; all the research objectives and protocols
reported in the manuscript were reviewed and
Vocal Variability in Pygmy Marmosets / 339
approved by the Ecuadorian Ministry of the
Environment, which gave us the legal permit to
conduct the research. We are grateful for the support
from the following institutions: Wisconsin Regional
Primate Center (NCCR Grant P51 RR000167),
Ecolap - USFQ, Amazoonico - Selva Viva, Transturi
and Sacha Lodge. We thank Pablo Yépez, Delfı́n
Payaguaje, Alfredo Payaguaje, Monserrat Bejarano,
Lucı́a de la Torre, Daniel Payaguaje, Fernanda Tomaselli, Carolina Proaño, Hernán Castañeda, Santiago
Molina, Beatriz Romero and Margarita Brandt for their
help in the field work and Carolina Proaño for the
sound analyses of some vocalizations. We thank Karen
Strier for her suggestions on the data analyses and
Rosamunde E. A. Almond, Katherine A. Cronin,
Tatiana Humle and two anonymous reviewers for
critical feedback.
Appendix A
Individual differences in acoustic parameters
(mean7SE—on second line in each cell) of Trills
and J calls of individuals (adult male, M; adult female,
F) in the five populations (P, San Pablo; S, Sacha; A,
Amazoonico; H, Hormiga; Z, Zancudococha; numbers
following the letters indicate group number within
each population). Variables with significant differences between individuals in a group (unpaired ttests, Po0.05) are marked with a star ().
Trills
Group
Individual
Duration (sec)
Cycles/sec
Peak freq (kHz)
P1
M
P1
F
P2
M
P2
F
P3
M
P3
F
S1
M
S1
F
S2
M
S2
F
S3
M
S3
F
A1
M
A1
F
A2
M
A2
F
H1
M
H1
F
251
1
249
3
301
38
275
34
214
11
374
39
328
53
373
65
359
37
379
28
271
2
379
2
194
11
195
13
218
34
238
15
311
24
309
30
34.1
0.6
33.6
0.7
35.6
0.4
33
0.8
31.7
0.8
31.6
1.1
34
0.7
32.4
0.8
35.5
0.7
34.7
0.7
32.2
0.7
34.8
0.7
38.1
0.8
37.9
1.0
40.2
0.9
37.9
1.0
33.6
0.5
30.5
0.7
11.88
0.30
11.54
0.19
11.71
0.17
13.41
0.21
13.57
0.09
11.28
0.18
11.67
0.12
12.12
0.15
10.86
0.32
12.59
0.17
11.88
0.15
12.52
0.15
11.30
0.11
10.45
0.18
9.74
0.09
10.62
0.12
11.78
0.2
12.21
0.15
Min freq (kHz)
7.97
0.19
8.52
0.18
8.62
0.20
9.51
0.22
9.43
0.23
8.29
0.16
8.35
0.1
8.41
0.17
8.10
0.16
8.98
0.29
9.52
0.09
8.91
0.26
8.50
0.18
7.77
0.08
7.82
0.14
8.01
0.18
7.32
0.12
7.7
0.09
Bandwidth (kHz)
3.90
0.22
3.02
0.19
3.08
0.2
3.90
0.29
4.15
0.25
2.99
0.23
3.32
0.16
3.72
0.18
2.77
0.24
3.61
0.24
2.35
0.18
3.61
0.27
2.81
0.19
2.69
0.19
1.92
0.12
2.61
0.17
4.46
0.18
4.52
0.17
Am. J. Primatol.
340 / de la Torre and Snowdon
H2
M
H2
F
H3
M
H3
F
Z1
M
Z1
F
Z2
M
Z2
F
Z3
M
Z3
F
293
29
304
34
339
20
307
17
342
38
280
20
251
25
323
23
286
17
220
33.1
0.4
30.1
0.4
28.9
1.0
30.8
0.9
28.6
0.9
31.1
0.4
32.1
0.9
30.6
0.8
30.1
0.4
33.9
11.53
0.23
11.01
0.24
10.85
0.18
11.01
0.12
11.42
0.16
11.16
0.05
11.23
0.21
11.53
0.18
10.74
0.17
11.22
8.07
0.10
7.59
0.11
7.6
0.13
8.12
0.70
8.09
0.12
7.74
0.13
8.02
0.1
7.74
0.14
7.26
0.14
7.99
3.46
0.26
3.42
0.20
3.25
0.22
2.89
0.15
3.33
0.23
3.43
0.18
3.20
0.24
3.79
0.17
3.48
0.19
3.23
J Calls
Group
Individual
Duration (sec)
Notes/sec
Peak freq (kHz)
Min freq (kHz)
Bandwidth (kHz)
P1
M
P1
F
P2
M
P2
F
P3
M
SP3
F
S1
M
S1
F
S2
M
S2
F
S3
M
S3
F
A1
M
A1
F
A2
M
797
140
644
100
639
41
790
68
781
8
733
11
570
43
608
4
568
4
605
4
504
4
640
5
516
4
611
3
586
38
17.7
0.5
18.3
0.4
22.5
0.4
22.8
0.3
14.1
0.6
16.1
0.8
16.7
0.9
15.9
0.7
19.7
0.8
18.5
0.9
20
0.9
19.6
0.9
18
0.6
19.2
0.8
16.7
0.4
13.35
0.16
12.19
0.24
14.95
0.11
14.40
0.22
14.02
0.26
12.63
0.29
11.89
0.2
12.85
0.21
11.67
0.2
13.05
0.26
11.56
0.2
13.16
0.25
10.45
0.21
9.85
0.16
10.40
0.10
7.67
0.17
8.72
0.17
9.98
0.08
9.72
0.09
8.54
0.12
8.72
0.17
8.15
0.06
8.22
0.18
8.15
0.06
8.08
0.17
8.45
0.57
8.93
0.18
7.75
0.09
7.51
0.14
8.24
0.04
5.68
0.19
3.47
0.26
4.97
0.14
4.68
0.25
5.48
0.28
3.92
0.29
3.73
0.22
4.63
0.31
3.51
0.18
4.96
0.16
3.12
0.67
4.23
0.30
2.708
0.28
2.33
0.19
2.16
0.10
Am. J. Primatol.
Vocal Variability in Pygmy Marmosets / 341
A2
F
H1
M
H1
F
H2
M
H2
F
H3
M
H3
F
Z1
M
Z1
F
Z2
M
Z2
F
Z3
M
Z3
F
650
37
789
33
679
39
723
55
599
42
695
47
748
53
727
47
712
37
836
45
741
46
714
60
785
65
15.4
0.7
20.7
0.2
22
0.2
20.4
0.9
22.8
0.2
18.5
0.7
18.1
0.5
20.5
0.4
16.1
0.4
16.6
0.5
18.6
0.3
20
0.4
14.5
0.7
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