Abstract
Bioacoustical
signals play a decisive role in social relationships of animal kingdom,
including in chimpanzees and humans. In both species, the sound repertoires are
very large. Although chimpanzees and humans are closely related, comparative
studies on vocalizations are rare; the present study helps fill this gap in our
acoustic knowledge of these species. Thirty four cries (mean fundamental
frequency; Fo 1519 Hz, duration 272 ms) of three infant chimpanzees, and 94
cries (mean Fo 1116 Hz, duration 383 ms) of seven adult chimpanzees, were collected. Acoustic analyses of these
sounds were compared with analyses of 98 cries (mean Fo 455 Hz, duration 821
ms) from 15 human infants and 46 cries (mean Fo 489 Hz, duration 793 ms) of
eight human adult women. However, the cries of both species show the typical
character of mammals, namely, a high number of harmonics, rising-falling
melodies, and varied fundamental frequency structures. Causes for the clear
differences in fundamental frequency and duration across species are discussed
in relation to both environmental and phylogenetic factors.
Introduction
The acoustic
signals inform the perceivers about the needs and possible dangers faced by the
sender (Cheney, & Seyfarth, 1990; Darwin, 1884; Griffin, 1991; Hauser,
1996, 2000, Kojima, 2003, Marler, 1955; Marler, & Hamilton, 1972; Newman;
& Symmes, 1982; Owings, & Morton, 1998; Rothgänger, 1999; Seyfarth,
& Cheney, 2003; Tembrock, 1996, Todt, 1988), but also about body size
(Gouzoules, & Gouzoules, 1990), emotional state (Scherer, 1982, 1985, 1992;
Scherer, & Kappas, 1988), agressive and fearful individual behaviour
(Moton, 1977), attractive female (Leong, Ortolani, Graham, & Savage, 2003)
or the presence of predator (Bergstrom, & Lachmann, 2001; Seyfarth, &
Cheney, 1986).
Crying, or
screaming, is generally viewed as a distress signals with an aversive state
that functions demand to care and across a distance (Ainsworth, 1977; Bowlby,
1972; Illingworth, 1980; Todt, 1988). This functional meaning of crying is the
same in both chimpanzees and humans and allows a comparison of the sounds
across species (Fitch, 2000; Kohts, 2002; Locke, & Hauser, 1999; Newman,
1985; Nishimura, 2005; Seyfarth, & Cheney, 2003).
In the early
20. century lot of studies about acoustics have dealt with the human languages
(Bates, et al. 1994; Brunner, 1964, 1987; Bühler, 1965; Chomsky, 1965; Fant,
1970; Fernald 1992; Griffin, 1991; Herzka, 1967; Irwin, 1953; Jakobson, 1941;
Jakobson, & Waugh, 1986; Kuhl, 2000; Lenneberg, 1967; Locke, 1996; Mowrer,
1960; Oller, 1978; Oller and Eilers, 1992; Piaget, 1972; de Saussure 1931,
Skinner, 1957) and about the infant cry by Scandinavian and American groups in
the 60th (Barr, 1998; Barr, et al. 2000; Bernal, 1972; Brazelton,
1962; Fisichelli, & Karelitz, 1963; Flatau, & Gutzmann, 1906; Formby,
1967; Fort, & Manfredi, 1998; Furlow 1997; Green, et al. 1998, 2000;
Gustafson, et al 1984, 1994, 2000; Hirschberg, & Szende, 1985; Lester,
1984; Lester, & Boukydis, 1985; Lenneberg, 1967; Lind, 1965; Michelsson,
1971; Michelsson, et al. 2002; Murry, & Murry, 1980; Ostwald, 1972;
Papoušek, 1994; Rothgänger, 1999, 2003, Scherer, 1982; Sedlàkovà, 1967;
Sherman, M. 1927; Shimura, M. A. & Yamanoucho, M. D. 1992; Sirviö, &
Michelsson, 1976; Soltis, 2004; Stark, 1981; Thodèn, & Koivisto, 1980;
Wasz-Höckert, et al. 1968; Wilden, & Baken, 1978; Wolff, 1969; Zeifman,
2001, 2004; Zeskind, 1985). The cries of human infant have been differentiated
in terms of function into birth, hunger (discomfort cry, spontaneous cry or
basic cry), rage, pain, frustration cries and cries of joy (Michelsson, 1971;
Rothgänger, 1999; Wasz-Höckert, et al. 1968; Wolff, 1969). In terms of
structure, human cries have been labeled as phonated (basic cry; voiced or
sound-like cry), turbulent (cry with voiceless part) and hyperphonated (cry
with shift or break) (Lind,1965; Rothgänger, 1999; Sedlàckovà, 1967). Although
most studies suggest that there are perceptual differences between pain and
hunger cries, investigations by Sherman (1927) and Wasz-Höckert et al. (1968)
did not show clear results. Mothers and nurses, as well as people experienced
in child care, recognized pain and hunger cries better than inexperienced
persons. For this reason, and also because of large differences in cry
characteristics (Papoušek, 1994), some authors suggest that infant crying only
expresses discomfort and displeasure (e.g., Bernal, 1972). New examinations of
hunger and pain cries suggest that difference especially exist in jitter
(Rothgänger, et al. 1990, 1993). In longer series of cry sounds, changes in the
cry’s structure may represent the degree of the baby’s arousal or excitement
(Green, et. al. 1998, 2000, Gustafson et al. 1984, 1994, 2000). Little is known
about crying in human adults (Peter, et al. 2001; van Tilburg, et al. 2002;
Vingerhoets, & Cornelius, 2001); however, adult humans do scream when in
pain or distress, both during sporting events and during cultural rituals
(Rothgänger, 1999, 2003).
Then the time
has come for working of animal vocalizations enclosed the calls of nonhuman
primates (Bermejo, & Omedes, 1999; Boesch, 1991, 2003; Brown, et al. 1995;
Cheney, & Seyfarth, 1988, 1990; Fischer, 2004; Fischer, &
Hammerschmidt, 2002; Fischer, et al. 2001; Fitch, 1997, 2000, 2000; Fitch, et
al 2002; Geissmann, & Nijman, 2006; Ghazanfar, et al. 2002; Goodall, 1986,
1991; Gouzoules, & Gouzoules, 1990, 2002, 2002; Gros-Louis, 2004; Hauser,
1993, 1996, 1998, 2000; Hauser, & Akre, 2001; Hauser, et al. 1993; van
Hooff, 1976; Mitani, 1996; Newman, 1985; Nikitopoulos, et al. 2004; Owren,
& Rendall, 2001; Owren, et al. 1993; Ploog, 1972; Prell, et al. 2002;
Seyfarth, & Cheney, 2003; Sommer, & Ammann, K. 1998; Symmes, &
Biben 1992; Tembrock, 1996; Todt, 1988; Todt, et al. 1995; de Waal, 1988, 1997;
Zimmermann, et al 2000). In 2000 Hauser has nevertheless written: "This
section shows how little we know about the units of organization within animal
vocal repertoires, and how such lack of information constrains our ability to
tackle the problem of syntactic structure".
Chimpanzees have a rich repertoire of
vocalizations that are used during the interaction of adults and infants as
well as between adults (Arcadi, 1996, 2000; Boesch, 1991; Clark, 1993; Clark,
& Wrangham, 1993, 1994; Crockford, & Boesch, 2003; Crockford, et al
2004; Goodall, 1986, 1991; Hauser, et al., 1993; Izumi, & Kojima, 2004;
Kajikawa, & Hasegawa, 2000; Kojima, et al., 2003; Marler, 1976; Marler,
& Hobbett, 1975; Marler, & Tenaza, 1977; Matsusaka, 2004; Mitani, &
Gros-Louis, 1995; Mitani, et al., 1992, 1994, 1996, 1999; Rothgänger, 2005; de
Waal, 1988, 1997). Among chimpanzees, cries occur in two situations described
by Goodall (1986) as intraparty calls and distance calls. Within a group, a
wide variety of sounds have social functions; these sounds have been described
as weeping, whimpering and screaming (victim screams, tantrum screams,
copulation screams), shouting, barking (barks, waa barks), pant hoot, hoo
sounds, food aaa-calls, huu sounds, laughing, gasping and grunting (soft
grunts, extended grunts, food grunts). The distance calls signal the existence
of danger or food; these are described as pant hoots, screams, cries, and wraa
cries (Marler, & Tenaza, 1977). At first Kojima (2003) and colleagues have
studied the ontogeny of chimpanzee screams, squeaks and whimpers related to
aversive emotion. They have found mean fundamental frequency (Fo) from 1664 Hz
in the first week developed to 844 Hz in the 17th week. Current
examinations about calls of chimpanzee results in dialects (Mitani, et al.
1992), identification of vocalizer (Kojima, 2003; Kojima, et al. 2003), crossmodal
representation of their vocalizations (Izumi, & Kojima, 2004), positive
feedback to the play partner (Matsusaka, 2004) and different barks into
different contexts (Crockford, & Boesch, 2003) like other nonhuman primates
(Cheney, & Seyfarth, 1990, Hauser, 1996).
The
vocalizations of chimpanzees and humans can be also differentiated because they
have different functions in different situations. Furthermore, the calls of
these two species appear to be strongly influenced by emotion (Green, &
Gustafson, 2000; Marler, & Tenaza, 1977; Rothgänger, 1995, 1999; van
Tilburg, et al. 2002). Despite the very close relations between these aspects
of chimpanzees’ and humans’ vocalizations, there are not any comparative
acoustic studies of crying in both species and just a few between chimpanzee,
bonobo and gorilla (Marler, & Tenaza, 1977; Mitani, 1996; Newman, &
Symmes, 1982; de Waal, 1988).
The aim of the
present study is to compare the cries of human infants and adults with the
cries of chimpanzee young and adults. Such results could contribute to our
understanding of animal behaviour and provide knowledges of ecology of apes
involved body size or habitat dependence of bioacoustics. In addition it is a
contribution to understanding of the possibly origins the evolution of speech
and language in humans.
Methods
Chimpanzee and
human calls were recorded using a high quality microphone (Sennheiser MKH 70
P48) and a cassette tape recorder (Sony WM-D6C). Calls were analyzed on a PC
equipped with a DSP33 signal processing card. This equipment enabled high
resolution fundamental frequency analysis has been described by Lüdge &
Gips (1989), Lüdge & Rothgänger (1990) and Rothgänger (1999) as well as the
determination of sound length, formant frequencies, and spectrographic evaluation
of the recordings (fundamental frequency shift, double harmonic break, vibrato,
“voiced” and “voiceless part”; defined by Sirviö, & Michelsson, 1976,
Rothgänger, 1999, as well as by Wasz-Höckert, et al. 1968). In addition, the
standard intonation was calculated through a separate analysis of the
fundamental frequency curve (Rothgänger, 1999, 2003). Each call was divided
into 10 equal-duration portions, separated by cursors (Fig. 1). The standard
intonation was calculated as the mean fundamental frequency of each of these
segments.
The
vocalizations of chimpanzees were recorded at the Berlin Zoo (Germany) and at
Burgers´ Zoo Arnhem (Netherlands). There were 94 cries of seven adults females
(65 cries) and three males (29 cries) between the ages of 11 and 40 years.
Cries were recorded in aggressive and pain contexts during beating and biteing,
including reactions to an attack or to social excitement (e.g. dispute over
food or dominance relationships). Thirty four cries of three chimpanzee infants
(females) were recorded at a mean age of 3 months; cries were recorded when
infants were hungry. They were in contact with their mothers. The living
conditions of chimpanzees have been described by van Hooff (1973).
Among humans,
only hunger cries were collected 30 minutes before feeding from 15 infants (98
cries) born between 1983 and 1986. Infants (7 males, 8 females) were 3 to 5
days of age. Their mean Apgar score at 5 min. was 9.5, birth weight was 3613 g,
and body length was 52.0 cm. The Apgar scores evaluate the newborns in turn 5
features with 0 – 2 points (skin colour, heart rate, breathing, reflexes,
muscle tension; 0 without; 2 optimal). Infants were born without complications
at the Charité-Universitätsmedizin Berlin have been described by Grauel, et al.
(1990). In addition, 46 different cries were analyzed from 8 women during the
onset of labour at the Charité. The mean age of the women was 26.5 years; they
were German and from the middle class. The cries of women were recorded if they
be in beds and were in labour pains. The
data of language was taken on study of laugther and speech from 10 women and 10
men German and 10 women and 10 men Italian students has been described by
Rothgänger, et al. 1998.
Invesitgations
of cries in relation to sex in chimpamnzees and humans were renounced because
previous unpublished analyses show no signifcant differences (also human babies
by Gardosik and Ross, 1980; Murray et al.,
1977).
Standard
parametric and non-parametric statistical analyses were used and significance
values were set at p=0,05. T-tests were used to compare using the tables of
Clauss & Ebbner (1968). Reggression analyses were used to ANOVA.
Results
The acoustic
structure of both chimpanzee and human cries appears to be characteristic of
mammals (Riede, et al. 2004)(Figures 2 & 3). The similarities across
species include the wide-band structure of signal, a number of harmonics of the
fundamental frequency, a rising-falling melody, a rising-falling volume
(characteristic of siren signals), and the existence of special parameters like
shift, double harmonic break (Fig. 2b & c and 3b & c) and voiceless
portions (Fitch, et al. 2002; Rothgänger, 1999; Sirviö, & Michelsson, 1978;
Wasz-Höckert, et al. 1968), especially in the context of excitement and pain.
The acoustic
analysis of chimpanzee cries shows a mean fundamental frequency of 1116.1 Hz,
with a mean duration of 382.6 ms in adults. Comparable values for chimpanzee
infants were 1519.3 Hz and 272.3 ms. Fundamental frequency and duration
differences were significant, P = 0.001 and
P = 0.001, N = 128, respectively.
Adult human
cries had a mean fundamental frequency of 489.2 Hz and a mean duration of 792.8
ms. Human infant cries had a mean fundamental frequency of 454.5 Hz, and a mean
duration of 820.5 ms (Fig. 4). These mean fundamental frequency differences
were statistically significant, P = 0.001, and the mean duration were not, P =
ns., N = 144, respectively. The mean fundamental frequency and the mean
duration of all cries of chimpanzees and humans were significantly different, P
= 0.001, and P = 0.001; N = 271, respectively.
The mean
fundamental frequency of language were signifikant different between men and
women (German and Italian men Fo 123,0 Hz, N = 190; German and Italian women Fo
214,0 Hz, N = 187; P= 0,001).
The species
differences were pronounced, both in the range of fundamental frequency and in
the proportion of fundamental frequency to duration of the cry. There was a
basic rising-falling melody in both species, but the ranges of the fundamental
frequency were very different. Infant chimpanzees had a mean melody range from
879.1 to 1684.9 Hz, and adult chimpanzees ranged from 835.1 to 1496.7 Hz. On
the other hand, the cries of infant humans had a fundamental frequency range of
only 342.5 to 546.9 Hz, whereas adult humans ranged from 313.0 to 689.0 Hz.
Chimpanzees tended to increase their fundamental frequency range in the context
of excitement. In addition, men an women humans used a mean melody range from
121 to 217 Hz for speech, but with an important sexual dimorphism as well as a
constant melody and little intonation (Fig. 5).
Placing all
four groups of cries on the same scatterplot (Fig. 6), the fundamental
frequency shows a significant decrease across the groups of infant chimpanzee,
adult chimpanzee, infant human and adult human (regression r = -0.8887, P =
0.01, N = 271). However, the cry duration shows a significant increase across
the same series of groups (regression r = +0.8882, P = 0.01, N = 271). A
comparison of the two regression lines shows a high significant difference
(regression r = -0.58009, P = 0.01, N = 542).
Discussion
In primates,
fundamental frequency is related to weight (Gouzoules, & Gouzoules, 1990).
Hauser (1996) has written "Thus large species such as gorillas (Gorilla gorilla) und chimpanzees (Pan troglodytes) tend to produce calls
with relatively low fundamental frequencies, whereas small species such as the
marmosets and tamarins (Callitrichidae)
tend to produce calls with relatively high fundamental frequencies." The
relation between fundamental frequency and weight was affirmed in the present
study of human and chimpanzee weights. Adult humans, who generally weigh
between 58.200 and 66.200g (von Harnack, & Heimann, 1990; Sommer, 1990),
had a significantly lower cry fundamental frequency (489.2 Hz) than
chimpanzees, who had average weights of 35.000 to 45.000 g and a mean
fundamental frequency of 1116,1 Hz. Further, this relation of weight to
fundamental frequency was shown in the offspring of both species. Human
newborns generally weigh between 3.400 and 3.500 g (Kyank, et al. 1981; Sommer,
1990), and their fundamental frequency of 454.5 Hz was significantly lower than
that of chimpanzee infants (1519.3 Hz), whose weight averages 1.800 g.
In the cries of
human adults and infants, there was significant difference in fundamental
frequencies (infant: hunger cry 454.5 Hz, [pain cry 482,6 Hz Rothgänger 2003],
adult: 489.2 Hz) but in revers order. The fundamental frequency of human
infants should be clearly higher than that of adults because of their much
lower weight. Of course, investigation of the weight and fundamental frequency
relation in only two species of primates could be misleading, and further
studies of other primates are necessary. Weight maybe less important in
investigations of the different fundamental frequencies of primates than the
ecological context, phylogenetic relations, and ontogenetic comparisons (Brown,
& Waser, 1988; Gouzoules, & Gouzoules, 1990, 2000; Rothgänger, &
Rothgänger, 2001, 2002).
According to
Kortland (personal communication), there exist two different filter conditions
in the rainforest and the savannah that affect sound propagation. Crying with
lot of harmonics is a wide-band signal. It has a rising-falling melody and high
amplitude, which helps it travel across wide distances (Goodall, 1986; Leong,
et al. 2003; Marler, 1956; Papoušek, 1994). Therefore, it has been called a
distress signal and will be decrease during attachment behaviour of parents
(Ainsworth, 1977; Bowlby, 1972; Todt, 1988). Ostwald (1972) has written that
the listener has the choice to leave or soothing the baby. Consequently, the
relative low-frequency cry of human and the relative high-frequent cry of
chimpanzee perhaps also reflect adaptations to the ecologies of the species
(Jilka, & Leisler, 1974; Perla, & Stobodchikoff, 2002; Wasserman, 1979;
Waser, & Brown, 1984; Wass, 1987).
The human
ancestor occupied first open savannah landscapes (Boesch, 2003; Fouts, &
Mills, 2000; Leakey, & Lewin, 1998; Storch, et al. 2001). During different
daily activities, the infants were most likely set down temporarily (Newman,
1985). If the infant cries during threat or other dangers, these were heard
over long distances because they had energy at relatively wide-band frequencies.
However, the chimpanzee, which lived (and still lives) in environments ranging
from the closed rainforest to the open savannah (Boesch, &
Boesch-Achermann, 2000), exhibits a markedly higher fundamental frequency than
humans. They have better adapted in rainforest and very close relationship to
their mother (Goodall, 1986; Boesch, & Boesch-Achermann, 2000; Owings,
& Morton, 1998).
In concert with
the ecological context, phylogenesis played a role in the acoustics of cries.
The individual hominoids as well the human and chimpanzee, descended from a
shared ancestor. This radiation stands beside other factors in the evolution
and differentiation of cry sounds, and all factors together may have been the
cause of different patterns of cry acoustics in morphologically very similar
species. The present results support this assumption. The extreme differences
of mean fundamental frequencies and the standard melodies of the human and
chimpanzee cries conflicted with their small differences of weights. If we
include the cries of bonobos (Pan
paniscus) in our consideration (Bermejo, & Omedes, 1999; de Waal, 1988)
the conclusions are reinforced. In this species, who live predominantly in
closed rainforest, the fundamental frequency of the cries is 1.600 to 3.500 Hz,
about one octave higher than in chimpanzees. Tembrock (1996) suggested that the
bonobo developed the high frequency cries to maintain a acoustic distance from
the chimpanzee. The general consensus is that bonobo evolved in isolation from
both chimpanzees and gorillas south of the Congo River, filling a unique
ecological niche with only limited feeding competition (Kano, 1992; White,
1992).
Of course, the
adaptations of the ancestral humans to the open landscape impacted the
evolution of the speech, also. Low fundamental frequencies permitted more or
less continuous communication (Mathelisch, & Friedrich, 1995) because the
physiological demands are not great. The parallel fall of the fundamental
frequency and rise in the duration of the cry from the infant to the adult
chimpanzee and from the infant to the adult human are consistent with these
ideas. Speech is the most important mode of communication in humans, and has
allowed to develop the human culture (Fouts, & Mills, 2000; Leakey, &
Lewin, 1998; Lorenz, 1988; Kojima, 2003). Its phonetic characteristics are
affected by many factors, including sex of speaker, emotional state of the
speaker (Rothgänger, 1995; Scherer, 1985, 1992; Scherer, & Kappas, 1988),
and the context of the speaker (Reissland, & Snow, 1996; Shimura, &
Yamanoucho, 1992). In human speech, the fundamental frequency of men contains
about 123 Hz, compared with about 214 Hz in women (Rothgänger, 1999, 2003;
Rothgänger, et al. 1998). Because fundamental frequency is controlled by
anatomical-physiological parameters, such the length and the tension of the
vocal fold, fundamental frequency tends to be a specific characteristic of
individuals. The development of anatomic propotions of head led to changes in
bioacoustics of all species with the centric of head, reduction of prognathy
and the changes of vocal tract on humans (Fitch, 2000; Lieberman, et al. 1972;
Nishimura, 2005). But the fundamental frequency is very low compared to other
hominoids (Fant, 1970, Golub, & Corwin, 1985; Lenneberg, 1972; Lester,
1984; Lieberman, & Blumstein, 1988; Wendler, et al. 1996) and have got
favourable features for a long communication procedure (Mathelitsch, &
Friedrich, 1995) and a high resolution of frequency. The difference threshold
of frequency were about 10 – 15 Hz
between 0.5 kHz and 2 Hz, but rose to 35-40 Hz at 4 kHz (Kojima, 2003).
In conclusion,
it is clear that individual characteristics and typical weight play crucial
roles in the formation of the fundamental frequency of cries across humans and
chimpanzees. Also, however, the ecology of the two environments, and the
phylogeny of the two species, are important determinants of the cry
characteristics of infants and adults as well as speech of human. As results we
have got a human speech with lowest fundamental frequency in language, that was
also separated of crying. Now, humans have got tow separate acoustic
communication systems (Rothgänger, 2003)
Legends
Figure 1 Method
to standardise the function of the fundamental frequency (standard melody) of
human cry. The division of the duration of a signal into 10 parts equal in size
(left part) and determination of the mean fundamental frequency of all
separated sections (right part). Middle part shows the mean Fo of all 4 ms
parts of the cry and duration.
C1: Cursor one,
position 28 ms; f = 351 Hz fundamental frequency on cursor position.
Figure 2
Sonagram (left part) and the mean value as well as the high-resolution
fundamental frequency (right part) of three chimpanzee cries. The mean
fundamental frequency and the part of double harmonic structure increase with
the rising excitement.
Figure 3
Sonagram (left part) and the mean value as well as the high-resolution
fundamental frequency (right part) of three human cries. The mean fundamental
frequency and the part of double harmonic structure increase with the rising
excitement.
Figure 4
Comparison of the mean fundamental frequency (1-4) and mean duration (5-8) of
the infants (1, 5) and adults chimpanzee cries (2, 6) as well as infants (3, 7)
and adult human cries (4, 8).
Figure 5
Comparison of the standardised melody curve (standard melody) of the infant
(white triangles) and adult chimpanzee cry (black triangles), of the infant
(white diamonds) and adult human cry (black diamonds) as well as of the woman
(white circles) and man human language (black circles).
Figure 6
Correlation of fundamental frequency (black diamonds) and duration (white
circles) of all infant (1. part) and adult (2. part) chimpanzee cries as well
as of all infant (3. part) and adult (4. part) human cries. The constant line
shows the fundamental frequency gradient (r = -0.8887, P = 0.001, N = 271) and
the broken line the duration gradient (r = +0.8882, P = 0.001, N = 271).
