The adult male Diana monkeys (Cercopithecus diana) produce predator-specific alarm calls in response to two of their predators, the crowned eagles and the leopards. The acoustic structure of these alarm calls is remarkable for a number of theoretical and empirical reasons. First, although pulsed phonation has been described in a variety of mammalian vocalizations, very little is known about the underlying production mechanism. Second, Diana monkey alarm calls are based almost exclusively on this vocal production mechanism to an extent that has never been documented in mammalian vocal behavior. Finally, the Diana monkeys’ pulsed phonation strongly resembles the pulse register in human speech, where fundamental frequency is mainly controlled by subglottal pressure. Here, we report the results of a detailed acoustic analysis to investigate the production mechanism of Diana monkey alarm calls. Within calls, we found a positive correlation between the fundamental frequency and the pulse amplitude, suggesting that both humans and monkeys control fundamental frequency by subglottal pressure. While in humans pulsed phonation is usually considered pathological or artificial, male Diana monkeys rely exclusively on pulsed phonation, suggesting a functional adaptation. Moreover, we were unable to document any nonlinear phenomena, despite the fact that they occur frequently in the vocal repertoire of humans and nonhumans, further suggesting that the very robust Diana monkey pulse production mechanism has evolved for a particular functional purpose. We discuss the implications of these findings for the structural evolution of Diana monkey alarm calls and suggest that the restricted variability in fundamental frequency and robustness of the source signal gave rise to the formant patterns observed in Diana monkey alarm calls, used to convey predator information.

1.
Abel
,
S. M.
(
1972
). “
Discrimination of temporal gaps
,”
J. Acoust. Soc. Am.
52
,
519
524
.
2.
Allen
,
E.
, and
Hollien
,
H.
(
1973
). “
A laminagraphic study of pulse (vocal fry) phonation
,”
Folia Phoniatr.
25
,
241
250
.
3.
Au, W. W. L. (1993). The Sonar of the Dolphin (Springer Verlag, New York).
4.
Berry
,
D. A.
(
2001
). “
Mechanisms of modal and nonmodal phonation
,”
J. Phonetics
29
,
431
450
.
5.
Berry
,
D. A.
,
Herzel
,
H.
,
Titze
,
I. R.
, and
Krischer
,
K.
(
1994
). “
Interpretations of biomechanical simulations of normal and chaotic vocal fold oscillations with empirical eigenfunctions
,”
J. Acoust. Soc. Am.
95
,
3595
3604
.
6.
Blomgren
,
M.
,
Chen
,
Y.
,
Ng
,
M. L.
, and
Gilbert
,
H. R.
(
1998
). “
Acoustic, aerodynamic, physiologic, and perceptual properties of modal and vocal fry registers
,”
J. Acoust. Soc. Am.
103
,
2649
2658
.
7.
Bradbury, J. W., and Vehrencamp, S. L. (1998). Principles of Animal Communication (Sinauer, Sunderland).
8.
Buus, S., and Florentine, M. (1985). “Gap detection in normal and impaired listeners: The effect of level and frequency,” in Time Resolution in Auditory Systems, edited by A. Michelsen (Springer, New York).
9.
Fant, G. (1960). Acoustic Theory of Speech Production (Mouton, The Hague).
10.
Fischer
,
J.
,
Hammerschmidt
,
K.
,
Cheney
,
D. L.
, and
Seyfarth
,
R. M.
(
2002
). “
Acoustic features of male baboon loud calls: influences of context, age, and individuality
,”
J. Acoust. Soc. Am.
111
,
1465
1474
.
11.
Fuks
,
L.
,
Hammarberg
,
B.
, and
Sundberg
,
J.
(1998). “A self-sustained vocal-ventricular phonation mode: acoustical, aerodynamic and glottographic evidences,” TMH-QPRS 3, 49–59.
12.
Gerratt
,
B.
, and
Kreiman
,
J.
(
2001
). “
Toward a taxonomy of nonmodal phonation
,”
J. Phonetics
29
,
365
381
.
13.
Gramming, P. (1988). “The phonetogram: An experimental and clinical study,” Malmoe Sweden, Dept. Otolaryngology, Univ. of Lund.
14.
Grimm
,
R. J.
(1967). “Catalogue of sounds of the pigtailed macaque (Macaca nemestrina),” J. Zool. Lond. 152, 361–373.
15.
Henton, C., and Bladon, A. (1988). “Creak as a sociophonetic marker,” in Language, Speech, and Mind: Studies in Honour of Victoria A. Fromkin, edited by L. M. Hyman and C. N. Li (Routledge, London), pp. 3–29.
16.
Herzel
,
H.
,
Berry
,
D.
,
Titze
,
I. R.
, and
Saleh
,
S.
(
1994
). “
Analysis of vocal disorders with methods from nonlinear dynamics
,”
J. Speech Hear. Res.
37
,
1008
1019
.
17.
Hollien
,
H.
(
1974
). “
On vocal registers
,”
J. Phonetics
2
,
125
143
.
18.
Hollien
,
H.
, and
Michel
,
J.
(
1968
). “
Vocal fry as a phonational register
,”
J. Speech Hear. Res.
11
,
600
604
.
19.
Hollien
,
H.
,
Damsté
,
H.
, and
Murry
,
T.
(
1969
). “
Vocal fold length during vocal fry phonation
,”
Folia Phoniatr.
21
,
257
265
.
20.
Hollien
,
H.
,
Girard
,
G. T.
, and
Coleman
,
R. F.
(
1977
). “
Vocal fold vibratory patterns of pulse register phonation
,”
Folia Phoniatr.
29
,
200
205
. (1972).
21.
Ishizaka, K., and Flanagan, J. L. (1972). “
Synthesis of voiced sounds from a two-mass model of the vocal cords,” Bell Syst. Tech. J. 51, 1233–1268.
22.
Lindestad
,
P.
,
Soedersten
,
M.
,
Merker
,
B.
, and
Granqvist
,
S.
(
2001
). “
Voice source characteristics in Mongolian ‘throat singing’ studied with high-speed imaging technique, acoustic spectra, and inverse filtering
,”
J. Voice
15
,
78
85
.
23.
Mergell
,
P.
,
Fitch
,
W. T.
, and
Herzel
,
H.
(
1999
). “
Modeling the role of non-human vocal membranes in phonation
,”
J. Acoust. Soc. Am.
105
,
2020
2028
.
24.
Miller
,
D. G.
,
Sulter
,
A. M.
,
Schutte
,
H. K.
, and
Wolf
,
R. F.
(
1997
). “
Comparison of vocal tract formants in singing and nonperiodic phonation
,”
J. Voice
11
,
1
11
.
25.
Morton
,
E. S.
(
1977
). “
On the occurrence and significance of motivation—structural rules in some bird and mammal sounds
,”
Am. Nat.
111
,
855
869
.
26.
Murry
,
T.
, and
Brown
,
W. S.
, Jr.
(
1971
). “
Subglottal air pressure during two types of vocal activity: vocal fry and modal phonation
,”
Folia Phoniatr.
23
,
440
449
.
27.
Neubauer
,
J.
,
Mergell
,
P.
,
Eysholdt
,
U.
, and
Herzel
,
H.
(
2001
). “
Spatio-temporal analysis of irregular vocal fold oscillations: biphonation due to desynchronization of spatial modes
,”
J. Acoust. Soc. Am.
110
,
3179
3192
.
28.
Owren
,
M. J.
(
1990
). “
Acoustic classification of alarm calls by veret monkeys (Cercopithecus aethiops)
,”
J. Acoust. Soc. Am.
101
,
2951
2963
.
29.
Owren, M., and Linker, C. D. (1995). “Some analysis techniques that may be useful to acoustic primatologists,” in Current Topics in Primate Vocal Communication, edited by E. Zimmermann, J. Newman, and U. Jürgens (Plenum, New York), pp. 1–27.
30.
Peters
,
G.
(1981). “Das Schnurren der Katzen,” Säugetierkundl. Mitteilungen 29, 30–37.
31.
Peters
,
G.
, and
Tonkin-Leyhausen
,
B. A.
(1999). “Evolution of communication signals of mammals: friendly close range vocalizations in felidae (Carnivora),” J. Mammalian Evol. 6, 129–159.
32.
Ploog, D., Hupfer, K., Jürgens, U., and Newman, J. D. (1975). “Neuroethological studies of vocalization in squirrel monkeys with special reference to genetic differences of calling in two subspecies,” in Growth and Development, edited by M. A. B. Brazier (Raven, New York).
33.
Richman
,
B.
(
1976
). “
Some vocal distinctive features used by gelada monkeys
,”
J. Acoust. Soc. Am.
60
,
718
724
.
34.
Riede, T., and Zuberbühler, K. (in press). “The relationship between acoustic structure and semantic information in Diana monkey alarm calls.” J. Acoust. Soc. Am.
35.
Riede
,
T.
,
Wilden
,
I.
, and
Tembrock
,
G.
(1997). “Subharmonics, biphonations, and frequency jumps—common components of mammalian vocalization or indicators for disorders,” Z. Säugetierkunde 62, 198–203.
36.
Riede
,
T.
,
Herzel
,
H.
,
Mehwald
,
D.
,
Seidner
,
W.
,
Trumler
,
E.
,
Böhme
,
G.
, and
Tembrock
,
G.
(
2000
). “
Nonlinear phenomena in the natural howling of a dog-wolf mix
,”
J. Acoust. Soc. Am.
108
,
1435
1442
.
37.
Schoen Ybarra
,
M. A.
(
1986
). “
Loud calls of adult male red howling monkeys (Alouatta seniculus)
,”
Folia Primatol (Basel)
47
,
204
216
.
38.
Smith
,
M.
(1980). “Behavior of the Koala, Phascolarctos cinereus (Goldfuss), in captivity, III. Vocalizations,” Aust. Wildl. Res. 7, 13–34.
39.
Steinecke
,
I.
, and
Herzel
,
H.
(
1995
). “
Bifurcations in an asymmetric vocal fold model
,”
J. Acoust. Soc. Am.
97
,
1874
1884
.
40.
Svec
,
J. G.
,
Schutte
,
H. K.
, and
Miller
,
D. G.
(
1999
). “
On pitch jumps between chest and falsetto registers in voice: Data from living and excised human larynges
,”
J. Acoust. Soc. Am.
106
,
1523
1531
.
41.
Tembrock, G. (1996). Akustische Kommunikation der Säugetiere. Wissenschaftl (Buchgesell, Darmstadt).
42.
Tigges
,
M.
,
Mergell
,
P.
,
Herzel
,
H.
,
Wittenberg
,
T.
, and
Eysholdt
,
U.
(
1997
). “
Observation and modeling of glottal biphonation
,”
Acustica
83
,
707
714
.
43.
Titze
,
I. R.
(
1989
). “
On relation between subglottal pressure and fundamental frequency in phonation
,”
J. Acoust. Soc. Am.
85
,
901
906
.
44.
Titze, I. R. (1991). “Mechanisms underlying the control of fundamental frequency,” in Vocal Fold Physiology: Acoustic, Perceptual and Physiological Aspects of Voice Mechanisms, edited by J. Gauffin and B. Hammarberg (Singular, San Diego), pp. 129–138.
45.
Titze, I. R. (1994). Principles of Voice Production (Prentice Hall, Englewood Cliffs, NJ).
46.
van den Berg
,
J.
(
1958
). “
Myoelastic-aerodynamic theory of voice production
,”
J. Speech Hear. Res.
1
,
227
244
.
47.
Wilden
,
I.
,
Herzel
,
H.
,
Peters
,
G.
, and
Tembrock
,
G.
(
1998
). “
Subharmonics, biphonation, and deterministic chaos in mammal vocalization
,”
Bioacoustics
9
,
171
196
.
48.
Winter
,
P.
(
1969
). “
Dialects in squirrel monkeys: vocalization of the roman arch type
,”
Folia Primatol (Basel)
10
,
216
229
.
49.
Zuberbühler
,
K.
(
2000a
). “
Causal knowledge of predators’ behavior in wild Diana monkeys
,”
Anim. Behav.
59
,
209
220
.
50.
Zuberbühler
,
K.
(
2000b
). “
Referential labeling in Diana monkeys
,”
Anim. Behav.
59
,
917
927
.
51.
Zuberbühler, K. (2003). “The effects of natural and sexual selection on the evolution of guenon loud calls,” in The Guenons, edited by M. Glenn and M. Cords (Plenum, New York).
52.
Zuberbühler
,
K.
,
Cheney
,
D. L.
, and
Seyfarth
,
R. M.
(
1999
). “
Conceptual semantics in a non-human primate
,”
J. Comp. Psychol.
113
,
33
42
.
53.
Zuberbühler
,
K.
,
Noe
,
R.
, and
Seyfarth
,
R. M.
(
1997
). “
Diana monkey long-distance calls: messages for conspecifics and predators
,”
Anim. Behav.
53
,
589
604
.
This content is only available via PDF.
You do not currently have access to this content.