Vocalizations of Madagascar’s lemurs have generally been less investigated than those of other primate groups, with virtually no information available about calling in the silky sifaka (Propithecus candidus), a large rainforest species. Current work examined the “zzuss” vocalization, one of the most common and loudest sounds produced by this monomorphic species, and included 160 calls from nine adults (five males, four females) in three groups. Analyses focused on overall acoustic features, individual and sex differences, call usage, and likely function. Acoustically, the calls included separable turbulent noise and tonal components, with the later often marked by frequency jumps and dramatic frequency modulation. Male and female zzuss calls differed most in F0- and amplitude-related features, characteristics that are relatively unconstrained by overall body size. All measures differed among individual callers, with F0-related variables again playing the largest role. Based on usage, these calls most likely function both as generalized alarm and group-coordination signals. The sounds were thus of interest in several regards, including showing sexual differentiation in the absence of other dimorphisms, exhibiting primarily F0-based differentiation in both sex- and individual-based comparisons, and combining apparent alarm and coordination functions across a variety of contexts.

1.
Altmann
,
J.
(
1974
). “
Observational study of behavior: Sampling methods
,”
Behaviour
49
,
227
265
.
61.
Bachorowski
,
J. A.
, and
Owren
,
M. J.
(
1999
). “
Acoustic correlates of talker sex and individual talker identity are present in a short vowel segment produced in running speech
,”
J. Acoust. Soc. Am.
106
,
1054
1063
.
2.
Benz
,
J. J.
,
French
,
J. A.
, and
Leger
,
D. W.
(
1990
). “
Sex differences in vocal structure in a callitrichid primate, Leontopithecus rosalia
,”
Am. J. Primatol.
21
,
257
264
.
3.
Blumstein
,
D. T.
, and
Recapet
,
C.
(
2009
). “
The sound of arousal: The addition of novel non-linearities increases responsiveness in marmot alarm calls
,”
Ethology
115
,
1074
1081
.
4.
Brown
,
C. H.
,
Alipour
,
F.
,
Berry
,
D. A.
, and
Montequin
,
D.
(
2003
). “
Laryngeal biomechanics and vocal communication in the squirrel monkey (Saimiri boliviensis)
,”
J. Acoust. Soc. Am.
113
,
2114
2126
.
5.
Brown
,
C. H.
,
Schessler
,
T.
,
Moody
,
D.
, and
Stebbins
,
W.
(
1982
). “
Vertical and horizontal sound localization in primates
,”
J. Acoust. Soc. Am.
72
,
1804
1811
.
6.
Buesching
,
C. D.
,
Heistermann
,
M.
,
Hodges
,
J. K.
, and
Zimmermann
,
E.
(
1998
). “
Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus
,”
Folia Primat.
69
,
295
308
.
7.
Cheney
,
D. L.
, and
Seyfarth
,
R. M.
(
1990
).
How Monkeys See the World
(
University of Chicago
,
Chicago, IL
), pp.
1
388
.
8.
Clark
,
A.
, and
Wrangham
,
R.
(
1993
). “
Acoustic analysis of wild chimpanzee pant hoots: Do Kibale Forest chimpanzees have an acoustically distinct food arrival pant hoot?
,”
Am. J. Primatol.
31
,
99
109
.
10.
Dollar
,
L. J.
,
Ganzhorn
,
J. U.
, and
Goodman
,
S. M.
(
2007
). “
Primates and other prey in the seasonally variable diet of Cryptoprocta ferox in the dry deciduous forest of western Madagascar
,” in
Primate Anti-Predator Strategies
, edited by
S. L.
Gursky
and
K. A. I.
Neckaris
(
Springer
,
New York)
, pp.
63
76
.
12.
Fichtel
,
C.
, and
Kappeler
,
P. M.
(
2002
). “
Anti-predator behaviour of group-living Malagasy primates: Mixed evidence for a referential alarm call system
,”
Behav. Ecol. Sociobiol.
51
,
262
275
.
13.
Fichtel
,
C.
, and
Kappeler
,
P. M.
(
2011
). “
Variation in the meaning of alarm calls in Verreaux’s and Coquerel’s sifakas (Propithecus verreauxi, P. coquereli)
,”
Int. J. Primat.
32
,
346
361
.
62.
Fitch
,
W. T.
, and
Hauser
,
M. D.
(
2002
). “
Unpacking ‘honesty’: Vertebrate vocal production and the evolution of acoustic signals
,” in
Acoustic Communication
, edited by
A.
Simmons
,
R. R.
Fay
, and
A.N.
Popper
(
Springer
,
New York)
, pp.
65
137
.
15.
Fitch
,
W. T.
,
Neubauer
,
J.
, and
Herzel
,
H.
(
2002
). “
Calls out of chaos: The adaptive significance of nonlinear phenomena in mammalian vocal production
,”
Anim. Behav.
63
,
407
418
.
16.
Gamba
,
M.
,
Colombo
,
C.
, and
Giacoma
,
C.
(
2011
). “
Acoustic cues to caller identity in lemurs: A case study
,”
J. Ethol.
30
,
191
196
.
17.
Gamba
,
M.
, and
Giacoma
,
C.
(
2007
). “
Quantitative acoustic analysis of the vocal repertoire of the crowned lemur
,”
Ethol. Ecol. Evol.
19
,
323
343
.
18.
Garreau
,
J. M.
, and
Manantsara
,
A.
(
2003
). “
The protected-area complex of the Parc National de Marojejy and the Reserve Speciale d’Anjanaharibe-Sud
,” in
The Natural History of Madagascar
, edited by
S. M.
Goodman
and
J. P.
Benstead
(
University of Chicago
, Chicago, IL), pp.
1451
1458
.
20.
Giacoma
,
C.
,
Sorrentino
,
V.
,
Rabarivola
,
C.
, and
Gamba
,
M.
(
2010
). “
Sex differences in the song of Indri indri
,”
Int. J. Primat.
31
,
539
551
.
21.
Goodman
,
S. M.
(
2003
). “
Predation on lemurs
,” in
The Natural History of Madagascar
, edited by
S. M.
Goodman
and
J. P.
Benstead
(
University of Chicago
,
Chicago, IL
), pp.
1221
1228
.
22.
Heffner
,
R. S.
(
2004
). “
Primate hearing from a mammalian perspective
,”
Anat. Rec.
Part A
281
,
1111
1122
.
23.
Irwin
,
M. T.
,
Raharison
,
J. L.
, and
Wright
,
P. C.
(
2009
). “
Spatial and temporal variability in predation on rainforest primates: Do forest fragmentation and predation act synergistically?
,”
Anim. Conserv.
12
,
220
230
.
24.
Kappeler
,
P. M.
(
1993
). “
Sexual selection and lemur social systems
,” in
Lemur Social Systems and Their Ecological Basis
, edited by
P. M.
Kappeler
and
J. U.
Ganzhorn
(
Plenum
,
New York)
, pp.
223
240
.
25.
Karpanty
,
S. M.
, and
Wright
,
P. C.
(
2007
). “
Predation on lemurs in the rainforest of Madagascar by multiple predator species: Observations and experiments
,” in
Primate Anti-Predator Strategies
, edited by
S. L.
Gursky
and
K. A. I.
Neckaris
(
Springer
,
New York)
, pp.
77
99
.
64.
Leger
,
D. W.
(
1993
). “
Contextual sources of information and responses to animal communication signals
,”
Psychol. Bull.
113
,
295
304
.
26.
Lehman
,
S. M.
,
Mayor
,
M.
, and
Wright
,
P. C.
(
2005
). “
Ecogeographic size variations in sifakas: A test of the resource seasonality and resource quality hypotheses
,”
Am. J. Phys. Anthropol.
126
,
318
328
.
27.
Leliveld
,
L.
,
Scheumann
,
M.
, and
Zimmermann
,
E.
(
2011
). “
Acoustic correlates of individuality in the vocal repertoire of a nocturnal primate (Microcebus murinus)
,”
J. Acoust. Soc. Am.
129
,
2278
2288
.
28.
Macedonia
,
J. M.
(
1986
). “
Individuality in a contact call of the ringtailed lemur (Lemur catta)
,”
Am. J. Primatol.
11
,
163
179
.
29.
Macedonia
,
J. M.
, and
Evans
,
C. S.
(
1993
). “
Variation among mammalian alarm call systems and the problem of meaning in animal signals
,”
Ethology
93
,
177
197
.
30.
Macedonia
,
J. M.
, and
Stanger
,
K.
(
1994
). “
Phylogeny of the Lemuridae revisited: Evidence from communication signals
,”
Folia Primat.
63
,
1
43
.
65.
Marler
,
P.
,
Evans
,
C. S.
, and
Hauser
,
M. D.
(
1992
). “
Animal signals: Reference, motivation or both?
” in
Nonverbal Vocal Communication: Comparative and Developmental Approaches
, edited by
H.
Papoucek
,
U.
Jurgens
, and
M.
Papoucek
(
Cambridge University Press
,
Cambridge, UK)
, pp.
66
86
.
31.
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
.
32.
Mitani
,
J. C.
(
1985
). “
Responses of gibbons (Hylobates muelleri) to self, neighbor, and stranger song duets
,”
Int. J. Primatol.
6
,
193
200
.
66.
Mitani
,
J. C.
, and
Gros Louis
,
J.
(
1995
). “
Species and sex differences in the screams of chimpanzees and bonobos
,”
Int. J. Primatol.
16
,
393
411
.
33.
Mittermeier
,
R. A.
,
Louis
,
E. E.
,
Richardson
,
M.
,
Schwitzer
,
C.
,
Langrand
,
O.
,
Rylands
,
A. B.
,
Hawkins
,
F.
,
Rajaobelina
,
S.
,
Ratsimbazafy
,
J.
,
Rasoloarison
,
R.
,
Roos
,
C.
,
Kappeler
,
P. M.
, and
MacKinnon
,
J.
(
2010
).
Lemurs of Madagascar
, 3rd ed. (
Conservation International
,
Washington, DC
), pp.
1
767
.
34.
Mundry
,
R.
, and
Sommer
,
C.
(
2007
). “
Discriminant function analysis with nonindependent data: Consequences and an alternative
,”
Anim. Behav.
74
,
965
976
.
35.
Owren
,
M. J.
, and
Rendall
,
D.
(
2001
). “
Sound on the rebound: Bringing form and function back to the forefront in understanding nonhuman primate vocal signaling
,”
Evol. Anthropol.
10
,
58
71
.
36.
Owren
,
M. J.
,
Seyfarth
,
R. M.
, and
Cheney
,
D. L.
(
1997
). “
The acoustic features of vowel-like grunt calls in chacma baboons (Papio cynocephalus ursinus): Implications for production processes and functions
,”
J. Acoust. Soc. Am.
101
,
2951
2963
.
37.
Patel
,
E. R.
(
2005
). “
Silky sifaka (Propithecus candidus) predation by a fossa (Cryptoprocta ferox)
,”
Lemur News
10
,
25
27
.
38.
Patel
,
E. R.
(
2009
). “
Silky sifaka, Propithecus candidus, 1871
,” in
Primates in Peril: The World’s 25 Most Endangered Primates 2008–2010
, edited by
R. A.
Mittermeier
,
J.
Wallis
,
A. B.
Rylands
,
J. U.
Ganzhorn
,
J. F.
Oates
,
E. A.
Williamson
,
E.
Palacios
,
E. W.
Heymann
,
M. C. M.
Kierulff
,
L.
Yongcheng
,
J.
Supriatna
,
C.
Roos
,
S.
Walker
,
L.
Cortés-Ortiz
, and
C.
Schwitzer
(
Conservation International
,
Arlington, VA
), pp.
23
26
.
39.
Patel
,
E. R.
, and
Owren
,
M. J.
(
2007
). “
Acoustics and behavioral contexts of ‘gecker’ vocalizations in young rhesus macaques (Macaca mulatta)
,”
J. Acoust. Soc. Am.
121
,
575
585
.
40.
Petter
,
J. J.
, and
Charles-Dominique
,
P.
(
1979
). “
Vocal communication in prosimians
,” in
The Study of Prosimian Behavior
, edited by
G. A.
Doyle
and
R. D.
Martin
(
Academic
,
New York
), pp.
247
305
.
41.
Ramsier
,
M. A.
, and
Dominy
,
N. J.
(
2010
). “
Comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang
,”
Am. J. Primatol.
72
,
217
233
.
42.
Range
,
F.
, and
Fischer
,
J.
(
2004
). “
Vocal repertoire of sooty mangabeys (Cercocebus torquatus atys) in the Taï National Park
,”
Ethology
110
,
301
321
.
43.
Rasoloharijaona
,
S.
,
Randrianambinina
,
B.
,
Braune
,
P.
, and
Zimmermann
,
E.
(
2006
). “
Loud calling, spacing, and cohesiveness in a nocturnal primate, the Milne Edwards’ sportive lemur (Lepilemur edwardsi)
,”
Am. J. Phys. Anthropol.
129
,
591
600
.
44.
Rendall
,
D.
, and
Owren
,
M. J.
(
2010
). “
Vocalizations as tools for influencing the affect and behavior of others
,” in
Handbook of Mammalian Vocalization, Vol. 19: An Integrative Neuroscience Approach
, edited by
S.
Brudzynski
(
Elsevier
,
New York
), pp.
177
185
.
45.
Rendall
,
D.
,
Owren
,
M. J.
, and
Rodman
,
P. S.
(
1998
). “
The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations
,”
J. Acoust. Soc. Am.
103
,
602
614
.
46.
Rendall
,
D.
,
Vokey
,
J. R.
, and
Nemeth
,
C.
(
2007
). “
Lifting the curtain on the wizard of Oz: Biased voice-based impressions of speaker size
,”
J. Exp. Psychol. Hum. Percept. Perform.
33
,
1208
1219
.
47.
Riede
,
T. R.
,
Arcadi
,
A. C.
, and
Owren
,
M. J.
(
2007
). “
Nonlinear acoustics in the pant-hoot vocalizations of common chimpanzees (Pan troglodytes), II: Vocalizing at the edge
,”
J. Acoust. Soc. Am.
121
,
1758
1767
.
48.
Riede
,
T. R.
,
Owren
,
M. J.
, and
Arcadi
,
A. C.
(
2004
). “
Nonlinear acoustics in the pant-hoot vocalizations of common chimpanzees (Pan troglodytes): Frequency jumps, subharmonics, biphonation, and deterministic chaos
,”
Am. J. Primatol.
64
,
277
291
.
49.
Schön Ybarra
,
M.
(
1995
). “
A comparative approach to the nonhuman primate vocal tract: Implications for sound production
,” in
Current Topics in Primate Vocal Communication
, edited by
E.
Zimmerman
,
J. D.
Newman
, and
U.
Jurgens
(
Plenum
,
New York
), pp.
185
198
.
50.
Seyfarth
,
R. M.
,
Cheney
,
D. L.
, and
Marler
,
P.
(
1980
). “
Vervet monkey alarm calls: Semantic communication in a free-ranging primate
,”
Anim. Behav.
28
,
1070
1094
.
51.
Smith
,
A. S.
,
Birnie
,
A. K.
,
Lane
,
K. R.
, and
French
,
J. A.
(
2009
). “
Production and perception of sex differences in vocalizations of Wied’s black-tufted-ear marmosets (Callithrix kuhlii)
,”
Am. J. Primatol.
71
,
324
332
.
67.
Smith
,
W. J.
(
1997
). “
The behavior of communicating, after twenty years
,” in
Perspectives in Ethology
, edited by
D. H.
Owings
,
M. D.
Beecher
, and
N. S.
Thompson
(
Springer-Verlag
,
New York
), pp.
7
51
.
52.
Snowdon
,
C. T.
(
2004
). “
Sexual selection and communication
,” in
Sexual Selection in Primates: New and Comparative Perspectives
, edited by
P. M.
Kappeler
and
C.
van Schaik
(
Cambridge University Press
,
New York
), pp.
57
70
.
53.
Titze
,
I. R.
(
1989
). “
Physiologic and acoustic differences between male and female voices
,”
J. Acoust. Soc. Am.
85
,
1699
1707
.
54.
Tokuda
,
I.
,
Riede
,
T.
,
Neubauer
,
J.
,
Owren
,
M. J.
, and
Herzel
,
H.
(
2002
). “
Nonlinear prediction of irregular animal vocalizations
,”
J. Acoust. Soc. Am.
111
,
2908
2919
.
55.
Trillmich
,
J.
,
Fichtel
,
C.
, and
Kappeler
,
P. M.
(
2004
). “
Coordination of group movements in wild Verreaux’s sifakas (Propithecus verreauxi)
,”
Behaviour
141
,
1103
1120
.
56.
Waser
,
P. M.
, and
Brown
,
C. H.
(
1986
). “
Habitat acoustics and primate communication
,”
Am. J. Primatol.
10
,
135
154
.
57.
Wilden
,
I.
,
Herzel
,
H.
,
Peters
,
G.
, and
Tembrock
,
G.
(
1998
). “
Subharmonics, biphonation, and deterministic chaos in mammal vocalization
,”
Bioacoustics
9
,
171
196
.
58.
Wright
,
P. C.
(
1998
). “
Impact of predation risk on the behaviour of Propithecus diadema edwardsi in the rainforest of Madagascar
,”
Behaviour
135
,
1
30
.
60.
Zimmermann
,
E.
,
Leliveld
,
L.
, and
Schehka
,
S.
(
2012
). “
Toward the evolutionary roots of affective prosody in speech and music: Universal affect cues in mammalian voices?
” in
Evolution of Emotional Communication: From Sounds in Nonhuman Mammals to Speech and Music in Man
, edited by
E.
Altenmüller
,
S.
Schmidt
, and
E.
Zimmermann
(
Oxford University
,
Oxford, U.K.
).
63.
See supplementary material at http://dx.doi.org/10.1121/1.4740475 for two audio files (1 male zzuss call and 1 female zzuss call).

Supplementary Material

You do not currently have access to this content.