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Bioacoustics of the black-headed night monkey, Aotus nigriceps

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PRIMATES
NEOTROPICAL
ISSN 1413-4703
A J ou rn al of th e Neotropical Section of the
IUCN/SSC Primate Specialist Group
Volume 24
Number 1
June 2018
Editors
Erwin Palacios
Bruna Bezerra
Jessica Lynch Alfaro
Liliana Cortés Ortiz
Júlio César Bicca-Marques
Eckhard Heymann
Anita Stone
News and Book Reviews
Brenda Solórzano
Ernesto Rodríguez-Luna
PSG Chairman
Russell A. Mittermeier
PSG Deputy Chairman
Anthony B. Rylands
Neotropical Primates
A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group
Conservation International
2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA
ISSN 1413-4703 Abbreviation: Neotrop. Primates
Editors
Erwin Palacios, Conservación Internacional Colombia, Bogotá DC, Colombia
Bruna Bezerra, Universidade Federal de Pernambuco, Recife, Pernambuco, Brasil
Jessica Lynch Alfaro, Institute for Society and Genetics, University of California-Los Angeles, Los Angeles, CA, USA
Liliana Cortés Ortiz, Museum of Zoology, University of Michigan, Ann Arbor, MI, USA
Júlio César Bicca-Marques, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brasil
Eckhard Heymann, Deutsches Primatenzentrum, Göttingen, Germany
Anita Stone, Museu Paraense Emílio Goeldi, Belém, Pará, Brazil
News and Books Reviews
Brenda Solórzano, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, México
Ernesto Rodríguez-Luna, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, México
Founding Editors
Anthony B. Rylands, Conservation International, Arlington VA, USA
Ernesto Rodríguez-Luna, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, México
Editorial Board
Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK
Adelmar F. Coimbra-Filho, Academia Brasileira de Ciências, Rio de Janeiro, Brazil
Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA
Stephen F. Ferrari, Universidade Federal do Sergipe, Aracajú, Brazil
Russell A. Mittermeier, Conservation International, Arlington, VA, USA
Marta D. Mudry, Universidad de Buenos Aires, Argentina
Anthony Rylands, Conservation International, Arlington, VA, USA
Horácio Schneider, Universidade Federal do Pará, Campus Universitário de Bragança, Brazil
Karen B. Strier, University of Wisconsin, Madison, WI, USA
Maria Emília Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Primate Specialist Group
Chairman, Russell A. Mittermeier Deputy Chair, Anthony B. Rylands
Vice Chair, Special Section on Great Apes, Liz Williamson
Vice Chair, Special Section on Small Apes, Benjamin M. Rawson
Regional Vice Chairs—Neotropics
Mesoamerica, Liliana Cortés-Ortiz
Andean Countries, Erwin Palacios and Eckhard W. Heymann
Brazil and the Guianas, M. Cecília M. Kierul, Fabiano R. de Melo and Mauricio Talebi
Regional Vice Chairs —Africa
W. Scott McGraw, Janette Wallis and David N.M. Mbora
Regional Vice Chairs —Madagascar
Christoph Schwitzer and Jonah Ratsimbazafy
Regional Vice Chairs — Asia
China, Long Yongcheng
Southeast Asia, Jatna Supriatna, Christian Roos, Ramesh Boonratana and Benjamin M. Rawson
South Asia, Sally Walker and Sanjay Molur
Layout: Patricia Salinas Garzón, Bogotá, DC <patrisalinas@gmail.com>
IUCN/SSC Primate Specialist Group logo courtesy of Stephen D. Nash, 2002.
Front cover: Black titi monkey (Plecturocebus cinerascens). Photo taken at Guaporé River, Municipality of Comodoro, Mato Grosso, Brazil. July 2015.
Photo taken by Breno Dias Vitorino.
is issue of Neotropical Primates was kindly sponsored by the Margot Marsh Biodiversity Foundation, 432 Walker Road, Great Falls, Virginia 22066,
USA, and the Los Angeles Zoo, Director John R. Lewis, 5333 Zoo Drive, Los Angeles, California 90027, USA.
Neotropical Primates 24(1), June 2018 29
Soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4,
D-37077 Göttingen, Germany.
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nary eld study of the moustached tamarin monkey (Sa-
guinus mystax) in northeastern Peru: questions concerned
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tems: unusual exibility. Trends Ecol. Evol. 3: 36–40.
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teen-year study of a marked population. Am. J. Primatol.
38: 57–8.
Heymann, E. W. 1995. Sleeping habits of tamarins, Sa-
guinus mystax and Saguinus fuscicollis (Mammalia; Pri-
mates; Callitrichidae), in north-eastern Peru. J. Zool.
237: 211–226.
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breeding in mammals. Trends Ecol. Evol. 9: 89–93.
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tive success in wild common marmosets (Callithrix jac-
chus). Am. J. Primatol. 35: 311–317.
Löttker, P., Huck, M. and Heymann, E. W. 2004. Demo-
graphic parameters and events in wild moustached tama-
rins (Saguinus mystax). Am. J. Primatol. 64: 425–449.
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1996. Demography, group composition, and dispersal in
wild cotton-top tamarin (Saguinus oedipus) groups. Am.
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Schaner, C. M. and French, J. A. 1997. Group size and
aggression: “recruitment incentives” in a cooperatively
breeding primate. Anim. Behav. 54: 171–180.
Stojan-Dolar, M. and Heymann, E. W. 2010a. Functions
of intermittent locomotion in mustached tamarins (Sagu-
inus mystax). Int. J. Primatol. 31 (5): 677–692.
Stojan-Dolar, M. and Heymann, E. W. 2010b. Vigilance
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D. Nichols (eds.), pp. 180–188. Oxford University Press,
Oxford.
BIOACOUSTICS OF THE BLACK-HEADED NIGHT
MONKEY, AOTUS NIGRICEPS
William D. Helenbrook
Leigh Preston
Noah A. Linck
Megan Quirk
Jessica A. Suarez
Introduction
Only three studies have assessed Aotus vocalizations (known
as either owl or night monkeys). None of these studies
have assessed the black-headed night monkey (A. nigriceps)
found in southeastern Peru, northern Bolivia, and cen-
tral-western Brazil, nor have they focused on bioacoustics of
Aotus spp. in the wild. Of these three captive-based studies,
13 dierent call types have been described in A. lemurinus
(Andrew 1963; Moynihan 1964) and A. azarae (Kantha et
al. 2009). Most of these calls are distinct from one anoth-
er; however, there are some inconsistencies in naming that
need to be addressed, as described in Table 1. First, the
Trill described by Andrew (1963) has similar structure and
bandwidth to the Scream described by Moynihan (1964).
Moynihan does describe a Low Trill which is distinct from
the Trill in Andrew (1963), and the Low Trill described by
Kantha et al. (2009) does not resemble structure, band-
width, or call duration of the Trill in Andrew (1963) or the
Low Trill in Moynihan (1964). erefore, we suggest that
the Trill in Andrew (1963) is structurally distinct from the
Low Trill in Moynihan (1964), and the Low Trill in Kantha
et al. (2009) appears to be a distinct call from the other
two studies. Secondly, one of the representative Squeaks
described by Andrew (1963) is very similar to the Gru
Grunt (Moynihan 1964). Each has numerous harmonics,
a similar descending frequency across the exact call dura-
tion, and a very similar bandwidth. erefore, the Gru
Grunt should be renamed Squeak, as it was previously de-
scribed in Andrews (1963). irdly, the Squeak described
by Moynihan (1964) is structurally similar to the Twitter
described by Andrews (1963) and should be renamed.
Fourth, neither the Long Scream nor the Short Scream
described by Kantha et al. (2009) appear to be similar in
structure, bandwidth, or duration to the Scream in Moyni-
han (1964) and should potentially be renamed. Fifth, the
Moan described by Moynihan (1964) is not similar to the
Moan in Kantha et al. (2009) in structure, bandwidth, or
duration. e low frequency band is structurally similar to
a variant Low Trill described by Moyniahn 1964, though
the quality of the spectrogram in Kantha et al. (2009)
makes it dicult to conrm this possibility. And nally,
the Gulp described by Kantha et al. (2009) is similar to the
Gulp in Moynihan (1964); however, the bandwidth in the
Neotropical Primates 24(1), June 201830
Table 1. Vocal descriptions from all previously published captive and semi-captive Aotus studies. Several similar calls were found in both
Moynihan 1964 and Kantha et al. 2009, though both were included because they were found in dierent species and have dierent band-
width and duration.
Species Call type
Mean
Bandwidth
(Hz)
Mean
Duration
(msec)
Description
Aotus lemurinus
griseimembra (a)
Twitter 2000-8000 40
Descending from 3.5-4 kHz to 2-3 kHz; Long rapid series once
every 200 msec. A fundamental frequency (2-4 kHz) with a
second harmonic at 5-8* kHz
Trill 1000-7000* 300 Series of Twitters
Aotus lemurinus
griseimembra (b)
Squeak 500-5000 100
"Guinea pig squeak" starting at lower frequency (500 Hz) and
rising steeply to 4-4 kHz; or, simply protracted lower frequency
(500-700 Hz)
Sharp Call 1000-15000 150-250 Sometimes sharp initial click. Once every 150-250 msec
Boom 150 1000+ Low soft call by vibration of false vocal cords
Low Trill 240-500* 600* Bubbling series of low-pitched notes, rapid but distinguishable
series. Varied from 3-12 notes
Gulp 0-650 100-260 Very common. Moderately loud and rather "liquid" sounding.
Uttered in series of 2 to 3 notes. Series repeats rapidly
Gru Grunt 100-4000* 100*
Most common. Uttered as singly or in short series of two to
ve notes. Successive notes uttered at slightly irregular intervals.
Longer pauses. Low-pitched, moderately long, and moderately
loud. Multiple harmonics
Squeak 1000-9500* 50* 1-3.5 kHz fundamental frequency, followed by two harmonics
ranging from 4-9.5 kHz
Sneeze Grunt 0-1000* 200*
Sneeze superimposed upon a loud Gru Grunt. Usually uttered
as a single note, though sometimes two in quick succession.
Often associated with Gulps, single Low or High Trill, or Moan
Resonant Grunts Unknown Unknown
More complex than Gru Grunt and rarer. Speed loudness,
and pitch varied considerably. Long series of 10-15 notes. Most
common series included soft and low notes rst half of series
(softer than Gru Grunt), and progressively louder towards
middle of series. Towards climax similarly loud, resonating, and
rapid. Finally, slowed in tempo, lower and softer
Aotus azarae (c)
Moan 220-480* 600*
Brief, soft, moan. Most common call type in captive individuals.
Often uttered along with other calls before or after, including
Low Trills, Gulps, and Sneeze Grunts
Scream 2000-8500* 800 High pitched but wavering. Quite prolonged. Multiple
harmonics (though an exact number not given)
Moan 140-300 500 No description given
Long Scream 2800-5800 260 No description given
Gulp 1800-5800 54 No description given
Low Trill 2000-3100 52 No description given
Short Scream 980-3300 190 No description given
Sneeze Grunt 1580-3310 50 No description given
earlier study is far less than 1 kHz, while the Kantha et al.
(2009) study shows an upper frequency of at least 10 kHz.
Based on the available data and without further descriptive
analysis in Kantha et al. (2009), these should likely be con-
sidered distinct calls.
Vocalization analysis for owl monkey species is particularly
important as it is dicult to dierentiate between individ-
uals or determine group dynamics because they are noc-
turnal. A vocal assessment could potentially be used to dif-
ferentiate individuals and assess group membership during
(a) Andrew 1963 (2 laboratory animals) and (b) Moynihan 1964 (12 semi-captive animals) originally classied as A. trivirgatus; (c) Kantha et al. 2009
(16 laboratory animals). *Estimates based solely on published spectrogram.
new group encounters simply based on bioacoustics (Salmi
et al. 2014). e objective of this study, consequently, was
to add to the Aotus bioacoustic literature by sampling sev-
eral geographically dispersed groups of wild A. nigriceps
(Fig. 1) in southeastern Peru.
Neotropical Primates 24(1), June 2018 31
Figure 1. Spectrogram images (left) and frequency distribution of calls (right) for three described calls: Twitter (High), Ch Ch, and Long
Trill. Frequency distributions represent upper frequency range (A), lower frequency range (B), and bandwidth (C) for each call. Box and
whisker represent mean, 1 standard deviation, and 2 standard deviations. For squeak, only low, high, and alto spectrograms are shown.
Ch ch calls shown as common pair.
Methods
Bioacoustic recordings were collected from eleven A.
nigriceps groups ranging in size from 2-5 individuals.
Sampling occurred April-May 2016, October-Novem-
ber 2016, and April 2017, for a total of twenty-eight
days at Villa Carmen Biological Station (12°53’39»S,
71°24’16”W) and nine days at Manu Learning Center
(CREES) research station (12°4722S 71°2332W) -
both in premontane rainforest. Seven groups were sam-
pled Villa Carmen and four groups at CREES, both lo-
cated on the edge of Manu National Park buer zone in
the Peruvian Amazon. Villa Carmen has a long history of
development, ecotourism and agriculture. Sampled areas
were largely dominated by secondary forest. At CREES,
groups were sampled in areas of rainforest regeneration.
Groups of 2-7 researchers searched for night monkey
groups from 5:30-7:30 am and 5:30-7:30 pm, times
when A. nigriceps groups are known to be active near their
nesting sites. Two recordings took place before 5:30 am,
when researchers left the eld station early to visit more
distant night monkey groups. Additional vocalizations
were heard during the day, though none were included
in this study. A Zoom H1 Handy Recorder was coupled
with a RØDE NTG-2 condenser shotgun microphone
and shoe shockmount on a micro boompole. Recordings
were collected at a sampling frequency of 48 kHz at a dis-
tance varying from 2-25 m. Certain groups were sampled
more extensively than others, due to logistic feasibility.
When feasible, behaviors associated with vocalizations
were categorized into three activities: resting, traveling,
or feeding. All calls were compared to the three previous
Neotropical Primates 24(1), June 201832
e Twitter was named after the similarly structured
Twitter call described by Andrew (1963), though mea-
surable dierences exist in number of harmonics and
bandwidth (Table 2). e Twitter was found in all but
one group and had up to 3 additional harmonics beyond
the fundamental frequency (191-553 Hz), ranging from
a mean of 1,755-2,847 Hz (High), to 3,666 4,140 Hz
(Alto), to 3,562 4,808 Hz (Ultra). e low fundamen-
tal frequency and high dominant harmonic were always
present in the Twitter, whereas the Alto and Ultra were
only found in single groups at Villa Carmen. e mean
bandwidth of the Ch Ch call was 1,611 9,961 Hz with
a mean duration of 183 msec.
Figure 2. Photo of the black-headed night monkey, Aotus nigri-
ceps. Photo credit: Jessica A. Suarez.
Aotus studies (Andrew 1963; Moynihan 1964; Sri Kan-
tha et al. 2009). Audio recordings were analyzed using
the spectral audio program Raven Pro 1.5 Sound Anal-
ysis Software (Cornell Lab of Ornithology Bioacoustics
Research Program, Ithaca, New York). Duration of calls,
dominant and fundamental frequencies, high and low
frequencies, and total bandwidth were then measured.
Amplitude was not analyzed because we could not control
for size or age of individuals. All recordings were con-
ducted non-invasively, minimized impact on behavior,
and avoided excessive disturbance, and the research was
therefore deemed exempt from the Institutional Animal
Care and Use Committee approval. All research adheres
to the principles for the ethical treatment of primates set
forth by Neotropical Primates. Audio les analyzed dur-
ing the current study are available from the correspond-
ing author on reasonable request through ResearchGate.
Results
ree distinct calls were identied in our study, including
the Twitter (N = 165), Ch Ch (N = 122), and Long Trill
(N = 3) (Figure 2). In a limited number of cases, we were
able to note an associated behavior with calls. Of 46 High
Twitter calls, 47.8 % took place while the individual was
traveling and 52.1 % of calls took place while resting. Of
19 Ch Ch calls, 36.8 % were associated with travel, and
63.2 % with resting. No behaviors were recorded during
the Long Trill.
Table 2. Acoustic properties of three calls in wild black-headed night monkeys, Aotus nigriceps. e squeak is characterized by a funda-
mental frequency (low), and dominant frequency (high).
Call Type Bandwidth
(Hz)
Mea Duration
(msec) Description
Twitter
Similar in structure of Twitter described by Andrew (1963), though additional harmonics
described here.
Ultra 3562-4808 49
Alto 3666-4140 20
High 1755-2847 43
Low 191-553 21
Ch Ch 1611-9961 183
Similar to Gulp described by Kantha et al. (2009); however, this name does not correspond
with the Gulp described by Moynihan (1964) which has a much lower frequency (<1000
Hz). erefore, we have renamed to reect a new call type.
Long Trill 470-3046 170 Similar to original Trill described by Andrew (1963) and the Scream described by Moynihan
(1964). ere are some structural dierences which is why we refer to it as the Long Trill
e Ch Ch call is similar to the Gulp described by Kantha
et al. (2009); however, this name does not correspond to the
Gulp described originally by Moynihan (1964). erefore,
we have renamed the call as an onomatopoeic description,
Ch Ch. e Ch Ch call was recorded as two closely paired
repetitive sounds in ten out of eleven groups (84.4 % of mea-
sured cases), a Ch Ch Ch (triplet) in four groups (14.8 %
of measured cases), and a Ch Ch Ch Ch (quadruplet) in
one group (0.01 % of measured cases). Only four groups
at Villa Carmen exhibited a triplet Ch Ch, and a group at
CREES produced the call in a quadruplet. e Long Trill is
named in part after the Trill described originally by Andrew
(1963), though structurally there are dierences. Namely,
in our study the call descends in frequency, whereas there is
an oscillation around 3,500-5,000Hz in A. lemurinus. e
Long Trill is also found primarily between 3,500-5,000HZ,
whereas our study had a higher frequency around 3,000HZ.
ere were several instances of the Long Trill, but only in two
groups found at Villa Carmen Biological Station. However,
only a single instance had a clear spectrogram that could be
used for analysis due to the complexity of the acoustic land-
scape at that particular frequency.
Neotropical Primates 24(1), June 2018 33
Discussion
No known studies have assessed the bioacoustics of any wild
Aotus species. Furthermore, no studies have analyzed Ao-
tus nigriceps vocalizations, even in captivity. is study de-
scribes three calls in A. nigriceps (Twitter, Ch Ch, and Long
Trill), though continued eld research may reveal additional
calls. irteen other calls have previously been described in
A. azarae and A. lemurinus, which suggests that the vocal
repertoire of Aotus nigriceps is likely larger than described
here. However, captive settings allow researchers to control
for background noise and to elicit calls in response to ex-
perimental stimuli, which may increase the number of calls
found in captivity compared to a wild setting. Bioacoustic
information in wild primates is also likely to be dierent
than those in captivity because of their capacity to adjust
calls in an environment lled with background white noise
from both biotic and abiotic factors (Brumm et al. 2004).
For example, the frequency range of captive Aotus species
was previously reported to be 140-5,800 Hz; however, some
of our calls peaked at 13,612 Hz (e.g., Ch Ch), and all but
one call fell within the previously reported range. is could
be an adaptation to a much more crowded acoustic envi-
ronment, where other organisms use a similar bandwidth
(Ey and Fischer 2009). We report initial ndings of behav-
ioral associations with vocalizations, though caution must
be taken in interpreting these results since the majority of
behaviors couldn’t be documented due to dense foliage or
total darkness. Our continued research includes aspects of
intra- and inter-group variability, geographic variability, in-
ter-species diversity, and behavioral playback experiments in
wild Aotus nigriceps populations.
Acknowledgements
ank you to the Amazon Conservation Association
(ACA), Villa Carmen Biological Station and Manu Learn-
ing Center (CREES) sta for hosting us, clearing trails,
and providing valuable insight into location and behavior
of groups. We are indebted to students and sta from the
School for Field Studies who assisted with data collection
and logistics.
William Daniel Helenbrook, State University of New
York College of Environmental Science and Forestry
(SUNY-ESF), Syracuse, New York and Tropical Conser-
vation Fund, Atlanta, Georgia; Email: <wdhelenb@syr.
edu>; Leigh Preston, Hamilton College, Clinton, New
York; Noah Alexander Linck, University of Minnesota
Twin-Cities, St. Paul, Minnesota; Megan Quirk, Gustavus
Adolphus College, St. Peter, Minnesota; Jessica Alexandra
Suarez, Tropical Conservation Fund, Atlanta, Georgia.
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NEW RECORDS OF THE BLACK TITI MONKEY
(PLECTUROCEBUS CINERASCENS) (PRIMATES,
PITHECIIDAE) IN THE ALTO VALE GUAPORÉ,
BORDER REGION BETWEEN BRAZIL AND
BOLIVIA
Breno Dias Vitorino
Angélica Vilas Boas da Frota
Solange Kimie Ikeda Castrillon
Introduction
e black titi monkey, previously classied as Callicebus cin-
erascens (Spix, 1823), from molecular evidence is currently
included in the genus Plecturocebus (Byrne et al., 2016).
Has a gray coat over almost all the body with a contrasting
brown patch on the back. It feeds on fruits, leaves, insect
and seeds. It inhabits dry land environments, Campinara-
na (forest fragments with poor, rocky, shallow soil and a
mix of trees and bamboo), secondary forests and relatively
open areas. Its known distribution is still imprecise due to
the limited number of records for the species (Veiga et al.,
2008). Current knowledge about Plecturocebus cinerascens
distribution indicates occurrence in the Madeira-Tapajós
interuves (Noronha et al., 2007), with records on the left
bank of the Juruena River, the region of the headwaters of
the Roosevelt River, the right bank of the Cabixi River, the
right bank of the Alto Guaporé River among municipality
of Vila Bela da Santíssima Trindade and Pontes e Lacerda,
and within the Juruena-Teles Pires interuves (Sampaio et
al., 2012). e western limit may be the municipality of
Pimenteiras do Oeste, in the middle of the Vale do Gua-
poré, in the state of Rondônia, Brazil (Gusmão and Costa,
2014). e species is considered endemic to Brazil.
For this poorly known species (Sampaio et al., 2012) with
an imprecise distribution delimitation especially in relation
to its southern and southeastern limits (Veiga et al., 2008),
new record reports are extremely important. e present
study presents four new observations of P. cinerascens in the
... In contrast to other genera, our knowledge of owl monkey vocal communication that would allow evaluation of the hypothesis remains quite limited. Only two studies on captive animals have assessed the vocal repertoire of Aotus (Moynihan 1964;Kantha et al. 2009); in two other studies of vocal communication in wild owl monkeys, the authors were not able to unequivocally identify the sexes or age of the individuals due to the strictly nocturnal habits of the species studied (Wright 1985;Helenbrook et al. 2018). These studies suggested that one call, the hoot call, conveys information over long distances and that could be differentiated into two sub-types, graff and tonal ones (Wright 1985). ...
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This is the first in a series of papers on some behavior patterns of New World monkeys. The main emphasis of these papers will be comparative. Special attention will be paid to social signal patterns (including hostile and sexual signals) and other patterns that differ significantly in the various species. It is hoped that analyses of these patterns may throw some light on the evolution of the group as a whole.
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