Noise affects black-tufted marmoset ( Callithrix penicillata ; GEOFFROY, 1812) phee call frequency

Abstract

Anthropogenic noise is very different from natural sounds, and could cause organisms living in noisy areas to modify their vocal communication. We assessed the influence of noise on black tufted-ear marmoset acoustic communication. Spontaneously produced phee vocalizations were recorded in two areas: a noisy urban park, located in Belo Horizonte, Minas Gerais state, Brazil and a quiet natural forest, located at Cauaia in Matozinhos, in the same state. We also recorded bus brakes sounds (BBS) in the noisy park because we noticed that the sounds produced by these vehicles were similar to the phee vocalizations. Frequencies and duration of phees and the BBS were measured and used to compare: 1- pheesfrom the urban and natural areas and 2- urban phee vocalizations and BBS. The duration of the phee calls was longer in the urban area. The low, high and dominant frequencies were significantly higher in the natural area. The low frequency extracted from BBS was similar to those of the phee calls of marmosets in the urban area. We suggest that the difference between the marmoset calls from urban and natural areas is influenced by noise and BBS compete with marmosets calls and may disturb the communication of these primates.

Full text

Comparing Contact Calling Between Black
Tufted-Ear Marmosets (Callithrix penicillata)
in a Noisy Urban Environment and in a
Quiet Forest
Noise Effects on Contact Calls in Black Tufted-Ear Marmosets
S. G. Santos
1
&M. H. L. Duarte
1,2
&
R. S. Sousa-Lima
3
&R. J. Young
4
Received: 1 February 2017 /Accepted: 2 October 2017 / Published online: 25 November 2017
#Springer Science+Business Media, LLC, part of Springer Nature 2017
Abstract All habitats have some level of noise but anthropogenic sounds such as those
produced by traffic are structurally different from natural sounds, and could cause
organisms living in noisy urban areas to modify their vocal communication. We
compared temporal and spectral parameters of contact calls in black tufted-ear marmo-
sets (Callithrix penicillata) living in a noisy and a quiet area. From February 2009 to
March 2012 we recorded spontaneously produced phee vocalizations by marmosets in
two areas in Minas Gerais, Brazil: a noisy urban park (N= 581) in Belo Horizonte, and
a quiet natural forest, on Cauaia farm in Matozinhos city (N= 560). We measured the
duration, frequencies, and rate of phee vocalizations. We found that marmosets’phee
vocalizations were significantly longer in the noisy area than in the quiet area. The low,
high, and dominant frequencies were significantly lower in the noisy area than in the
quiet area, and contact calling was less frequent in the noisy area than in the quiet area.
We suggest that the differences between marmoset contact calls from noisy and quiet
areas are influenced by anthropogenic noise.
Int J Primatol (2017) 38:1130–1137
https://doi.org/10.1007/s10764-017-0002-x
Handling Editor: Joanna M. Setchell
*S. G. Santos
sharada_bh@hotmail.com
1
Laboratory of Bioacoustics, Museum of Natural Sciences, Pontifical Catholic University of Minas
Gerais, Belo Horizonte, Minas Gerais 30535-901, Brazil
2
Graduate Program of Vertebrate Biology, Pontifical Catholic University of Minas Gerais, Belo
Horizonte, Minas Gerais 30535-901, Brazil
3
Laboratory of Bioacoustics, Federal University of Rio Grande do Norte, Natal 59078-970, Brazil
4
School of Environment and Life Sciences, University of Salford, Manchester M5 4WT, UK

Keywords Noise .Primates .Vocal communication
Introduction
Anthropogenic noise is a critical pollution problem for wildlife owing to its adverse
effects on animal behavior and physiology (Duarte et al.2015; Kight and Swaddle
2011; Popper and Hastings 2009; Warren et al.2006). Like chemical pollution, noise
pollution usually increases with increasing human population density (Katti and Warren
2004). All habitats are noisy, but the acoustic characteristics of sounds produced by
traffic (cars, motorcycles, trains, and aircraft), buildings, and industries are different
from most sounds in natural habitats, in terms of their dominant frequencies, rise time,
duty cycle, and impulsiveness (Brumm 2006). In humans, noise causes physiological
problems such as hearing loss, increased stress hormone levels, and hypertension
(Babisch 2003;Jarupet al.2008; Ryals et al.1999).
The effect of noise has been a concern for marine mammals that rely heavily on
sound communication since the 1990s (Richardson et al.1995) and for terrestrial fauna
more recently (Slabbekoorn and Peet 2003). Studies in urban areas show that noise
pollution is a serious threat for terrestrial animals (Halfwerk et al.2011;Rabinet al.
2003; Slabbekoorn and Ripmeester 2008). High levels of noise can mask acoustic
signals, hindering territorial defense, mate attraction, and other important social inter-
actions (Brumm et al.2004). Beside this, noise can distract animals, making them more
vulnerable to predation (Chan et al.2010) and can cause stress, with negative effects on
physiology and development (Kight and Swaddle 2011). Animals may use several
mechanisms to mitigate the effects of noise, for example, by altering their vocalizations
by increasing the amplitude, i.e., the Lombard effect; changing the frequency
(Slabbekoorn and Peet 2003), duration, or number of notes (Sun and Narins 2005;
Warr e n et al.2006); and changing the timing of vocal activity (Bergen and Abs 1997;
Sousa-Lima and Clark 2008).
There are several examples of vocal plasticity in primates. The vocal structure of
individuals can change as a result of social interactions (Janik and Slater 2000), changes
in social status or ecological niche (Snowdon 2009), and changes in the environment
(Brumm 2004). An increase in background noise amplitude was associated with a
significant increase in call amplitude and syllable duration in cotton-top tamarins
(Saguinus Oedipus: Egnor and Hauser 2006). Changes in the design of a signal may
have short- or long-term or even evolutionary consequences on the communication
system of animals via natural or sexual selection (Warren et al.2006).Studiesofthe
effects of noise on primates’vocalizations are important to develop management and
conservation strategies in natural areas close to anthropogenic activities (Brumm 2004;
Duarte et al.2011;Hotchkinet al.2015).
The black tufted-ear marmoset (Callithrix penicillata) is an endemic species from
Brazil that occurs in Cerrado, Caatinga, and Atlantic Forest (Miranda and Faria 2001).
Human encroachment on natural areas has induced occupation of urban areas by this
species (Chagas et al.1999). Owing to their behavioral flexibility, marmosets can adapt
to changing environmental conditions and, to some degree, to human influence
(Stevenson and Rylands 1988). Wild common marmosets (C. jacchus)possess13
different call types: trill,twitter,tsik,tsê,egg,chatter,squeal,moaning,very brief
Comparing Contact Calling Between Black Tufted-Ear Marmosets... 1131

whistle,alarm 1and2;scream,andphee calls (Bezerra and Souto 2008). Phee calls are
single- or multiphrase contact calls, which are frequently emitted by wild marmosets of
both species (C. jacchus and C. penicillata) in the same context. These calls are long
and tonal with durations of 0.5–2 s and fundamental frequencies varying from 6 to
10 kHz (Roy et al.2011). Phee calls are long-distance vocalizations and can have both
intra- and intergroup functions in Neotropical primates such as mate attraction, defense,
and territorial behavior (Norcross and Newman 1993; Oliveira and Ades 2004).
We tested the hypothesis that noise influences marmoset calls. We predicted that the
rate and structure of the marmosets’phee vocalization would differ between a noisy
urban area and a forested quiet area.
Methods
Study Area
We conducted the study from February 2009 to March 2012 in two areas in Minas
Gerais, Brazil: 1) noisy: an urban park (Municipal Park, Belo Horizonte) and 2) quiet: a
natural forest fragment on a farm in Matozinhos Municipality, where human presence is
rare. The noisy site is surrounded by major city avenues, a soundscape that differs
markedly from nature, mainly owing to excessive traffic noise sounds, park visitors,
and a fair every Sunday (Duarte et al.2011). The equivalent noise levels (a logarithmic
mean of noise levels at 20-min intervals) at the Municipal Park range from 50.1 to 80.0
dB on weekdays and from 50.1 to74.0 dB on weekends (Duarte et al.2011). The quiet
site is 600 acres of semideciduous forest, which is a private reserve, and is probably the
largest natural forest fragment in the region. Noise levels in the Quiet area ranged from
30.1 dB to 37.2 dB.
Study Subjects
We studied the only group of marmosets living in the Municipal Park. The number of
individuals ranged from 8 to 11 during the study owing to births and deaths. We
recorded vocalizations from three different groups in the quiet area. The number of
individuals ranged from 6 to 13 in group 1, 8 to 11 in group 2, and 9 to 13 in group 3.
Data Collection
We searched for the marmosets and recorded their spontaneous vocalizations when we
found them using a Marantz Professional Solid State Recorder (Model PMD660) and a
shotgun microphone (SennheiserME66). We also recorded the name of the individual
and the calling context after each vocalization sequence. We did not play any stimuli to
the marmosets to elicit call responses.
Data Analyses
We extracted the duration and low, high, and dominant frequency measurements of
each call from phee vocalizations using the program Raven Pro 1.5 (Bioacoustics
1132 Santos S.G. et al.

Research Program, Cornell Lab of Ornithology). We extracted all the measurements
from the fundamental frequency because the literature indicates that this band is most
modified by urban noise (Slabbekoorn and Peet 2003).
We used only the phee vocalizations for analyses, since other calls were difficult to
record from a distance. We compared the mean number of phee calls per hour and the
acoustic parameters of marmoset vocalizations from noisy and quiet areas using Mann–
Whitney test in Minitab version 15.
Ethical Note
The study reported in this paper complies with all appropriate laws in Brazil in relation
to the treatment of animals. The authors have no conflicts of interest to report
Results
We recorded 560 phee calls in the quiet area and 581 in the noisy area (Fig. 1).
Marmosets’phee vocalizations were significantly longer in the noisy area than in the
quiet area (U= 118495.5, P<0.001)(Fig.2). The low, high, and dominant funda-
mental frequencies of phee vocalizations were significantly higher in the quiet area than
in the noisy area (Low U= 110,118.5, P<0.001;HighU= 102,614.5, P<0.001,
Dominant U= 95,000, P<0.001)(Fig.2). Marmosets called more often in the quiet
(84 ± 43 calls/h) than in the noisy area (17.1 ± 29.9 calls/h) (U=12,000;P<0.001).
Discussion
We found differences in the temporal and spectral characteristics and rate of
marmoset phee vocalizations between quiet and noisy environments. We cannot
rule out group differences in vocalizations due to our study design, and our data are
pseudo-replicated owing to multiple measures of calls by the same individuals.
Fig. 1 Phee vocalizations selected from focal marmosets (Callithrix penicillata) recorded in the quiet forest
area (Cauaia farm, Matozinhos, Minas Gerais, Brazil).
Comparing Contact Calling Between Black Tufted-Ear Marmosets... 1133

Nevertheless, we found that marmoset calls were longer in a noisy than in a quiet
environment, that fundamental frequencies differed between the two environ-
ments, and that contact calling was less frequent in the noisy environment than
in the quiet environment.
Our finding that marmoset calls were longer in a noisy urban environment than
in a quiet environment reflects other studies in which primates’brief vocalizations
are longer in noisy environments than in quiet environments (Brumm et al.2004;
Egnor and Hauser 2006). The difference in mean call duration in our study was
significant but very small (140 ms). Nevertheless, marmosets may be able to
detect this difference because temporal resolution in mammals has a single time
integration constant of 8 ms (reviewed in Fay and Popper 1994). Therefore, an
increase in sound duration on the order of 140 ms could increase call detection
and recognition of the signals by marmosets in a noisy area. Psychoacoustic
studies would help to understand whether black-tufted marmosets can discriminate
the differences in spectral variables.
Our finding that marmosets called at lower low, high, and dominant frequencies in
the noisy area than in the quiet area contrasts, with the most common finding in birds
(Slabbekoorn and Peet 2003) and cetaceans (Parks et al.2007), where low-frequency
values are higher in the presence of noise, minimizing the overlap between the calls and
Fig. 2 Median and interquartile ranges of acoustic parameters of phee vocalizations by marmosets (Callithrix
penicillata) in a noisy (Municipal Park, Belo Horizonte, Minas Gerais, N= 581) and a quiet (Cauaia farm,
Matozinhos, Minas Gerais, N= 560) environment in Brazil.
1134 Santos S.G. et al.

anthropogenic sounds, i.e., reducing masking. Higher frequencies are less efficient than
lower frequencies over longer distances (Wiley and Richards 1978), and human
disturbance can change the way in which acoustic signals are transmitted (Rabin
et al.2003). We suggest that the marmosets decrease the frequency of contact calls
to improve their communication range, since the location of the sender is important in
contact calling.
The number of calls per hour was lower in the noisy area than in the quiet area,
suggesting that marmosets do not invest as much in contact calling in an environment in
which calls are often masked by noise and less likely to be detected. Our findings reflect
those for pygmy marmosets (Cebuella pygmaea), which vocalize less in areas with
human activity (de la Torre et al.2000). An alternative explanation is that the absence of
conspecific groups in the noisy area may have affected the amount of intergroup contact
calling. However, this is unlikely to influence intragroup contact calling, suggesting that
the effect of noise may explain reduced calling rates in the noisy area.
Belo Horizonte Municipal Park is located at the heart of the city’stransportationhub.
According to the mayor’s office of Belo Horizonte, the city has 2874 buses, which
transport 1.5 million people per day. We identified bus braking sounds in the recordings
that sounded like phee calls and have low fundamental frequencies similar to those of
the marmosets’phee calls in the noisy area. The overlap between the lower frequency
of phee calls and buses braking sounds may confuse the marmosets and cause them to
call less or change their call frequency.
Recent studies propose that birds could achieve higher signal-to-noise ratios more
efficiently by elevating amplitude rather than the frequency when exposed to low-
frequency noise (Nemeth and Brumm 2010). We did not calculate amplitude because
we could not measure distance to the vocalizing individual with confidence. However,
cotton-top tamarins (Saguinus oedipus) alter the amplitude of their vocalizations when
subjected to intense noise background, i.e., the Lombard effect (Egnor and Hauser
2006), and the same may have occurred in our study individuals.
Our results show that, although marmosets can inhabit urban environments, noise in
those areas may influence their communication. Together with a study showing that
marmosets prefer quieter areas in the park than louder areas (Duarte et al.2011), they
illuminate primate response to noise pollution. Differences in communication patterns
are indicators of human influence on animals and it is important to evaluate them when
making decisions about conservation strategies in urban areas.
Data Availability
The datasets analyzed during the study are availabe from the corresponding author on
reasonable request.
Acknowledgments The authors thank all of the staff at the Municipal Park of Belo Horizonte and Cauaia
farm. We are also grateful to Danusa Guedes for her help during data acquisition and the editor and
anonymous referees for their useful comments and suggestions on this manuscript. We also thank the
Programa de Educação Tutorial (MEC/SESu), for encouraging research and for financial support of S. G.
Santos. M. H. L. Duarte and S. G. Santos were also supported by the Fundação de Amparo à Pesquisa de
Minas Gerais (FAPEMIG), VALE S.A and CAPES postgraduate and post doc scholarships. R. J. Young and
R. S. Sousa-Lima received financial support from FAPEMIG and Conselho Nacional de Pesquisa (CNPq).
Comparing Contact Calling Between Black Tufted-Ear Marmosets... 1135

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