Content uploaded by Marcos Rodrigues
Author content
All content in this area was uploaded by Marcos Rodrigues on Sep 17, 2017
Content may be subject to copyright.
ORIGINAL ARTICLE
Mining noise affects loud call structures and emission patterns
of wild black-fronted titi monkeys
M. H. L. Duarte
1,2
•M. C. Kaizer
1,3
•R. J. Young
3
•M. Rodrigues
2
•
R. S. Sousa-Lima
4
Received: 20 April 2016 / Accepted: 15 August 2017
ÓJapan Monkey Centre and Springer Japan KK 2017
Abstract Anthropogenic noise pollution is increasing and
can constrain acoustic communication in animals. Our aim
was to investigate if the acoustic parameters of loud calls
and their diurnal pattern in the black-fronted titi monkey
(Callicebus nigrifrons) are affected by noise produced by
mining activity in a fragment of Atlantic Forest in Brazil.
We installed two passive acoustic monitoring devices to
record sound 24 h/day, 7 days every 2 months, for a year;
one unit was close to an opencast mine and the other
2.5 km away from it. Both sites presented similar habitat
structures and were inhabited by groups of black-fronted
titi monkeys. We quantified the noise at both sites by
measuring the equivalent continuous sound level every 2
months for 1 year and quantified the emission of loud calls
by titi monkeys through visual inspection of the recordings.
The close site presented higher ambient noise levels than
the far site. The quantitative comparison of loud calls of
black-fronted titi monkeys between the two sites showed
less calling activity in the site close to the mine than in the
site further away. Approximately 20 % of the calls detected
at the site close to the mine were masked by noise from
truck traffic. Loud calls were longer at the site far from the
mine and the diurnal patterns of vocal activity differed in
the amount of calling as well as in the timing of peak
calling activity between the two sites. Our results indicate
that mining noise may constrain titi monkeys’ long-dis-
tance vocal communication. Loud calls occupy a similar
frequency band to mining noise, and an increase in ambient
noise may be triggering black-fronted titi monkeys to
adjust their long-distance communication patterns to avoid
masking of their calls. Given that vocalizations are an
important means of social interaction in this species, there
are concerns about the impact of mining noise on popula-
tions exposed to this human activity.
Keywords Animal communication Mining activity
Noise pollution Social behavior Sound masking
Introduction
Noise pollution is known to affect the physiology and
behavior of many animal species (Warren et al. 2006;
Kight and Swaddle 2011). Studies have shown that animals
avoid foraging in noisy areas (Schaub et al. 2008), increase
their vigilance in the presence of noise (Delaney et al.
&M. H. L. Duarte
marinabioacustica@hotmail.com
M. C. Kaizer
marikaizer@hotmail.com
R. J. Young
r.j.young@salford.ac.uk
R. S. Sousa-Lima
sousalima.renata@gmail.com
1
Conservation, Ecology and Animal Behaviour Group-
Laboratory of Bioacoustics, Post-Graduate Program in
Vertebrate Biology and Museum of Natural Sciences,
Pontifical Catholic University of Minas Gerais, Avenida Dom
Jose
´Gaspar, 290, Bairro Corac¸a
˜o Eucarı
´stico,
Belo Horizonte, Minas Gerais 30535-901, Brazil
2
Laboratory of Ornithology, Department of Zoology, Federal
University of Minas Gerais, Avenida Presidente Anto
ˆnio
Carlos, 6627, Bairro Pampulha, Belo Horizonte,
Minas Gerais 31270-901, Brazil
3
School of Environment and Life Sciences, Peel Building,
University of Salford Manchester, Salford M5 4WT, UK
4
Laboratory of Bioacoustics (LaB), Department of Physiology
and Behavior, Federal University of Rio Grande do Norte,
Avenida Senador Salgado Filho, 3000, Bairro Lagoa Nova,
Natal, RN 59078-970, Brazil
123
Primates
DOI 10.1007/s10329-017-0629-4
1999; Karp and Root 2009), select quiet areas to perform
their daily activities (Sousa-Lima and Clark 2009, Duarte
et al. 2011) and can be distracted by noise, all of which can
increase the risk of predation (Chan et al. 2010). Noise can
also cause physiological stress (Campo et al. 2005; Kight
and Swaddle 2011) and impact on ecological aspects of the
lives of animals such as population distribution (Reijen
et al. 1998; Bejder et al. 2006), species abundance (Bayne
et al. 2008) and diversity (Proppe et al. 2013).
Acoustic communication is essential in the lives of
many species as they use such signals to exchange bio-
logically relevant information; for example, to recognize
reproductive partners (Brumm et al. 2009), to inform others
of their location and/or the type of predator (Chan et al.
2010;Ca
¨sar et al. 2012) and to defend resources (Zuber-
buehler et al. 1997). However, anthropogenic noise com-
monly impacts animal communication (Slabbekoorn and
Ripmeester 2008; Barber et al. 2009; Laiolo 2010). Noise
can interfere with the propagation and detection of signals
by masking animal sounds and thus, prevent effective
communication (Foote et al. 2004; Bee and Swanson
2007). Nonetheless, many studies have documented that
animals use a range of vocal adjustments to minimize the
immediate impact of noise on communication systems.
These adjustments include: frequency shifts (Slabbekoorn
and Peet 2003; Parks et al. 2007; Nemeth and Brumm
2009), changes in amplitude (Brumm 2004; Brumm et al.
2009; Hage et al. 2013), calling rate (Sun and Narins 2005),
number of notes (Slabbekoorn and Boer-Visser 2006),
timing (Fuller et al. 2007), and duration of calls (Brumm
et al. 2004). The direct impact of noise on animal beha-
viour and ecology, and incidental costs of maintaining an
efficient communication system through compensatory
mechanisms, can impose fitness costs on affected individ-
uals (senders and receivers) and consequently on their
survival and reproduction (Chan et al. 2010; Schroeder
et al. 2012), and lead to population and community-level
changes (Parks et al. 2007; Duarte et al. 2015).
Besides the effects of deforestation caused by mining,
one less obvious impact on wildlife is the noise it produces
(Alvarez-Berrı
´os and Aide 2015; Duarte et al. 2015). The
effects of noise on primates that rely on acoustic commu-
nication need to be better studied to understand its impact
and to raise the awareness of stakeholders to mitigate its
potentially deleterious effects.
Many of the forests inhabited by primates in South
America suffer from large-scale mining (Estrada 2009).
The black-fronted titi monkey (Callicebus nigrifrons)is
one of the primates affected by these activities. Black-
fronted titi monkey are endemic to Atlantic Forest and
classified as Near Threatened on the International Union
for Conservation of Nature’s Red List (Veiga et al. 2008).
Titi monkeys are socially monogamous and exchange loud
calls (as duets or chorus) to either defend territories or food
resources in their home ranges and, probably, for mate
defense. Thus, these vocalizations are important regulators
of their social behaviour (Robinson 1979; Caselli et al.
2014). Coordinated loud calls are typically emitted at
dawn, but also during the day when another group is
sighted or heard (Kinzey et al. 1977; Kinzey and Robinson
1983; Melo and Mendes 2000). For black-fronted titi
monkeys, loud calls are emitted more often from their core
area or near to important food resources in their home
range (Caselli and Setz 2011; Caselli et al. 2014; Santos
et al. 2012; Santos 2012).
Loud calls of black-fronted titi monkeys are character-
ized by different vocal units including components that
range from near 1 to 12 kHz, and with a low frequency
near to 1 kHz (Caselli et al. 2014). Due to the spectral
characteristics of loud calls of titi monkeys, such as high
amplitude and low frequency, they can be heard over long
distances (Melo and Mendes 2000; Caselli et al. 2014).
Unfortunately, the same acoustic characteristics that are
adaptive for long-distance communication mean that these
calls have to compete with mining noise. In this study, we
investigated how the noise produced by one of the largest
opencast mines in the world affects the acoustic commu-
nication of a population of C. nigrifrons in an Atlantic
Forest fragment in southeast Brazil. We tested whether the
emission rate, duration and diurnal pattern of loud calls
would change between the areas exposed to different
ambient noise levels: one area close to an opencast mine
and one further away. Considering that animals would try
to optimize communication among neighboring groups by
minimizing the temporal overlap of their calls with noise
resulting from the mining activity, we predicted that titi
monkeys living in the fragment close to the mine would:
(1) reduce their call emission rate, (2) decrease the mean
call duration, and (3) alter the timing of their natural
diurnal calling pattern to avoid masking when noise from
the mine was most prevalent.
Methods
Study area
This study was conducted at Peti Environmental Station,
which is located in an Atlantic Forest fragment of
approximately 605 ha. The reserve is located in the upper
Rio Doce Basin (altitude range 630–806 m) in the
municipalities of Sa
˜o Gonc¸alo do Rio Abaixo and Santa
Ba
´rbara, Minas Gerais State, Brazil (19°5305700 S and
43°2200700W), one of the most fragmented Atlantic Forest
regions of Brazil (Machado and Fonseca 2000). Peti
Environmental Station harbors approximately 46 species of
Primates
123
mammals (Paglia et al. 2005), 231 species of birds (Faria
et al. 2006) and 29 species of anurans (Bertoluci et al.
2009). The climate is moderately humid subtropical, with
an average annual temperature of 21.7 °C (Paglia et al.
2005). The rainfall patterns are strongly seasonal with
110-mm mean rainfall, mean temperature of 23.9 °C and
61.9% humidity in the rainy season (October–March), and
with a dry season from April to September with 13-mm
mean rainfall, mean temperature of 18 °C and 58.1%
humidity.
A large part of the reserve is covered by secondary
arboreal vegetation, and is surrounded by a matrix mainly
composed of Eucalyptus, small cattle farms and areas of
exposed soil due to the activities of the Brucutu mine.
Mining activity occupies an area of approximately 8 km
2
and produces noise through road traffic, heavy machinery,
sirens and explosions during the day and night (Roberto
2010).
Data collection
One autonomous sound recorder (Song Meter SM2;
Wildlife Acoustics) was installed at two points inside the
protected area, each point located inside the home ranges
of two different groups of titi monkeys. One of these
groups inhabited a forest fragment with an area of 81 ha
close to an opencast iron mine (close site). The song meter
at this site was installed at a distance of 100 m from the
road that provided access to the mine (Fig. 1). The other
focal group inhabited a 84-ha forest fragment 2500 m away
from the mine (far site). In order to control for a potential
border effect, the song meter at this site was installed
100 m away from a low traffic road.
The average home range for black-fronted titi monkeys
is around 20 ha (Santos et al. 2012; Santos 2012; Caselli
et al. 2014), and the species shows site fidelity (Bicca-
Marques and Heymann 2013). Although the density of titi
monkeys in each site was unknown, other localities of
similar size have population densities ranging from 2.3 to
7.5 groups/km
2
(Gestich et al. 2016). There are geographic
barriers (roads and a river) that probably isolated these two
monkey groups, which inhabited similar forest fragments.
Both fragments are of similar size, floristic composition
and habitat structure, so we assume that the acoustic range
of titi monkey calls in both is the same.
The loud calls of titi monkeys can be detected up to
500 m away, with a critical distance of about 250–350 m
(Robinson 1981). The passive acoustic monitoring devices
were programmed to record for 7 days every 2 months
from October 2012 to August 2013, comprising six ses-
sions and totaling 1092 h of recordings (two sites 9six
sessions 913 h covering the animals’ active period from
0500 to 1800 hours 97 days). Each SM2 was fixed to a
tree 1.5 m above the ground, leaving the two lateral
microphones free from interference from any obstacle to
incoming sound waves. They were configured to record in
.WAV format at a sampling rate of 44,100 Hz, at 16 bits,
and with a 36% microphone gain. This configuration has
been recommended for optimal recordings of soundscapes
in the Atlantic Forest (Pieretti et al. 2015) and covers the
frequency range of Callicebus calls.
Fig. 1 Satellite images showing the two sites close to and far from the Brucutu mine (brown and grey area) at Peti Environmental Station,
southeast Brazil. Red lines represent the geographic barriers surrounding each site
Primates
123
In order to infer the level of noise exposure, the ambient
sound pressure levels (equivalent continuous sound level)
were measured on the A curve using a B&K2270 (Den-
mark) sound level meter. The sound pressure level mea-
surements were calculated based on 20-min intervals
randomly spaced between 0600 and 1800 hours, at both
sites simultaneously, on week days, once every 2 months,
for 10 months.
The truck traffic noise in the mine area was very intense,
occupying 70% of the frequency bandwidth recorded
(0–22 kHz) and 16% of the daytime (Duarte et al. 2015).
This important source of sound pollution varies over the
day with intervals of lower noise levels (Vargas-Salinas
et al. 2014). To quantify the disturbance from truck traffic,
we counted all instances of noise generated by passing
trucks from 0500 to 1800 hours on the road in front of the
site close to the mine. Hourly counts were done by audio
and visual identification of the trucks’ broadband pattern in
spectrograms (fast Fourier transform 1024 points, filter
bandwidth 135 Hz; frequency resolution, 93.8 Hz; grid
time resolution 2.13 ms) generated in Raven Pro 1.5
(Cornell Lab of Ornithology, Ithaca, NY). Statistical
analyses were performed in Statistica version 8.0 with a
significance level of 0.05.
This research adhered to the Brazilian legal require-
ments for field research (permit 034/2012) and to the
American Society of Primatologists Principles for the
Ethical Treatment of non-Human Primates.
Data analyses
The sound pressure level measurements were analyzed by
using BZ 5503 software. In order to avoid bias in the
measured sound pressure levels we excluded all recordings
in which we verified high received levels of animal sounds.
A Mann–Whitney U-test was used to verify if there was a
significant difference in the ambient noise pressure levels
between the sites.
We used three parameters to characterize the titi mon-
keys’ vocal behaviour between the sites: call emission rate,
call duration, and diurnal calling pattern. These parameters
were chosen based on previous studies on the effects of
anthropogenic noise on other species (Brumm et al. 2004;
Sun and Narins 2005). Loud calls emission rates of black-
fronted titi monkeys were calculated based on manual,
individual call detections per hour on spectrograms gen-
erated in Raven Pro 1.5 software (Cornell Lab of
Ornithology). Call durations were extracted using the delta
time measurement in the same software. The diurnal pat-
tern of titi monkeys’ vocal behaviour in each site was
determined from the temporal distribution of the number of
loud calls emitted from 0500 to 1800 hours and plotted
using the software Oriana (Kovach Computing Services,
Anglesey, UK) for circular data.
We used a v
2
-test to compare the observed rates of loud
calls of black-fronted titi monkeys in the close site and the far
site, considering the same expected frequency. We per-
formed a Mann–Whitney U-test to evaluate if there were
significant differences in loud call durations between the two
sites. A Friedman test was used to verify if there were dif-
ferences in calling rate between the hours of the day.
Results
Equivalent ambient sound levels (noise) were significantly
louder at the site close to the mine (Mann–Whitney U-test,
U=1, Z=2.72, n=6, P\0.01) (Table 1). Black-fron-
ted titi monkeys emitted more loud calls than expected at the
site far from the mine and less than expected at the close site
(X
2
-test, X
2
=339.96, df =1, P\0.001,n
close
=187,
n
far
=752). A considerable part (20.32%) of the vocalisa-
tions in the site close to the mine were partially masked by
noise from mining activity; however, visual and aural
inspection of the spectrograms still allowed for the detection
and identification of calls (Fig. 2b).
Loud calls were significantly longer at the site far from the
mine (Mann–Whitney U-test, U=29142.5, Z=12.40,
n
close
=187, n
far
=752, P\0.01; median
close
=1.77 s,
median
far
=16.33 s). The temporal distribution pattern of
the vocalisations was also different between the two sites
(Fig. 3). There were significant differences in calling rate
among the hours of the day in both sites, but not for truck
traffic events (Friedman test, X
2
=42.259, df =13,
P\0.001, n
far
=6; X
2
=40.915, df =13, P\0.001,
n
close
=6; X
2
=13.096, df =12, P=0.362, n
truck
=6).
At the site far from the mine, titi monkeys were more vocally
active early in the morning (0600–1000 hours), while at the
site close to the mine their vocal activity was very low, and
even lower after 1400 hours, which coincided with one of the
peaks in truck traffic at that site (Fig. 3). The period of higher
Table 1 Sound pressure levels (equivalent continuous sound level;
Leq) at sites close to and far from an opencast mine near Peti Envi-
ronmental Station, southeast Brazil
Measurement Close
Leq dB(A)
Far
Leq dB(A)
1 42.6 33.8
2 38.7 30.3
3 42.0 30.1
4 60.9 37.2
5 42.9 38.8
6 41.2 33.3
Primates
123
emission of loud calls at the site far from the mine (quieter
site) coincided with one of the peaks in truck traffic at the site
close to the mine (0700 hours) (Fig. 3).
Discussion
Our results show that titi monkey vocal activity is lower
and calls are shorter at the site close to the mine where
ambient noise levels are higher. Diurnal calling distribution
is also different between the two sites, with early morning
peak calling activity at the far site and no such peak at the
site close to the mine.
The higher rate of loud calls found at the site far from the
mine could be explained by several non-exclusive hypotheses:
1. More titi monkey groups are present at the far site.
2. There are more encounters between titi groups at the
site far from the mine.
3. Titi monkeys from the site close to the mine may
reduce their vocal emission rate due to noise.
4. Masking may decrease the detection of vocal activity
at the site close to the mine.
Fig. 2a, b Sound spectrograms of loud calls of black-fronted titi
monkeys at Peti Environmental Station southeast Brazil. aHigh-
quality, non-masked calls, at the site far away from the mine; bloud
calls partially masked by the noise of mining activities. Spectrograms
were generated using Raven Pro 1.5 with a fast Fourier transform of
1024 points, filter bandwidth 135 Hz, frequency resolution 93.8 Hz
and grid time resolution 2.13 ms
Primates
123
Opportunistic observations of titi monkey groups were
common in both sites during this study. During these non-
systematic observations, we identified similar numbers of
groups and individuals at both sites, which suggests that
hypotheses 1 and 2 are less likely. Habitat type and area
were similar, and while there were probably some differ-
ences between the sites, these were unlikely to affect the
rate of loud calls. A decrease in animal call rate in the
presence of increased ambient noise has already been
established for anurans and other mammals, and interpreted
as a response to avoid interference from anthropogenic
noise (Miksis-Olds and Tyack 2009; Sun and Narins 2005;
Parks et al. 2007; Sousa-Lima and Clark 2008).
Additionally, at the site close to the mine, many loud calls
(20%) were partially masked by noise, thereby supporting
hypotheses 3 and 4 which suggest that increased noise levels
may prevent titi monkeys from communicating effectively
(Lohr et al. 2003; Foote et al. 2004; Bee and Swanson 2007).
One particularly important factor driving vocalization effort
is the range over which the signaler and receiver must
effectively communicate (Miksis-Olds and Tyack 2009). In
this context, when noise masks vocalisations there is a
decrease in the acoustic space over which the information
can spread.
Longer calls emitted at the site far from the mine were in
accordance with our original prediction (2). In contrast,
common marmosets Callithrix jacchus increase the dura-
tion and amplitude of their calls as noise levels rise
(Brumm et al. 2004). This difference in response to
increased noise level might be related to the temporal
distribution of the noise. Adjusting vocal behaviour to
shorter calls during exposure to broadband noise that
occupies a significant spectral band, but is not continuous
in time (providing short windows of opportunity to call),
may decrease the probability of masking (Leo
´n et al. 2014;
Slabbekoorn and den Boer-Visser 2006). Our results sug-
gest that there is more available acoustic space at the far
site, especially in the lower frequencies, which are natu-
rally used by titi monkeys. At the close site, noise from the
mine overlapped with the titi monkeys’ loud calls and
could have been excluding them from an acoustic niche.
Thus, the monkeys are probably emitting calls of shorter
duration to communicate more effectively and/or to save
energy, since acoustic communication is energetically
00:00
06:00
12:00
18:00
250 250
250
250
200 200
200
200
150 150
150
150
100 100
100
100
50 50
50
50
truck
far
close
Fig. 3 Diurnal distribution of
the mean number of loud calls
emitted by black-fronted titi
monkeys at both sites (one close
to and the other far away from
the mine) as well as the mean
number of truck noise events
recorded by the song meters at
the site close to the mine near
Peti Environmental Station,
southeast Brazil
Primates
123
expensive and vocalization effort is increased by increasing
call duration (Miksis-Olds and Tyack 2008).
The difference in the diurnal pattern of loud calls
between the two sites can also be a consequence of the
mining noise disturbance on titi monkeys’ vocal behaviour.
As observed in other primate species such as indris
(Geissmann and Mu
¨tschler 2006) and gibbons (Mitani
1985), titi monkeys were vocally active mainly during the
first hours of the day (outside of intraspecific encounters)
(Melo and Mendes 2000; Caselli et al. 2014). These pri-
mates may concentrate the emission of loud calls in the first
hours of the morning when humidity is higher and tem-
perature lower and transmission of sound is presumed to be
more efficient (Mitani 1985; Wiley and Richards 1978). In
our study, this expected natural pattern of peak calling
activity in the early morning was observed only at the far
site. At the site close to the mine, truck traffic noise was
present at all hours of the day. In fact, at the close site we
observed a very low vocal activity throughout the entire
day apart from more calling around 1300 hours (Fig. 3).
Many mammals affected by anthropogenic noise have
limited developmental capacity to change the acoustic
parameters of their calls to avoid masking by other noise,
as seen in some birds (Weiss et al. 2014). However,
mammals may avoid the impact of noise with other
behavioral modifications, such as vocalizing during periods
of low noise (Rabin et al. 2003; Sousa-Lima and Clark
2008) or moving to quieter areas (Duarte et al. 2011).
Loud vocalisations are key signals involved in the reg-
ulation of titi monkey social behavior (Caselli et al. 2014).
One consequence of masking such calls can be increased
territory invasion by neighboring groups and, conse-
quently, increased rates of intergroup agonistic encounters.
Such changes could impact on the survival and reproduc-
tive success of the affected individuals, and result in dis-
ruption with potential population-level consequences. In
addition, studies with birds show that species that use low
frequency calls are more likely to avoid roads than those
that emit calls at higher frequencies, indicating how noise
may change the organization of avian communities
(Rheindt 2003; Francis et al. 2009). Considering there is a
similar spectral overlap between truck noise and loud calls
of titi monkeys, the avoidance of areas affected by truck
traffic noise by the monkeys may prevent their use of
suitable habitat. The black-fronted titi monkey is a Near
Threatened primate endemic to Atlantic Forest (Veiga et al.
2008) and if avoidance of suitable habitat occurs because
of noise disturbance this is of concern for this species’
conservation in the long term.
It would be interesting to investigate the natural
diurnal patterns and acoustic parameters of titi monkeys
in a gradient away from the noise source to investigate
other effects due to exposure to different noise levels.
The identification of noise levels that have decreased
disturbance effects would aid in the development of
regulations on distance between mining areas and nearby
natural areas. We have shown for the first time how
noise disturbance can affect black-fronted titi monkey
communication. We also highlight the importance of
considering noise pollution when creating reserves close
to areas with human activity (Madliger 2012). Brucutu’s
iron ore extraction started in 1992 and expansion com-
menced in 2004 to increase capacity to make it one of
the largest opencast mines in the world (Roberto 2010).
We suggest that acoustic monitoring of the mine and the
wildlife in this area should be part of the licensing
process of this mine, and should also be applied to all
other large-scale mining initiatives.
Acknowledgements We thank all the staff at the Peti Environmental
Station, especially Leotacı
´lio da Fonseca. We are also grateful to
Luane Ferreira for help with the analyses and figures, Marina Scar-
pelli and Renan Duarte for their help during data acquisition, and
engineer Krisdany Cavalcante for help with the noise measurements.
We are grateful to Martin Fisher and two anonymous reviewers for
comments on the manuscript. M. H. L. D. and M. C. K. were sup-
ported by CAPES (PNPD) and the Fundac¸a
˜o de Amparo a
`Pesquisa
de Minas Gerais (FAPEMIG/VALE). M. R., R. J. Y. and R. S. L.
received financial support from FAPEMIG/VALE and the Conselho
Nacional de Pesquisa (CNPq).
References
Alvarez-Berrı
´os NL, Aide TM (2015) Global demand for gold is
another threat for tropical forests. Environ Res Lett 10
Barber JR, Crooks KR, Fristrup KM (2009) The costs of chronic noise
exposure for terrestrial organisms. Trends Ecol Evol 25:180–189
Bayne EM, Habib L, Boutin S (2008) Impacts of chronic anthro-
pogenic noise from energy-sector activity on abundance of
songbirds in the boreal forest. Conserv Biol 22:1186–1193
Bee MA, Swanson EM (2007) Auditory masking of anuran adver-
tisement calls by road traffic noise. Anim Behav 74:1765–1776
Bejder L, Samuels A, Whitehead H, Gales N (2006) Interpreting
short-term behavioural responses to disturbance within a longi-
tudinal perspective. Anim Behav 72:1149–1158
Bertoluci J, Canelas MAS, Eisemberg CC, de Palmuti CFS,
Montingelli GG (2009) Herpetofauna of Estac¸a
˜o Ambiental de
Peti, an Atlantic Rainforest fragment of Minas Gerais State,
southeastern Brazil. Bio Neotrop 9:147–155
Brumm H (2004) The impact of environmental noise on song
amplitude in a territorial bird. J Anim Ecol 73:434–440
Brumm H, Voss K, Ko
¨llmer I, Todt D (2004) Acoustic communi-
cation in noise: regulation of call characteristics in a New World
monkey. J Exp Biol 207:443–448
Brumm H, Schmidt R, Schrader L (2009) Noise-dependent vocal
plasticity in domestic fowl. Anim Behav 78:741–746
Campo JL, Gil MG, Da
´vila SG (2005) Effects of specific noise and
music stimuli on stress and fear levels of laying hens of several
breeds. Appl Anim Behav Sci 91:75–84
Ca
¨sar C, Byrne R, Young RJ, Zuberbu
¨hler K (2012) The alarm call
system of wild black-fronted titi monkeys, Callicebus nigrifrons.
Behav Ecol Sociobiol 66:653–667
Primates
123
Caselli CB, Setz EZF (2011) Feeding ecology and activity pattern of
black-fronted titi monkeys (Callicebus nigrifrons) in a semide-
ciduous tropical forest of southern Brazil. Primates 52:351
Caselli CB, Mennill DJ, Bicca-Marques JC, Setz EZF (2014) Vocal
behavior of black-fronted titi monkeys (Callicebus nigrifrons):
acoustic properties and behavioral contexts of loud calls. Am J
Primatol 76:788–800
Chan AAY-H, Giraldo-Perez P, Smith S, Blumstein DT (2010)
Anthropogenic noise affects risk assessment and attention: the
distracted prey hypothesis. Biol Lett 6:458–461
Delaney DK, Gurbb TG, Seibr P, Pater LL, Reiser MH (1999) Effects
of helicopter noise on Mexican spotted owls. J Wildl Manage
63:60–76
Duarte MHL, Vecci MA, Hirsch A, Young RJ (2011) Noisy human
neighbours affect where urban monkeys live. Biol Lett 7:840–842
Duarte MHL, Sousa-Lima RS, Young RJ, Farina A, Vasconcelos M,
Rodrigues M, Pieretti N (2015) The impact of noise from
opencast mining on Atlantic Forest biophony. Biol Conserv
191:623–631
Estrada A (2009) Primate conservation in South America: the human
and ecological dimensions of the problem. In: Garber PA,
Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds)
South American primates. Springer, New York, pp 463–505
Faria CM, Rodrigues M, do Amaral FQ, Mo
´dena E
´(2006) Aves de
um fragmento de Mata Atla
ˆntica no alto Rio Doce, Minas
Gerais: colonizac¸a
˜o e extinc¸a
˜o. Rev Bras Zool 23:1217–1230
Foote AD, Osborne RW, Hoelzel AR (2004) Whale-call response to
masking boat noise. Nature 428:910
Francis CD, Ortega CP, Cruz A (2009) Noise pollution changes avian
communities and species interactions. Curr Biol 19:1415–1419
Fuller RA, Warren PH, Gaston KJ (2007) Day time noise predicts
nocturnal singing in urban robins. Biol Lett 3:368–370
Geissmann T, Mu
¨tschler T (2006) Diurnal distribution of loud calls in
sympatric wild indri (Indri indri) and ruffed lemurs (Varecia
variegata): implications for call functions. Primates 47:393–396
Gestich CC, Caselli CB, Nagy-Reis MB, Setz EZF, da Cunha RGT
(2016) Estimating primate population densities: the systematic
use of playbacks along transects in population surveys. Am J
Primatol 9999:1–9
Hage SR, Jiang T, Berquist SW, Feng J, Metzner W (2013) Ambient
noise induces independent shifts in call frequency and amplitude
within the Lombard effect in echolocating bats. Proc Natl Acad
Sci USA 110:4063–4068
Bicca-Marques JC, Heymann EW (2013) Ecology and behavior of titi
monkeys (genus Callicebus). In: Veiga LM, Barnett AA, Ferrari SF,
Norconk MA (eds) Evolutionary biology and conservation of titis,
sakis, and uacaris. Cambridge University, Cambridge, pp 196–207
Karp DS, Root TL (2009) Sound the stressor: how hoatzins
(Opisthocomus hoazin) react to ecotourist conversation. Biodiv
Conserv 18:3733–3742
Kight CR, Swaddle JP (2011) How and why environmental noise
impacts animals: an integrative, mechanistic review: environ-
mental noise and animals. Ecol Lett 14:1052–1061
Kinzey WG, Robinson JG (1983) Intergroup loud calls, range size,
and spacing in Callicebus torquatus. Am J Phys Anthropol
60:539–544
Kinzey WG, Rosenberger AL, Heisler PS, Prowse DL, Trilling JS
(1977) A preliminary field investigation of the yellow handed titi
monkey, Callicebus torquatus torquatus, in northern Peru.
Primates 18:159–181
Laiolo P (2010) The merging significance of bioacoustics in animal
species conservation. Biol Conserv 143:1635–1645
Leo
´n E, Beltzer A, Quiroga M (2014) El jilguero dorado (Sicalis
flaveola) modifica la estructura de sus vocalizaciones para
adaptar se a ha
´bitats urbanos. Rev Mex Biod 85:546–552
Lohr B, Wright TF, Dooling RJ (2003) Detection and discrimination
of natural calls in masking noise by birds: estimating the active
space signal. Anim Behav 65:763–777
Machado RB, Fonseca GAB (2000) The avifauna of Rio Doce Valley,
southeastern Brazil, a highly fragmented area. Biotropica
32:914–924
Madliger CL (2012) Toward improved conservation management: a
consideration of sensory ecology. Biodivers Conserv
21:3277–3286
Melo FR, Mendes SL (2000) Emissa
˜o de gritos longos por grupos de
Callicebus nigrifrons e suas reac¸o
˜es a playbacks. In: Alonso C,
Langgut A (eds) A Primatologia no Brasil—7. Sociedade
Brasileira de Primatologia and Editora Universita
´ria, Joa
˜o
Pessoa, pp 215–222
Miksis-Olds JL, Tyack PL (2009) Manatee (Thichechus manatus)
vocalization usage in relation to environmental noise levels.
J Acoust Soc Am 125:1806–1815
Mitani JC (1985) Gibbon song duets and intergroup spacing.
Behaviour 92:59–96
Nemeth E, Brumm H (2009) Blackbirds sing higher-pitched songs in
cities: adaptation to habitat acoustics or side-effect of urbaniza-
tion? Anim Behav 78:637–641
Paglia AP, Lopes MOG, Perini FA, Cunha HM (2005) Mammals of
the Estac¸a
˜o de Preservac¸a
˜o e Desenvolvimento Ambiental de
Peti (EPDA-Peti), Sa
˜o Gonc¸alo do Rio Abaixo, Minas Gerais,
Brazil. Lundiana 6:89–96
Parks ES, Clark CW, Tyack PL (2007) Short-and long-term changes
in right whale calling behavior: the potential effects of noise on
acoustic communication. J Acoust Soc Am 122:3725–3731
Pieretti N, Duarte MHL, Sousa-Lima RS, Young RJ, Rodrigues M,
Farina A (2015) Determining temporal sampling schemes for
passive acoustic studies in different tropical environments. Trop
Conserv Sci 8:215–234
Proppe DS, Sturdy CB, St Clair CC (2013) Anthropogenic noise
decreases urban songbird diversity and may contribute to
homogenization. Glob Chang Biol 19:1075–1084
Rabin LA, McCowan B, Hooper SL, Owings DH (2003) Anthro-
pogenic noise and its effect on animal communication: an
interface between comparative psychology and conservation
biology. Int J Psychol 16:172–192
Reijen R, Foppen R, Braak CT, Thissen J (1998) The effects of car
traffic and breeding bird populations in woodland. III. Reduction
of density in relation to the proximity of main roads. J Appl Ecol
32:187–202
Rheindt FE (2003) The impact of roads on birds: does song frequency
play a role in determining susceptibility to noise pollution?
J Ornithol 144:295–306
Roberto JB (2010) Influe
ˆncia dos diversos tipos litolo
´gicos nas
operac¸o
˜es de concentrac¸a
˜o da instalac¸a
˜o de beneficiamento de
Brucutu. Master’s dissertation, Universidade Federal de Minas
Gerais (available at http://www.bibliotecadigital.ufmg.br/
dspace/handle/1843/BUOS-8DJFVY)
Robinson JG (1979) Vocal regulation of use of space by groups of titi
monkeys Callicebus moloch. Behav Ecol Sociobiol 5:1–15
Robinson JG (1981) Vocal regulation of inter- and intra-group
spacing during boundary encounters in the titi monkey, Callice-
bus moloch. Primates 22:161–172
Santos RV (2012) A
´rea de vida e uso do espac¸o por Callicebus
nigrifrons Spix, 1823 (Primates: Pitheciidae). Master’s disserta-
tion, Pontifı
´cia Universidade Cato
´lica de Minas Gerais
Santos GP, Galva
˜o C, Young RJ (2012) The diet of wild black-fronted
titi monkeys Callicebus nigrifrons during a bamboo masting
year. Primates 53:265–272
Schaub A, Ostwald J, Siemers BM (2008) Foraging bats avoid noise.
J Exp Biol 211:3174–3180
Primates
123
Schroeder J, Nakagawa S, Cleasby IR, Burke T (2012) Passerine birds
breeding under chronic noise experience reduced fitness. PLoS
One 7
Slabbekoorn H, den Boer-Visser A (2006) Cities change the songs of
birds. Curr Biol 16:2326–2331
Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban
noise. Nature 424:267
Slabbekoorn H, Ripmeester EA (2008) Birdsong and anthropogenic
noise: implications and applications for conservation. Mol Ecol
17:72–83
Sousa-Lima R, Clark C (2008) Modeling the effect of boat traffic on
the fluctuation of humpback whale singing activity in the
Abrolhos National Park, Brazil. Can Acoust 36:174–181
Sousa-Lima RS, Clark CW (2009) Whale sound recording technology
as a tool for assessing the effects of boat noise in a Brazilian
marine park. Park Sci 26:59
Sun JWC, Narins PM (2005) Anthropogenic sounds differentially
affect amphibian call rate. Biol Conserv 121:419–427
Vargas-Salinas GM, Cunnington A, Ame
´zquita L Fahrig (2014) Does
traffic noise alter calling time in frogs and toads? A case study of
anurans in eastern Ontario, Canada. Urban Ecosyst 17:945–953
Veiga LM, Kierulff CM, de Oliveira MM, Mendes SL (2008)
Callicebus nigrifrons. The IUCN Red List of threatened species
version 20143 http://www.iucnredlist.org. Accessed 17 Decem-
ber 2014
Warren PS, Katti M, Brazel Ermann M (2006) Urban bioacoustics:
it’s not just noise. Anim Behav 71:491–502
Weiss DJ, Hotchkin CF, Parks SE (2014) Modification of spectral
features by nonhuman primates. Behav Brain Sci 37:574–576
Wiley RH, Richards DG (1978) Physical constraints on acoustic
communication in the atmosphere: implications for the evolution
of animal vocalizations. Behav Ecol Soc 3:69–94
Zuberbuehler K, Noe R, Seyfarth RM (1997) Diana monkey long-
distance calls: messages for conspecifics and predators. Anim
Behav 53:589–604
Primates
123
