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Effects of anthropogenic noise on the acoustic behaviour of Sotalia guianensis (Van Bénéden, 1864) in Pipa, North-eastern Brazil

Authors:
  • Universidade Federal do Recôncavo da Bahia / Curtin Universtity

Abstract and Figures

This study investigated the emission of subaquatic noise from recreational tourism motorboats, schooners and a sea-bottom mounted water pump. Analyses demonstrated alterations in several whistle (IF: t = 2.42, P = 0.015; FF: t = −2.22, P = 0.025) and calls patterns (MIF: t = −3.13, P = 0.001; MAF: t = −3.49, P = 0.0005; FD: t = −2.21, P = 0.027; D: t = 2.89, P = 0.004), caused primarily by motorboats. Duration of clicks was also modified (D: t = −3.85, P = 0.0001), mainly by the water pump. The frequency range of all noises (0.43–35.8 kHz) overlaps that used by dolphins (1–48 kHz), causing sound emissions changes, with a considerable increase in number of whistles and a reduction in clicks trains. These changes may be a strategy developed by these dolphins to overcome the noise band. Mitigation measures, such as boating regulations and environmental education for the local community, boaters and tourists are needed to conserve the species. The Guiana dolphin population is apparently already suffering, evidenced by diminished residence time and reduced number of individuals entering the inlet during the presence of pleasure craft.
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Effects of anthropogenic noise on the
acoustic behaviour of Sotalia guianensis (Van
Be
´ne
´den, 1864) in Pipa, North-eastern Brazil
dalila t. lea
~o martins
1
, marcos r. rossi-santos
1,2
and fla
vio jose
de lima silva
1,3
1
Programa de Po
´s Graduac¸a
˜o em Psicobiologia, Departamento de Fisiologia, Universidade Federal do Rio Grande do Norte, Campus
Universita
´rio Lagoa Nova, Natal, Rio Grande do Norte, Brazil,
2
Laborato
´rio de Ecologia Acu
´stica e Comportamento Animal, Centro
de Cie
ˆncias Agra
´rias, Ambientais e Biolo
´gicas. Universidade Federal do Reco
ˆncavo da Bahia, Campus Cruz das Almas, Bahia, Brazil,
3
Departamento de Turismo, Universidade do Estado do Rio Grande do Norte, Avenida Airton Senna, 4241, Neo
´polis Natal, Rio
Grande do Norte, Brazil
This study investigated the emission of subaquatic noise from recreational tourism motorboats, schooners and a sea-bottom
mounted water pump. Analyses demonstrated alterations in several whistle (IF: t¼2.42, P¼0.015; FF: t¼22.22, P¼
0.025) and calls patterns (MIF: t¼23.13, P¼0.001; MAF: t¼23.49, P¼0.0005; FD: t¼22.21, P¼0.027; D: t¼
2.89, P¼0.004), caused primarily by motorboats. Duration of clicks was also modified (D: t¼23.85, P¼0.0001),
mainly by the water pump. The frequency range of all noises (0.43– 35.8 kHz) overlaps that used by dolphins (1– 48 kHz),
causing sound emissions changes, with a considerable increase in number of whistles and a reduction in clicks trains.
These changes may be a strategy developed by these dolphins to overcome the noise band. Mitigation measures, such as
boating regulations and environmental education for the local community, boaters and tourists are needed to conserve
the species. The Guiana dolphin population is apparently already suffering, evidenced by diminished residence time and
reduced number of individuals entering the inlet during the presence of pleasure craft.
Keywords: vessel noise, North-eastern Brazil, Guiana dolphin, Sotalia guianensis, Pipa beach, acoustic behaviour
Submitted 4 August 2016; accepted 24 August 2016
INTRODUCTION
The disordered growth of the human population in coastal
areas, in addition to recreational, artisan and commercial
fishing (Wells et al., 1998), as well as ship and tourist boat
traffic has been increasing for decades and, consequently,
bringing impacts to marine life (Wells & Scott, 1997). In add-
ition to these processes, chemical and sound pollution have
reached increasingly higher levels, causing serious disturbance
and even damage, primarily to cetaceans that use hearing and
sound emission as their main means of communication and
environment exploration through biosonar (Ketten, 1992;
Richardson et al., 1995; Tyack, 2000; Hildebrand, 2009).
Hearing in cetaceans is one of the most important senses
and a good auditory apparatus is essential for the life of
species, especially for predation, sensing the environment
and social interactions (Ketten, 1992; Prideaux, 2003).
Decreased auditory sensitivity caused by physical damage or
masking noise compromises individuals and may subsequently
affect an entire population (Richardson et al., 1995; Prideaux,
2003). Using the acoustic impact assessment model, Erbe
(2002) showed that whale-watching boats interfere in killer
whale – Orcinus orca (Linnaeus, 1758) communications,
cause behavioural changes and may even generate temporary
or permanent hearing losses in resident populations.
Other studies demonstrated that behavioural and sound
emission changes can be due to the presence of watercraft.
Parijs & Corkeron (2001) observed that Indo-Pacific hump-
back dolphins Sousa chinensis (Osbeck, 1765) exhibit
an increase in number of whistles immediately after boats
pass through their habitats.
The Sotalia guianensis dolphin (family Delphinidae) is also
known as the Guiana dolphin. It is a small animal (mean of
1.80 m) that primarily inhabits estuaries, bays, inlets and
mangrove areas (Da Silva & Best 1996; Rosas et al.,2003).
Its worldwide distribution ranges along the Atlantic Ocean,
from Honduras, in Central America, to the state of Santa
Catarina, southern Brazil (Da Silva & Best, 1996; Flores &
Da Silva, 2009).
As a consequence of its coastal distribution, the species has
been constantly approached by dolphin-watching tourism
boats, and some studies have demonstrated the impact suf-
fered by this species on the Brazilian coast (Santos et al.,
2006; Rezende, 2008; Tosi & Ferreira, 2008). Santos et al.
(2006) report that boats approaching dolphins in Pipa
beach, Rio Grande do Norte state, may induce subtle behav-
ioural alterations, especially in regard to displacement. At
the same site, Tosi & Ferreira (2008) observed that approach-
ing boats had an influence on individuals, evidenced by the in-
crease in respiratory synchronism, reported as a defence
strategy against the presence of these vessels.
Corresponding author:
D.T. Lea
˜o Martins
Email: dalilaleao@gmail.com
1
Journal of the Marine Biological Association of the United Kingdom, page 1 of 8. #Marine Biological Association of the United Kingdom, 2016
doi:10.1017/S0025315416001338
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Filla & Monteiro-Filho (2009) found Guiana dolphins from
the region of Canane
´ia, Sa
˜o Paulo state react less negatively
the longer boats remain in the area, due to habituation.
However, boats approaching to within 50 m of dolphins
were responsible for most of the negative responses like
trying to withdraw from the boat and these were interpreted
as being a defence behaviour, through which the animals
seek protection, especially for the youngest, by moving far
away.
Because wildlife-watching tourism in Brazil is undergoing a
process of constant change, this study aims to propose pos-
sible solutions to mitigate and prevent disturbance and/or
damage inflicted on dolphins, thereby contributing to their
conservation, particularly in areas where Guiana dolphins
are a tourist attraction.
The present study seeks to characterize the frequency para-
meters produced by different tour boat motors in the area,
examine whether noises have an influence on the acoustic ex-
pression of dolphins and determine which anthropogenic
underwater noise has the greatest effect on the sounds
emitted by these animals.
This investigation tested the hypothesis that different
sound categories are emitted by dolphins in the presence
and absence of boats, and that these variations are influenced
by the type of noises present in the area.
MATERIALS AND METHODS
Study area
The study area consists of two inlets, Madeiro and Curral,
belonging to the district of Pipa in the municipality of Tibau
do Sul. It is located in the southernmost part of Rio Grande
do Norte state (0681323.9′′S3580414.8′′W), 90 km from
Natal, the state capital, North-eastern Brazil (Figure 1).
The inlets exhibited high water turbidity, since they are
high energy beaches, with constant movement of suspended
sediment. Both inlets are surrounded by cliffs with a mean
height of 30 m, protecting the region from winds and
coastal currents and resulting in a relatively stable area,
affected only by tides and rainfall (IDEMA, 2003).
Data collection
Dolphin and boat motor sounds were recorded on 11 collec-
tion days between April and June 2009. Sampling effort was
49 h 48 m with a daily mean of 4.5 h. The collections were
considered satisfactory when the weather conditions were ,
2 on the Beaufort scale.
Recordings were made from a 5-m fibreglass motorboat
equipped with a Mercury 60HP 4-stroke outboard motor.
Sounds were recorded using an HTI SSQ 94 hydrophone (fre-
quency response up to 24 kHz) positioned at a depth of 1.5 m
connected to a digital recorder (M-Audio Microtrack II,
Cumberland, RI) with 16 bits of precision at a sampling rate
of 96 kHz.
The boat initially approached at low speed and the engine
was turned off during recordings. Recording sessions took
place when dolphins were less than or equal to 100 m away,
concluding when individuals swam beyond that distance
and/or were no longer visible.
Recordings were initiated 2 h before commercial tours
began (around 8:00 h), extending until they were half com-
pleted (around 13:00 h) in order to determine the influence
of boat noise on sound emissions of dolphins present in the
area. On three days, recordings were also made after the end
of the tours, at 16:00 h. It was, therefore, possible to record
dolphin sound emissions without noise interference as well
as sounds and noises that occurred simultaneously.
Two motorboats were analysed: (motorboat one: Yamaha
115HP 2-stroke gasoline engine; motorboat two: Mercury
60HP 4-stroke gasoline engine) and two schooners (both
equipped with 6MWM D229 diesel engines), randomly
chosen as a sample of the boats used in the area. Data were
collected regarding the presence and type of vessel (schooner
or motorboat) in the area during recordings in order to com-
plement analyses on the influence of tour boats on dolphin
behaviour.
The three sound categories that are used in this study fol-
lowed Monteiro-Filho & Monteiro (2001).
Analysis
To analyse any acoustic signal it is important to consider time
and frequency. The time domain represents the amplitude as a
function of time and in the frequency domain, the amplitude
displayed as a function of frequency (Au & Hastings, 2008).
Because of this relevance this study analysed both domains,
such as previously applied to analysis of anthropogenic
sounds in the cetacean soundscape ecology in Brazilian
waters (Rossi-Santos, 2015). Time representation is a signal
usually referred to as the waveform, while the frequency re-
presentation of a signal is usually referred to as the frequency
spectrum (Au & Hastings, 2008).
Recordings were analysed with RAVEN PRO
w
1.4 soft-
ware. The following parameters were determined for each
boat: minimum frequency (MIF), maximum frequency
(MAF), frequency variation (FV). Parameters calculated
from sound emissions of dolphin calls were minimum fre-
quency (MIF), maximum frequency (MAF), frequency vari-
ation (FV) and duration (D), and for whistles the same
frequencies were measured in addition to initial frequency
(IF) and final frequency (FF). All the parameters were calcu-
lated considering the fundamental note.
Sauerland & Dehnhardt (1998) reported that the dominant
frequency for the species’ clicks is around 88 kHz. The
maximum frequency values for clicks trains in this study
always reached the maximum value of the recorder
(48 kHz); thus, this frequency parameter was not considered
in our analyses. Therefore, herein we utilized the minimum
frequency (MIF) and click train duration (D) as click para-
meters for analysis.
To examine whether boat noises influence dolphin sound
emissions, based on the means of each parameter, calculated
from sound classes in the presence and absence of noise a
Kolmogorov Smirnov normality test of the data and a
Mann Whitney analysis with 0.05 significance were con-
ducted for each parameter.
Kruskal Wallis was used to determine if the noise influ-
ence varies according to the type of producer (motorboat,
schooner and other noises), followed by a posteriori analysis
using comparisons between pairs to show which noise has
the greatest influence.
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~omartinset al.
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RESULTS
The total recording time was 18 h 49 m, consisting of 260 ses-
sions, 109 (42%) of which included the presence of boats. The
current dolphin-watching tourism boat fleet in Pipa consists
of six motorboats and four schooners making an average of
four and three trips daily, respectively. Including all commer-
cial tours, total tour time averages 6 h a day, 7 days a week,
enabling a total noise recording time of 6 h 20 m. The
median number of dolphins present during recordings was
three individuals (two adults and one infant).
The recorded boats emit sounds with a mean peak fre-
quency of around 10 kHz. However, noises produced, in add-
ition to fundamental sounds, also contain harmonics
(multiple values of the fundamental note), which reach
higher frequencies, reverberating in the acoustic environment.
Accordingly, the range used by the noises encompasses fre-
quencies between 0.42 and 15.3 kHz and if considering the re-
verberation the range reaches to 35.82 kHz.
During some recording sessions, generally conducted after
tourist activities ended, the presence of a different noise from
that produced by boats was recorded, exhibiting a narrow fre-
quency and little reverberation. This noise was identified as
originating from water tubes coming from the shore to a
building, these being a water suction pump located 2.5 km
away from our study site, installed underwater by the rocky
shore of a luxury hotel in the region. We then analysed and
described this new pattern of noise for the species along
with the boat noise description (Table 1).
Based on between-boat comparisons, it was observed that
variations in frequencies (including reverberation) emitted
by motorboats are greater than those emitted by schooners.
Furthermore, there are differences between types of outboard
engines, since motorboat 1 used a 2-stroke engine, exhibiting
higher means at all frequencies, whereas motorboat 2, which is
driven by a 4-stroke engine, displays lower mean frequencies
(Table 1).
Analysis of dolphin sounds generally demonstrated an
overlap of frequency ranges between noises and their sound
emissions, which ranged from 1 to 48 kHz, considering all
sound categories recorded. Spectrograms (Figures 2A, B)
show dolphin sound emission occurring simultaneously with
the noises and no noise.
For a better comparison of the influence of anthropogenic
noise on each sound emission class, the parameters calculated
were separated according to the absence and presence of noise
(Table 2).
There was a considerable increase in the number of whis-
tles during the presence of noise, from 1146 whistles in the
absence of noise to 2112 when it was present. However,
the number of click trains sequences decreased from 524 in
the absence of sounds and to 349 in the presence of noise.
There was no difference in the number of calls during the
presence (144) and absence (145) of sounds.
Fig. 1. Study area located at Pipa beach, municipality of Tibau do Sul, Rio Grande do Norte state, Brazil. (Map elaboration by Ana Alencar.)
Table 1. Mean values of parameters obtained from the acoustic noise pro-
duced by boats and a water pump in Pipa beach, Rio Grande do Norte,
Brazil. Frequency is in kHz.
MIF MAF FV
Motorboat 1 2.88 35.82 35.04
Motorboat 2 0.79 28.1 27.31
Schooner 1 0.42 25.71 25.28
Schooner 2 0.52 22.00 21.47
Water pump 1.84 8.14 6.30
MIF, Minimum Frequency; MAF, Maximum Frequency; FV, Frequency
Variation.
anthropogenic noise and dolphins in north-eastern brazil 3
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The Mann Whitney Utest showed the presence of noise
influenced the initial and final frequency parameters of whis-
tles (IF: U¼115434, P¼0.029; FF: U¼116027, P¼0.050);
however, it did not alter the remaining parameters (MIF: U¼
120295, P¼0.770; MAF: U¼120295, P¼0.350; FV: U¼
120871, P¼0.950; D: U¼117456, P¼0.160).
For click trains, the Mann Whitney only revealed differ-
ences between the presence and absence of noise in the para-
meters duration (D: U¼78403.50, P¼0.0001), without
altering all frequency parameters (MIF: U¼91218.00, P¼
0.950; MAF: U¼84492.50, P¼0.057; FV: U¼89733.50,
P¼0.640). In calls, all frequency and duration parameters
Fig. 2. Spectrogram of anthropogenic noise and dolphins’ sound emissions recorded at Pipa beach, Rio Grande do Norte, Brazil. (A) noise of a motorboat together
with whistles of dolphins. (B) whistles without anthropogenic noise.
Table 2. Mean, standard deviation and amplitude of the acoustic parameters of Sotalia guianensis whistles, calls and recorded during the absence and
presence of noise between the months April and June 2009, in Pipa beach in the state of Rio Grande do Norte, Brazil. Frequency is in kHz and durationin
seconds.
IF FF MIF MAF FV D
Whistle without noise 11.50 +5.02 18.80 +4.60 10.20 +3.76 19.50 +4.40 9.30 +0.10 0.19 +0.10
(0.9347.5) (3.20– 36.50) (0.70– 25.10) (3.2047.50) (1.3044.10) (0.02–2.66)
Whistle with noise 11.80 +4.69 19.10 +4.62 10.40 +4.01 19.60 +4.40 9.20 +4.76 0.20 +0.12
(0.9347.50) (1.3038.50) (0.9028.20) (5.2047.50) (0.30 44.40) (0.02–0.87)
U 115434 116027 120295 120295 120871 117456
P0.0290.0500.770 0.350 0.950 0.160
Calls without noise 7.10 +4.28 9.50 +4.59 2.45 +1.01 0.22 +0.14
(0.56– 16.90) (1.8019.60) (0.726.57) (0.04 1.09)
Calls with noise 8.70 +4.50 11.50 +4.64 2.70 +1.08 0.18 +0.09
(0.93– 19.80) (2.9023.20) (1.037.10) (0.03 0.65)
U 8259.00 8087.500 8785.000 8261.000
P – 0.0020.0000.0190.002
Clicks without noise 6.40 +3.04 1.75 +1.38
(1.00– 17.10) – (0.14– 10.27)
Clicks with noise 6.50 +3.23 2.18 +1.90
(1.10– 20.50) – (0.29– 15.70)
U 91218.00 – 78403.500
P 0.95 – 0.000
IF, initial frequency; FF, final frequency; MIF, minimum frequency; MAF, maximum frequency; FV, frequency variation; D, duration.
Significant values.
4dalilat.lea
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change in the presence of noise (MIF: U¼8259.00, P¼0.002;
MAF: U¼8087.50, P¼0.000; FV: U¼8785.00, P¼0.019;
D: U¼8261.00, P¼0.002).
The means of dolphin sound patterns in the presence of
motorboat, schooner and water pump noise were separated
in order to determine which of the three had more influence
on the three sound classes (Table 3). Water pump noise is
not present in analyses of calls, since they were not emitted
in the presence of this noise.
The Kruskal Wallis demonstrated that whistles exhibit
differences in IF and FF parameters for the different types
of noise (IF: H¼17.121, P¼0.000; FF: H¼11.527, P¼
0.003). The a posteriori showed the motorboat had the greatest
influence. Analyses of click trains revealed a difference
between types of noises in parameter D (D: H¼35.44704,
P¼0.000). The a posteriori for click trains parameters indi-
cated they were more influenced by the water pump (Table 3).
The Kruskal Wallis for calls showed no difference
between types of noise for MIF and MAF (MIF: H¼1.582,
P¼0.453; MAF: H¼0.404, P¼0.816; D: H¼2.517, P¼
0.280). However, a difference was recorded for frequency vari-
ation (FV: H¼9.722, P¼0.007). The a posteriori confirmed
the difference between the motorboat and schooner, the
former exerting the greatest influence (Table 3).
DISCUSSION
Dolphin-watching tourism has been growing steadily,
with positive and negative repercussions. If applied in a
well-organized operation it may promote an increase in envir-
onmental responsibility and generate income for local popula-
tions (Corkeron, 1995). However, when uncontrolled, these
activities may cause short- and long-term damage to the
animal populations of the region (Constantine, 2001).
Guiana dolphin watching in Pipa occurs daily and the boats
used for this activity generate significant sound pollution, since
they used a wide frequency range, considering the harmonics
and the reverberation of the noises produced. Reverberation
occurs when the difference in time between the emission and
the sound reflection is very short, enhancing sound propagation
in a certain acoustic enviroment (Rossing, 2007).
Between-boat comparisons demonstrated that the schoon-
ers, equipped with low rotation engines (centre of the boat),
seem to be less harmful than high rotation engines (stern)
when maximum noise frequency values are involved. The
4-stroke motorboat engine emits lower frequency ranges
than the 2-stroke version. A lower frequency range can
cause less impact because dolphins are able to adjust and
use higher frequencies and also depends on the hearing
curve that is less sensitive to lower frequencies.
The different frequency parameters recorded in the boats
under study confirm the findings of Au & Green (2000).
The authors believe the smaller boats produce sounds of
equal or greater intensity than large boats. This occurs
because the number of rotations per minute (RPM) required
by a high rotation engine with small propellers to overcome
thrust must be much greater than the RPM needed for
inboard motors with larger propellers. Thus, outboard
motors can generate more noise and possibly more injuries
to marine life. Moreover, wood hulls are excellent sound con-
ductors, preventing engine noise from being dissipated in the
water (Filla & Monteiro-Filho, 2009).
Signal parameters are influenced by the distance and orien-
tation of the vocalizing animal to the recording hydrophone.
Lower frequencies are less attenuated over distance than
Table 3. Means and standard deviation of parameters of three sound classes that were influenced by separate noises in presence of the water pump, the
boat and the schooner recorded between April and June 2009, in Pipa beach, Rio Grande do Norte, Brazil.
IF FF MIF MAF FV D
Whistle with water pump 11.26 +3.66 18.27 +4.18 10.59 +3.29 18.56 +3.91 7.97 +4.42 0.20 +0.12
(3.63– 21.79) (4.18 31.34) (3.29 19.87) (3.91 31.34) (1.01 23.59) (0.02– 2.66)
Whistle with motorboat 11.43 +4.74 19.22 +4.65 10.58 +4.02 19.72 +4.43 9.14 +4.80 0.19 +0.12
(1.13– 47.48) (2.87– 38.59) (1.13 28.17) (4.43 47.48) (1.61 44.40) (0.02– 0.87)
Whistle with schooner 10.59 +4.81 19.30 +4.67 9.98 +4.14 19.72 +4.45 9.72 +4.70 0.19 +0.12
(0.92– 37.24) (1.33 34.53) (0.92 24.60) (4.45 37.24) (2.63 30.62) (0.02– 0.87)
H 17.121 11.527 10.079 16.621 30.114 1.404
P0.0000.0310.060 0.055 0.053 0.490
Call with water pump – – – –
––
Call with motorboat 8.52 +4.38 11.40 +4.62 2.88 +1.14 0.18 +0.09
(0.92 19.83) (2.98 23.22) (1.02 7.09) (0.03– 0.65)
Call with schooner 9.54 +4.86 11.76 +4.77 2.22 +7.08 0.16 +0.08
(2.15 19.54) (4.77 22.09) (0.70 3.70) (0.05– 0.39)
H 1.582 0.404 9.722 2.517
P 0.453 0.816 0.0070.280
Click with water pump 8.84 +3.15 3.11 +1.88
(3.15 19.73) – (0.4709.14)
Click with motorboat 5.96 +3.23 2.17 +1.55
(1.43 20.55) – (0.3015.69)
Click with schooner 6.40 +2.62 1.67 +1.33
(1.0213.18) – (0.29 09.33)
H 38.602 – 35.447
P 0.08 – 0.000
Significant values.
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higher frequencies. The orientation of the animal to the record-
ing device changes the signal properties as well, as higher
overall amplitudes and more high frequency energy is expected
when the animal’s vocal beam is on axis with the recorder (Au,
1993). Signals obtained from random axis orientations may
have distorted asymmetric wave forms, which include rever-
berations caused by reflections within the head, from the exter-
nal environment or even both (Au et al.,1978).
Although we know that the number of harmonics in a
spectrogram is a whistle variable that is defined by whistle dir-
ectionality (Lammers & Au, 2003) and by the upper frequency
limit of the recording system, thus it is not the best variable to
be used when referring to the effects of anthropogenic noise
on the acoustic behaviour of animals, this was the tool we
had to start this study in this unique area for S. guianensis con-
servation. The results obtained when comparing values using
the number of harmonics seen in the spectrogram has little
biological relevance for dolphin studies and does not
provide a strong explanation for the noise interference. For
future studies we assume and recommend to remove this par-
ameter from the analysis so as not give so much emphasis on
the reverberation aspect. In this way, we plan to develop new
research efforts utilizing additional analysis with more robust
parameters, such as: Signals Intensity, Source Pressure Level,
Signal to Noise Ratio, Root Mean Squared, Peak-to-Peak
and Centre Frequency.
In contrast to the boats, the water pump exhibits a narrow
frequency range and no harmonics. Peak frequency noise is
around 2 kHz. We could observe that the water pump is
used to remove salt water from the sea to supply a hotel swim-
ming pool. It is generally turned on in the late afternoon, after
commercial tours, thereby increasing exposure of the dolphins
to anthropogenic noise.
Considering many associated factors can influence engine
noise including type and power, speed and boat building ma-
terial (Ng & Leung, 2003; Constantine et al.,2004; Filla &
Monteiro-Filho, 2009), dolphin-watching vessels in Pipa
beach exhibit characteristics that may harm dolphins in the
area, primarily when different engines are used, such as
2-stroke and 4-stroke versions and high power. Acoustic mon-
itoring is therefore needed to evaluate this damage.
A number of studies have revealed that dolphins seem to
respond to the presence of boats by emitting more whistles
(Parijs & Corkeron, 2001; Scarpaci et al., 2001). In the
present study, boat tours to observe Guiana dolphins in
their natural habitat in Pipa beach cause modifications in
their standard sound emissions. Similar to the bottlenose
dolphin, Tursiops truncatus (Montagu, 1821) (Scarpaci et al.,
2001), Guiana dolphins practically doubled whistle produc-
tion when boat noise occurred in the same area as the
individuals.
Frequency ranges of the boats in Pipa are generally similar
to those used by dolphins and the phenomenon of reverber-
ation caused by engine noise increases frequency overlap
even more. This overlap can generate masking, occurring
when an anthropogenic noise covers or ‘masks’ the sounds
produced by dolphins (Foote et al., 2004; Nowacek et al.,
2007). At certain moments, generally during motor acceler-
ation, masking occurs in such a way as to preclude determin-
ing any other type of sound other than engine noise. However,
at other times, even with interference, it was possible to iden-
tify the fundamental note and record the dolphins’ sound
parameters.
All sounds produced by dolphins in Pipa registered an in-
crease in at least two acoustic parameters in the presence of
sounds, with whistles (IF and FF) and calls (MIF, MAF, FV
and D) exhibiting changes primarily in their frequency
values. Based on this result, it can be hypothesized that the
large amount of noise present in the area causes modifications
in the dolphins’ acoustic niche, evidenced by sound emissions
at higher frequencies. Thus, there is an attempt to avoid the
higher ranges used by boats.
Data obtained here agree with the hypothesis of Parks et al.
(2009), who believed that cetaceans, such as the North
Atlantic right whale Eubalaena glacialis (Mu¨ller, 1776)
modify their calls with an increase in frequencies, depending
on where they are, to overcome background and anthropo-
genic noise from the different areas they inhabit throughout
the year.
The Mann Whitney test showed no differences in fre-
quency parameters in clicks values during the presence and
absence of noise. A wide range of frequencies are used in
dolphin click emissions, irrespective of the existence of
noise, varying between 1 and 48 kHz. It will probably be un-
necessary to modify the frequency niche of this sound,
because dolphins already use this wide range for echolocation.
Duration was the only parameter altered in the click cat-
egory. This increased during the presence of noise, probably
to overcome the noise barrier, since frequencies remained un-
changed. Producing a longer lasting sound can permit greater
echolocation accuracy during masking moments, due to
sound interference.
Although the pump displayed a narrow frequency range
and little reverberation, this characteristic does not seem to
interfere in clicks trains, given that the frequency parameters
of this sound category remained unchanged. However, the un-
interrupted noise of the pump appeared to have a greater in-
fluence on clicks, since duration increased in the presence of
noise.
In addition to these parameters, production of this sound
category fell considerably during the presence of noise.
Thus, dolphins seem to avoid using this sound during these
moments. This fact may be related to dispersion of fish
during the approach of boats and/or visual identification,
thereby avoiding energy expenditures with more intense echo-
location to overcome anthropogenic noise. It is also possible
that dolphins are distracted by boats, or need to pay more at-
tention to the boats than to feeding.
In contrast to clicks, the sound parameters of whistles were
significantly altered in the presence of boat noise. The a pos-
teriori showed that the increase in values observed at IF and
FF are related to the presence of motorboats, likely due to
their high frequency values when compared with schooners.
Since IF exhibit lower frequency values than FF, the former
are more susceptible to higher noise levels (mean ¼
10 kHz). Furthermore, the number of whistles produced in
the presence of motorboats was greater when compared
with schooners. This may reflect the larger number of motor-
boats in the area and greater number of tours these boats
make. Calls showed alterations only with respect to frequency
variation and between boats. An increase in the parameter oc-
curred for this sound category, as well as in whistles, in the
presence of motorboats.
Accordingly, it is difficult to determine which noise causes
the greatest impact on the sound parameters of dolphins in
Pipa, given that the pump affected clicks more, while the
6dalilat.lea
~omartinset al.
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boats exerted greater influence on the other categories.
However, motorboats tend to have more influence than
schooners, since they accounted for the greatest impact on
whistles and calls. Moreover, irrespective of source, the pres-
ence of these sounds alters the sound emissions of Guiana dol-
phins in Pipa, generating concern for creating impact
reduction measures.
The harm caused to dolphins by noise can be auditory and/
or behavioural (Richardson et al., 1995; Rezende, 2008). Daily
exposure to moderate to high-intensity sounds generates tem-
porary hearing losses that can eventually become permanent
(Pavan, 2002; Wartzok et al., 2005). Based on a study using
a photo-identification technique, dolphins visit the inlet
every day and an average total population of 105 individuals
was estimated in the area, which varies between 88 and 129
through the year, with a quarter of the population presenting
high fidelity (Link, 2000; Silveira, 2006; Ananias et al., 2008;
Paro, 2010). Thus, it seems likely that some individuals are
exposed to these noises daily, possibly sustaining damage
from this interference.
Impacts caused by tour boats in Pipa are still unclear.
Studies in the region have revealed a number of behavioural
modifications and the present study showed changes in
some sound emission patterns. All previous investigations de-
scribe short-term alterations there are still no long-term
studies on the vessels’ interference in dolphins. Monitoring
of this population is needed to minimize these impacts,
mainly those that can generate long-term damage.
According to Constantine (2001), boats cause negative
long-term effects when they affect important behaviours for
the conservation of the population, such as foraging and re-
production. The decrease in clicks trains during the presence
of noise must be monitored to determine whether this inter-
ference is compromising foraging activity, since, although
this may only affect a few individuals in the short term, it
may compromise the entire population in the long term, de-
creasing survival or altering their living area.
There are no studies in long-term estimations of popula-
tion density in the region; however, direct information from
local fishermen and tour boat owners revealed that residence
time and the number of individuals entering the inlets has
declined in recent years (Izac, personal communication).
Cases of marine mammal species abandoning areas as a
result of negative impacts are not rare. Stevens & Boness
(2003) observed that the South American fur seal
Arctocephalus australis (Zimmermann, 1783) seems to
abandon optimal reproduction areas, due to human distur-
bances in these areas. Thus, measures must be taken to dis-
courage dolphins in Pipa from leaving this important
feeding and reproduction area (Nascimento, 2006).
Tosi & Ferreira (2008) conducted an impact study of boats
in the Pipa area during a period in which boat traffic was con-
trolled. They found that behavioural changes were fewer than
those observed before controls were established. However,
these measures are no longer in force and tour boat traffic is
very heavy. Further studies to determine the impact of boats
owing to different types of motors used, based on comparisons
of these motors at a same speed, may identify the one that has
the least impact on local marine life.
Attempting to convince boat owners to replace old motors
with less powerful, 4-stroke engines, in addition to performing
regular maintenance, is essential to reducing noise. Further-
more, environmental education programmes involving the
local community and tourists are needed to show the import-
ance of conserving marine life, mainly because, once enligh-
tened, these individuals often become monitors of tour boat
activities.
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Correspondence should be addressed to:
D.T. Lea
˜o Martins
Programa de Po
´s Graduac¸a
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de Fisiologia, Universidade Federal do Rio Grande do Norte,
Campus Universita
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Norte, Brazil
email: dalilaleao@gmail.com
8dalilat.lea
~omartinset al.
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... Boats may be potential agents of disturbance for marine mammals (New et al., 2015), especially cetaceans of the order Odontoceti, because they depend on emissions of sound to communicate with other members of the species and to capture prey (Monteiro-Filho and Monteiro, 2001). Boat noise in coastal areas is a major source of disturbance for cetaceans, especially for resident populations (Leão-Martins et al., 2018), and the interactions between boats and cetaceans appear to be biologically significant for these animals (Lusseau, 2003;New et al., 2015). Whale-watching boat operators commonly exhibit inappropriate conduct in cetacean areas, including directly and insistently approaching dolphins and dividing dolphin groups with their boats. ...
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