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Acoustic ecology of humpback whales in Brazilian waters investigated with basic and sophisticated passive acoustic technologies over 17 years


Abstract and Figures

Whales are difficult to study. These large marine mammals cannot be maintained in captivity so they have to be studied in nature, and observing their underwater behavior becomes a challenge. The extensive distribution, large size, and aquatic life style of these leviathans constrain efforts to observe and understand the scale of what is being studied. Researchers have dealt with this challenge with wit, determination and creativity. Large whales are known for using long distance acoustic communication to coordinate social interactions such as mate attraction and group feeding, as well as a means for orientation and navigation. Therefore, sound is relied on to help “see” beyond the surface. Marine mammalogists were the first to modify existing technology from ocean bottom sensors to develop novel ways to listen underwater, taking advantage of the fact that these animals rely mostly on sound to survive and reproduce. In effect, biologists eavesdrop on the underwater lives of marine mammals by listening. Researchers listen to humpback whales using different passive acoustic technologies that span a variety of spatial and temporal scales. In this paper, studies conducted in Brazilian waters are reviewed, primarily in the Abrolhos Bank region, where basic and advanced technologies have been used to understand the acoustic ecology of this large marine mammal species. Male humpback whale culture, their social dynamics revealed by spatial and temporal vocal activity patterns, and their interaction with the encroaching noise generated by humans, are reviewed.
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Chief Editor José Paula
Special Issue 1/ 2018 | Jul 2018 | ISSN: 0856-860X
Western Indian Ocean
Marine Science
Humpback Whales in the
Western Indian Ocean
Guest Editor Olivier Adam
Chief Editor José Paula | Faculty of Sciences of University of Lisbon, Portugal
Copy Editor Timothy Andrew
Published biannually
Aims and scope: The Western Indian Ocean Journal of Marine Science provides an avenue for the wide dissem-
ination of high quality research generated in the Western Indian Ocean (WIO) region, in particular on the
sustainable use of coastal and marine resources. This is central to the goal of supporting and promoting
sustainable coastal development in the region, as well as contributing to the global base of marine science.
The journal publishes original research articles dealing with all aspects of marine science and coastal manage-
ment. Topics include, but are not limited to: theoretical studies, oceanography, marine biology and ecology,
sheries, recovery and restoration processes, legal and institutional frameworks, and interactions/relationships
between humans and the coastal and marine environment. In addition, Western Indian Ocean Journal of Marine
Science features state-of-the-art review articles and short communications. The journal will, from time to time,
consist of special issues on major events or important thematic issues. Submitted articles are subjected to
standard peer-review prior to publication.
Manuscript submissions should be preferably made via the African Journals Online (AJOL) submission plat-
form ( Any queries and further editorial corre-
spondence should be sent by e-mail to the Chief Editor, Details concerning the preparation
and submission of articles can be found in each issue and at
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Disclaimer: Statements in the Journal reect the views of the authors, and not necessarily those of WIOMSA,
the editors or publisher.
Copyright © 2018 —Western Indian Ocean Marine Science Association (WIOMSA)
No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form
or by any means without permission in writing from the copyright holder.
ISSN 0856-860X
Western Indian Ocean
Marine Science
Editorial Board
Atanásio BRITO
South Africa
South Africa
Issufo HALO
South Africa/Mozambique
Christina HICKS
Blandina LUGENDO
South Africa
Cover image: © 2015, Association Cetamada
Editorial Note
Humpback whales are well known especially for their very long migration routes and also because of
the songs that males emit during the breeding season. In 1971, in their famous article published in the
journal ‘Science’, Payne and McVay describe these songs as “a series of surprisingly beautiful sounds”!
Since 1971, more acoustic data have been collected and more knowledge generated; we now know that
the song ‘leitmotiv’ is dierent from one geographic area to another, and from one year to the next.
We also now know how they produce these sounds from their respiratory system.
In the last two decades, dierent techniques have been deployed to observe humpback whales in all the
oceans. Not only have passive acoustic monitoring techniques been used, but also visual observations,
electronic devices, and genetics. The objectives of these studies have been to better understand whale
activities, behaviors, and also the underwater environment in which they live, and the potential eects
of anthropogenic activities on their societies. This has involved many dierent research teams, with
their own skills, methods and programmes. Results have been published in the scientic literature and
presented at dierent international conferences.
However, three things have recently become apparent: Firstly, the study of humpback whales is a wide
subject requiring people with complementary skills. It was apparent that it was necessary to bring these
people together to discuss this species of whale for several reasons: a) because it would highlight the
major results obtained thus far; b) because it would be interesting to share experiences (especially on
the data and methods used, but also on common challenges); c) to co-design future projects and iden-
tify priorities; and d) because it would provide an opportunity to start new collaborations.
Secondly, before 2015, no international scientic conference or workshop existed with regular annual
sessions especially dedicated to this species of Mysticeti whales. In order to address this, we initiated
the creation of the Humpback Whale World Congress (HWWC, The rst ses-
sion was held in Madagascar in 2015 and the second in La Réunion Island in 2017. Our idea was to
bring together researchers and technicians from universities, research institutes, government organ-
izations, and industry, dealing with all aspects of the biology, ethology, genetics, ecology, acoustics,
signal processing, pattern recognition, mathematics, and computer sciences applied to the study of the
humpback whales and their environment, and the potential eects of anthropogenic activities on the
species. The goal of the HWWC is to provide a forum for exchange of new results obtained from the
latest advances in instrumentation and methods.
Thirdly, during the BaoBaB project I led from 2012 to 2014, it became apparent that the extensive
movement of humpback whales, even during the breeding season (with more than 100 km being cov-
ered per day), resulted in the same individuals being observed from the east coast of Africa to the
Mascarene Islands. Because of this remarkable characteristic of this baleen whale species, it was obvi-
ous that we needed to encourage collaboration at a regional level, and we envisaged a consortium of
people who work collaboratively on the Southwestern Indian Ocean humpback whale population.
During the international HWWC we were very pleased by the quality of the work shared by dier-
ent teams, and the strong motivation to exchange information and work together. For this reason,
we requested some colleagues to describe their projects in full papers, to put them together, and pub-
lish this unique special issue.
I would like to thank all the authors and co-authors, all the persons who contributed to this special issue,
and more strongly the Cetamada Team who currently does such amazing work on these humpback whales!
Enjoy reading!
Olivier ADAM
Institut d’Alembert
Sorbonne University, Paris, France
WIO Journal of Marine Science Special Issue 1 / 2018 23-40
Whales are dicult to study. These large marine mammals cannot be maintained in captivity so they have to be stud-
ied in nature, and observing their underwater behavior becomes a challenge. The extensive distribution, large size,
and aquatic life style of these leviathans constrain eorts to observe and understand the scale of what is being studied.
Researchers have dealt with this challenge with wit, determination and creativity. Large whales are known for using
long distance acoustic communication to coordinate social interactions such as mate attraction and group feeding, as
well as a means for orientation and navigation. Therefore, sound is relied on to help “see” beyond the surface. Marine
mammalogists were the rst to modify existing technology from ocean bottom sensors to develop novel ways to listen
underwater, taking advantage of the fact that these animals rely mostly on sound to survive and reproduce. In eect,
biologists eavesdrop on the underwater lives of marine mammals by listening. Researchers listen to humpback whales
using dierent passive acoustic technologies that span a variety of spatial and temporal scales. In this paper, studies
conducted in Brazilian waters are reviewed, primarily in the Abrolhos Bank region, where basic and advanced technol-
ogies have been used to understand the acoustic ecology of this large marine mammal species. Male humpback whale
culture, their social dynamics revealed by spatial and temporal vocal activity patterns, and their interaction with the
encroaching noise generated by humans, are reviewed.
Keywords: male display, communication, Megaptera novaeangliae, song, passive acoustics.
Acoustic ecology of humpback whales in Brazilian
waters investigated with basic and sophisticated
passive acoustic technologies over 17 years
Renata S. Sousa-Lima1,2,3,9,*, Márcia H. Engel3, Victor Sábato4, Bianca R. Lima5,
Thiago S. M. Queiróz4, Marcos R. M. Brito1, Deborah P. Fernandes1,2, Cristiane A. C. Martins3,6,
Paula S. Hatum1,2, Thamires Casagrande1,2, Laura K. Honda1,2, M. Isabel C. Goncalves1,7,
Júlio E. Baumgarten7, Artur Andriolo8,9, Milton C. Ribeiro10, Christopher W. Clark11
Original Article
1 Laboratório de Bioacústica,
Departamento de Fisiologia
e Comportamento, Centro de
Biociências, Universidade Federal
do Rio Grande do Norte, Natal,
RN, Brasil
4 Laboratório de Mastozoologia,
Departamento de Zoologia,
Instituto de Ciências Biológicas,
Universidade Federal de Minas
Gerais, Belo Horizonte, MG,
7 Laboratório de Ecologia Aplicada
à Conservação, Universidade
Estadual de Santa Cruz, Ilhéus, BA,
Universidade Estadual Paulista
(UNESP), Rio Claro, SP,
2 Programa de Pós-Graduação
em Psicobiologia, Centro de
Biociências, Universidade Federal
do Rio Grande do Norte, Natal,
RN, Brasil
5 Instituto de Ciências Biológicas e
da Saúde, Pontifícia Universidade
Católica de Minas Gerais, Belo
Horizonte, MG,
8 Laboratorio de Ecologia
Comportamental e Bioacústica,
Universidade Federal de Juiz
de Fora, Juiz de Fora, MG,
11 Bioacoustics Research Program,
Cornell Lab of Ornithology,
Cornell University, Ithaca, NY,
3 Projeto Baleia Jubarte, Instituto
Baleia Jubarte, Caravelas, BA,
6 Tryphon Océans, Tadoussac, QC,
9 Instituto Aqualie, Juiz de Fora, MG,
* Corresponding author:
24 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
“Technology advances rapidly. Nonetheless our listen-
ing technology remains limited to study large whales.
The future will continue to bring us tools that will ena-
ble humans to pick up whale sounds far away in ocean
refugia. We can only hope that whales will still exist
and not be made of the fabric of legends, as they once
were...monsters and mermaids….”. (Sousa-Lima, 2007).
Who are we listening to?
The humpback whale.
The humpback whale (Megaptera novaeangliae) is a
baleen whale (Fig. 1) that has a cosmopolitan distri-
bution, inhabiting all oceans of the world. Similar
to other large whales, the humpback has a distinct
temporal geographical distribution, undertaking
long migrations annually that can exceed 8000 km
one-way (Horton et al., 2011), between their feeding
and breeding grounds. In the Southern hemisphere
during summer months, they feed at high latitudes
o South Georgia and the Sandwich Islands in Ant-
arctica (Zerbini et al., 2006, 2011; Stevick et al., 2006;
Engel and Martin, 2009). During winter, they migrate
to tropical waters, where they mate, give birth and
nurse the young, and occasionally feed along the
South Atlantic coast (Dawbin, 1966; Danilewicz et al.,
2009; Alves et al., 2009). Migrations are structured by
age, sex and reproductive status. Lactating females
leave the feeding grounds rst, followed by imma-
ture whales, mature males and females, and pregnant
females leaving last. On the return migration, newly
pregnant females are the rst to return to the feeding
grounds (Dawbin, 1966, 1997). Individual humpback
whales show variable levels of site delity even within
the same population (Weddekin et al., 2010; Bara-
cho-Neto et al., 2012) and some return to the same
area between migrations (Clapham et al., 1993; Bara-
cho-Neto et al., 2012).
During summer while feeding, social organization of
humpback whales is oen limited to small, unstable
groups, mostly pairs (Whitehead, 1983). Groups with
calves are oen composed only of calf and mother
(Clapham et al., 1993). When in the breeding grounds,
interactions are oen composed of small groups with
brief associations. Nevertheless, frequent agonistic
behavior between several males happen (Mattila et al.,
1994). Singletons, dyads and trios are common during
this period, where dyads and trios are frequently seen
with dierent associates (Mobley and Herman, 1985).
Females with calf are oen accompanied by a male,
betting on the possibility of mating, in the event of
the female entering postpartum estrus (Tyack, 1981).
Larger groups, with surface activity and aggression
between members, have been named competitive
or active groups, where males actively compete for
access to a mature female (Tyack and Whitehead,
1983; Clapham et al., 1992).
The Western South Atlantic Ocean (WSA) humpback
whale population that winters o Brazil is distributed
from Rio de Janeiro to Rio Grande do Norte (24o to
Figure 1.
Figure 1. Humpback whales, Megaptera novaeangliae, photographed by Renata Sousa-Lima on the Abrolhos Bank, Brazil.
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
5o S) (Andriolo et al., 2006; Wedekin et al., 2010) and
re-occupying areas along the coast (Rossi-Santos et al.,
2008; Gonçalves et al., 2018). The WSA population has
been estimated to be close to 20,000 (Bortolotto et al.,
2016; Pavanato et al., 2017) indicating a population size
of around 60% of its estimated pre-modern whaling
abundance and may recover to its pre-exploitation size
sooner than previously thought (Bortolotto et al., 2016).
Where are we listening for humpback
Since the year 2000 systematic passive acoustic mon-
itoring eorts have focused on the Abrolhos Bank
(AB). AB is located o the east coast of Brazil between
16o40’and 19o30’S with a mean depth of 30 m, covering
an area of approximately 30,000 km2 (Fainstein and
Summerhayes, 1982). Five small islands comprise the
Abrolhos archipelago in the northeastern part of the
AB. The Abrolhos Marine National Park was created
on 6th April 1983 (Decree 88.218) and is located in the
northeast portion of the AB. It includes the Abrolhos
archipelago and two reefs: Abrolhos and Timbebas, a
total area of 913 km2 (IBAMA/FUNATURA, 1991).
Individual whales tend to have longer residence times
on the AB when compared to other areas north of the
bank (Wedekin et al., 2010; Baracho-Neto et al., 2012),
which corroborates previous evidence that suggests that
the AB is the main area of concentration for humpback
whales wintering in Brazilian waters (Siciliano, 1997;
Martins et al., 2001; Andriolo et al., 2006). Approxi-
mately 80% of all individuals that visit the coast of Brazil
are in this region, while the remaining 20% are distrib-
uted along the northeastern coast (Andriolo et al., 2006).
AB is especially important for nursing females, which
represent 50% of social groups in the area contrasting
with only 17 % of female with calf groups registered on
the northern coast of Bahia (NCB) (Rossi-Santos et al.,
2008). These data justied the concentration of our
acoustic monitoring eorts in the AB region.
How are we listening for humpback
During the quiet age of sail, under conditions of excep-
tional calm and proximity, whalers were occasionally
able to hear the sounds of whales transmitted faintly
through a wooden hull (Aldrich, 1889). Then, seamen
could hear the sounds of humpback whales, but to
explore the intricacies of this vocal behavior was still
out of reach. Detailed qualitative description of a spe-
cies’ behavior, such as their sound repertoire, is impor-
tant. Nevertheless, the questions that drive the advance-
ment of knowledge about a species’ communication
system are oen answered by quantitative analyses of
the variation on some specic trait. Metrics of this var-
iation should provide objective evidence for determin-
ing the occurrence of the evolutionary mechanisms
hypothesized by researchers (Sousa-Lima, 2007).
Figure 2. Map of the coastal Brazilian states where humpback whales are known to occur and limits of the
Abrolhos National Marine Park within the Abrolhos Bank.
26 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
As Tchernichovski et al. (2004) point out, the invention
of the spectrogram at Bell Laboratories in the late 1950’s
was invaluable for the quantitative investigation of ani-
mal vocal behavior. Animal sounds started to be fur-
ther inspected quantitatively as analytical tools became
handy and sound acquisition hardware became avail-
able for recording underwater sounds. Nowadays we
employ basic and advanced technologies to explore the
acoustic ecology of large whales such as humpbacks.
Dipping hydrophones
Listening to marine mammals underwater today is
only possible due to the early ndings of Pierre Curie,
who together with his elder brother Jacques, in 1880,
observed that an electric potential was produced
when mechanical pressure was exerted on a quartz
crystal (Curie and Curie; 1880a, b). Hydrophones are
built based on this observation. In this study ,dierent
combinations of recording equipment were used that
allow the recording of sounds within the frequency
ranges know for humpback whales: Sony DAT D8 or
Marantz PMD670 solid state recorders (frequency
response up to 20 kHz) connected to hydrophones
HTI 90 series (frequency response up to 30 kHz).
Singers were silently approached to within approximate-
ly 100m to obtain high quality recordings, and depth
measurements at the site of the singing whale were col-
Figure 3.
Figure 3. Basic passive acoustic methods, showing dipping hydrophone deployed from a boat or a zodiac
at the Abrolhos Bank, Brazil.
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
lected using a small zodiac or boat (a trawler, a sailboat
with or without outboard engine, or a berglass center
engine shing boat). The approach aboard the zodiac was
carried out using an umbrella as an improvised sail, or a
paddle to get as close as possible without disturbing the
whale. Silent boat approaches were done by navigating
upwind from the singer and then cutting the boat engine
and driing downwind toward the focal whale with the
engine o. When a silent approach was not feasible, we
attempted recordings from the research boat by cutting
the engine o, and driing towards the focal animal.
The song and behavior observed above the water of the
focal singer (breathing, swimming, exposure of body
parts) were simultaneously recorded and the exact time
that a behavior occurred was registered on the record-
ings (second voice channel) or on a data sheet (Fig. 3).
Array of autonomous recording systems
During the late 1960’s, a change of spatial scale occurred
in marine geophysical research when studies on earth-
quakes became focused in smaller areas of the seaoor.
This shi required higher accuracy and resolution of
measurements made using geophysical instruments,
which then led to the development of ‘autonomous
instruments’ to monitor and record earthquakes under-
water. Incidentally, these xed autonomous instruments
are also capable of recording low frequency sounds of
baleen whales. McDonald et al. (1995) were the rst to
use Ocean Bottom Seismometer (OBS) or Hydrophone
(OBH) data to study blue and n whale calls. OBSs and
OBHs were too expensive for most researchers so, dur-
ing the 1990’s, several laboratories started to develop
their own autonomous recorders to lower costs and to
collect bio-acoustic data from marine mammals. More
recently, advances in low-power electronics, high-data
capacity data-storage, computer processing technology,
and power supply units have enabled the proliferation of
autonomous recording systems capable of monitoring
the acoustic behavior of many species of marine mam-
mals as well as environmental sounds (Sousa-Lima et al.,
2013). Ongoing continuous improvements in data-stor-
age and battery technologies are making data collection
possible for much longer periods of time and at higher
data-sampling rates.
The rst deployment of autonomous bottom mounted
acoustic sensors in South America was in 2003. Sounds
of humpback whales were listened for on the ocean
oor o the Abrolhos archipelago and the local acous-
tic habitat (Fig. 4). A variable percentage of the park area
was acoustically monitored using an array of MARUs
(“Marine Autonomous Recording Units” developed
by the Bioacoustics Research Program of the Cornell
Laboratory of Ornithology - BRP) between the years
2003 and 2005. These devices includes a microproces-
sor, hard disks for data storage, acoustic communica-
tions circuitry, and batteries, all sealed in a glass sphere
and protected by a plastic harness (Fig. 4). An exter-
nal hydrophone was connected to the unit through a
waterproof connector.
Figure 4.
Figure 4. Array of marine autonomous recording units (MARUs) synchronized on land and tested before
deployment. Photograph of a MARU showing the internal electronics and external hydrophone.
28 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
Each MARU carries an onboard clock that is synchro-
nized before and aer deployment in order to time
signals received from global positioning system (GPS)
satellites with a precision of ± 10 µsec. This makes it
possible to perform sound source localization and
tracking of signals recorded by an array of MARUs.
The arrays consisted of 4-5 MARUs deployed northwest
and south of the Abrolhos archipelago where Martins
(2004) calculated the density of whales to be similar.
The MARUs were programmed to record continu-
ously at a sampling rate of 2,000 Hz during 26 days to
4 months, depending on the logistics to redeploy aer
a change in batteries. At the conclusion of the eld sea-
son, a boat equipped with an acoustic transponder unit
communicated with the deployed MARUs and com-
manded each one to separate from its anchor using a
unique acoustic release signal. The MARUs oated to
the surface where they were retrieved.
What are we listening to?
Humpback whales of all ages and both sexes display
a variety of aerial behaviors: breaching, lobtailing,
ippering and tail breaching, which are thought to be
used as a means of communication (Whitehead, 1985).
Furthermore, both males and females can produce
sounds used for communication (Zoidis et al., 2008),
but only males are known for producing long and pat-
terned sequences of sounds, called songs (Payne and
McVay, 1971). Song is heard mainly on the breeding
grounds and are thought to function to mediate mat-
ing (see the seminal song evolution review by Her-
man, 2016).
The song
As early as 1951, mysterious sounds were recorded in
the ocean by the U. S. Navy and described by Schrei-
ber (1952). The mystery sounds were believed to be
from humpback whales, but were only attributed to
the species a decade later (Schevill and Watkins, 1962;
Schevill, 1964; Watkins, 1967). Payne and McVay (1971),
inspired by bird literature and armed with acoustic
spectrographic analyses tools, rst described the basic
patterned hierarchical structure of humpback whale
sounds recorded during the late winter and early
spring o Bermuda.
Payne and McVay (1971) noted that “one of the char-
acteristics of bird song is that they are xed patterns
of sounds that are repeated” and, having observed
xed patterns in the sounds of humpback whales,
subsequently adopted the term “song” to describe it.
These authors relied on Broughton’s (1963) categories
of the term “song” to choose the best denition for
the observed pattern in humpback whale sounds: “…
a series of notes, generally of more than one type,
uttered in succession and so related as to form a
recognizable sequence or pattern in time”.
Aer justifying their choice to call the humpback
whale sounds “song”, Payne and McVay (1971) provided
a terminology for the various hierarchical levels they
observed. Starting from the smallest element, when
listening to a sound at lower speeds, subunit is dened
as a single element in a series of short pulses com-
prising a sound. A unit, or note, is dened as a con-
tinuous sound to the human ear if played in normal
speed. Thus, some units are composed from subunits.
Units are arranged in phrases, which are generally
composed of combinations of similar units. Simi-
lar phrases are repeated to form themes, which are
“unbroken” sequences or repetitions of phrases. The
song is dened as the combination of several distinct
themes. The highest hierarchical level is the song ses-
sion, which consists of a series of songs with silent
intervals of less than a minute. Songs recorded from
a boat by Payne and McVay (1971) lasted between 7 and
30 minutes but continuous singing activity may last
much longer. The duration of individual male hump-
back whales’ singing bouts recorded with the MARU
array during the current study (N =136) varied between
30 to 1,230 minutes (20.5 hours, similar to the 22 hours
of singing recorded by Winn and Winn (1978)).
The role of the long and complex song of male hump-
back whales was initially described as having a xed
stereotyped pattern within a population, but sub-
sequent studies have shown that the song changes
during one or more breeding seasons within a single
population and this may be regarded as cultural trans-
mission (Noad et al., 2000). The structural variability
of the humpback whales’ song in AB has been studied
by the authors since the year 2000, describing the var-
iations found on the level of phrases to identify line-
ages of themes along the dierent years as suggested
by Cholewiak et al. (2012).
The identication of theme lineages was only possi-
ble aer determining where the song of the hump-
back whale started. Considering the long duration of
song sessions, manual browsing of 26 continuous days
of acoustic recordings from MARUs was done to nd
instances where song was heard abruptly preceded by
silence (Lima and Sousa-Lima, 2012). Data from dip-
ping hydrophones were also browsed to determine
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
the contribution of each phrase type within each song
cycle, allowing statistical testing if the initial themes
found in the MARU data were indeed preferred as the
rst theme to be sung by males, or if they appeared as
the initial theme by chance alone.
Merging information from two dierent datasets
acquired by deploying basic, simple recording equip-
ment and advanced autonomous technologies allowed
this very dicult question to be answered: Yes, males
that sing in AB do have a preference to start a song
session with a specic theme which has been dened
as theme 1 for all subsequent AB song analyses.
Listening to song to understand
humpback whale culture
Even though there have been many debates about the
denition of culture and many diculties in quantifying
cultural transmission in non-humans species (Laland
and Janik, 2006), studies of humpback whale song pro-
vide compelling evidence for cultural transmission in
the learning of vocal patterns in these large animals.
Knowing that dierent humpback whale populations,
living in dierent ocean basins, normally have distinct
song patterns that change through time within their
own population, Noad et al. (2000) reported a radical
song change in the population inhabiting the Austral-
ian east coast. In a period of approximately two years,
the song they used to sing was completely replaced
by a new song. Brought by a small group of singers
coming from the Australian west coast, the group rap-
idly incorporated the new patterns in their own song,
which was completely modied aer two years. In
Mexico and Hawaii, two breeding grounds 4800 km
apart, synchronous changes in songs have been doc-
umented (Cerchio et al., 2001), with many variables in
song pattern changing in a similar manner. The same
was observed between songs recorded more than
5500 km apart, from AB and Gabon (Darling and Sou-
sa-Lima, 2005). Songs from the Brazilian humpback
whale population in Abrolhos were strikingly simi-
lar to songs from the African population recorded in
Cape Lopez, sharing ve themes in their songs, with
very similar units and phrases. Song patterns had
more in common between sites than songs from the
same population in dierent years. It was speculated
that these song similarities could be indicative of cul-
tural transmission or according to an innate template.
Long term monitoring of humpback whale songs
from Bermuda (Payne and Payne, 1985) and Tonga
Figure 5.
Figure 5. Spectrogram of part of a Brazilian humpback song recorded with a dipping hydrophone connected to a portable
recorder from a boat.
30 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
(Eriksen et al., 2005) showed that through the years,
songs contained unique twists every year, as well
as material from the previous year’s song, and also
that the speed of this change could vary, sometimes
changing drastically in a span of two years, while at
other times changing at a slower pace over a larger
timespan. Nonetheless, change was always directional,
indicating learning instead of driing.
Changes over a much larger geographical scale were
only detected in a comparative study conducted by
Garland et al. (2011). They were able to document, in
an 11-year period, a fast paced and repeating hori-
zontal cultural transmission in six populations in the
western and central South Pacic Ocean. The song
types clearly changed and were spread from the west-
ern populations to the eastern populations. New types
of songs identied in one population would spread to
another population further east between consecutive
breeding seasons. This rapid transmission, combined
with a high level of site delity of the studied popula-
tions, was a strong indicator of cultural transmission.
Research in AB has focused on identifying changes be-
tween years at the phrase level within the same popula-
tion. Twenty-one themes were registered in AB between
2000 and 2005, and lineages were built for the themes
in which it was possible to dene a standard phrase
(as suggested by Cholewiak et al., 2012). Changes were
observed in the spectral structure of the units, introduc-
tion of new units, removal of units and also variation in
the general sentence structure intra- and inter-individ-
ually (Brito and Sousa-Lima, 2014; Hatum, 2015).
Using simple dipping hydrophones connected to port-
able recorders in AB, distinct forms of male phrase
variation were found: changes in unit spectral struc-
ture, insertion of new units, unit removal and also var-
iations in the general structure of phrases, both intra
and inter-individually. The identication of song lin-
eages between years has allowed for a better under-
standing of cultural changes, as shown in the lineage
for theme 1 recorded in Abrolhos in 2003 (Fig. 6). In
the rst year, the theme was composed of one phrase
of 4 units (A3-B3-B3-B3), and it was maintained in
the following year. Nonetheless, in 2005, only the
rst unit remained the same, and the following units
underwent spectral changes (from B3 to B5) and rep-
etitions of a new unit appeared for the rst time (b5).
Understanding the variations found in the evolu-
tion of songs in humpback whales is of fundamental
importance to allow for a better understanding of
song learning and cultural transmission within and
between populations. Ongoing development of met-
rics capable of pointing out how and where in the
song the changes are happening will allow for more
accurate assertions of patterns being transmitted and
learned by interacting individuals.
Humpback culture can be investigated at varying spa-
tial and temporal scales using very basic passive acous-
tic technologies. The challenge is to think of creative
ways to ask questions about this behavioral trait that
will inspire collaborative eorts throughout the oceans.
Listening to understand the social
dynamics of singing
Real time monitoring of humpback whale vocal activ-
ity in AB has been carried out using basic equipment
deployed from boats. Surveys dedicated to investigat-
ing the AB underwater acoustic ecology focused on
humpbacks have been carried out since 2000 (Sou-
sa-Lima et al., 2002). A total of 201 humpback whale
groups and 493 individuals were sighted and 103 of
these were vocally active groups and 98 were vocally
inactive. Of the vocally active groups (N = 103), 72%
did not include calves (N = 74) and 28% did (N = 29).
The remaining groups were vocally inactive (N = 98)
and 43% of these did not include calves (N = 42) and
57% did (N = 56).
Figure 7 shows that each group category had a dif-
ferent level of vocal activity. Mother and calf (MoCa)
groups showed the smallest occurrence of vocal activ-
ity. However, in groups with calves and the presence
of principal and secondary escorts, the percentage
of vocal activity was higher. Solitary individuals pre-
sented the highest percentage of vocal activity in AB.
What do male humpback whales do
when they are singing?
Due to the hierarchical structure and long duration of
their songs, male humpback whales are an excellent
model for applying passive acoustic source localization
to track their movement. This was possible with the use
of a set of synchronized acoustic sensors (MARUs). By
comparing dierences on time-of-arrival of the same
acoustic signal on each sensor, it was possible to estimate
with precision the location of each singer in short time
intervals, which allowed their trajectories to be traced at
a ne scale. This made it possible to visualize how and
where singing humpback males moved, what were the
characteristics of their trajectories, if they had preferred
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
locations, if they interacted among themselves, and
even to make inferences about their behavior.
Male singers were acoustically followed for up to
5 hours with individuals traveling up to 16 km at
speeds of up to 30 km/h. These animals live in areas
of transcontinental proportions; therefore, move-
ment parameters must present dierent values when
migration paths and trajectories are compared inside
reproductive and feeding areas. Typically, the move-
ment speed is higher and the trajectory is less tortuous
when the animals are migrating (Kennedy et al., 2014;
Mate et al., 1998; Zerbini et al., 2011).
Around the Abrolhos archipelago males spent 47%
of the time moving, while during the other 53% they
practically stayed at the same spot. The average move-
ment speed in Abrolhos was 2.3 km/h, but the high-
est speed ever recorded for this species, 30.05 km/h,
was registered within the trajectories. Mean speed of
singing males in Australia is 2.5 km/h (Noad and Cato,
2007), and silent males travelled faster (4 km/h).
While singing in Abrolhos, males showed a bias
towards persisting in the same direction – a direction-
ality index of 0.58, in a range where 0 is a highly tortu-
ous trajectory and a straight trajectory is represented
by a value of 1. This means that, although most of the
time they were stationary, when singers moved they
tended to have a set direction of movement rather
Figure 6.
Figure 6. Spectrograms containing phrases of the Theme 1 lineage for the years 2003, 2004 and 2005. Capital letters
indicate the position of the unit in the phrase, numbers indicate the year they rst appeared, lower case letters indicate
a new type of unit not present in the years before.
Figure 7.
Figure 7. Distribution of the percentage of sighted humpback whale
groups that were vocal, or not, during acoustic monitoring dedicated
boat surveys in AB in two consecutive years (2004 and 2005). MoCa:
mother and calf; MoCaPe: mother and calf with principal escort;
MoCaCG: competitive group with a mother-calf pair; SOL: individual;
PA: pair; CG: competitive group.
32 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
than moving at random, which suggests an interac-
tion between singers and a conspecic (as observed
by Darling et al., 2006) or in response to a localized
Even at the start of the reproductive season, singing
activity at AB was high. In a 391 h recording at the
beginning of the reproductive season in 2005, more
than 90% of the hours showed singing activity of at
least two males simultaneously. This fact highlights
the importance of acoustic interactions between sing-
ers, independently of their movement. Visualization
of male tracks using advanced technologies as applied
here is a strong tool to understand the function of the
humpback whale song.
Darling et al. (2006), recording focal males from a
small boat, were capable of detecting 167 interactions
among singing males over a timespan of around 6
years. Similar inferences were reached during the
present study using data from a few days but with a
much larger spatial coverage provided by the detec-
tion range of the MARU array. However, complemen-
tary real time visual information was not available in
the present study about silent interacting animals as
potential sources of stimuli to elicit singer responses.
Figure 8 shows trajectories of two males recorded
simultaneously by the methods used in the present
study as compared with the interaction schematics
published by Darling et al. (2006). It is possible to see
that the information of localization resulting from
acoustic tracking is more detailed, so that the infer-
ences about male-male interactions may be explored
in a ner scale than using traditional visual obser-
vations while recording from a boat. Nonetheless,
acoustic tracking methods coupled with simultane-
ous information from sightings, such as individual
identication, age and behavior interactions of other
nearby individuals (as realized by Darling et al., 2006)
can lead to a higher level of understanding. The
application of more advanced technologies of acous-
tic tracking of singing males may greatly enhance the
potential of continuous and intensive observation of
these animals and open avenues for a deeper com-
prehension of ecological and behavioral aspects of
the species.
Listening to understand the spatial
distribution of vocal activity
The spatial model that best predicted vocal activity
in AB included “Calf Presence”, “Distance to Reefs”
and “Depth”. The model predicted that vocally active
groups were less likely to have calves, were farther away
from coral reefs and found in shallower waters. When
a calf was present in the group, it was unlikely that
there would be a singing male present. Even though
mothers and calves produce vocalizations (Simão
and Moreira, 2005; Zoidis et al., 2008; Videsen et al.,
2017), they have not yet been documented singing.
Figure 8.
Figure 8. (a) Original trajectories inferred using PAM. Red and black dots represent dierent singers, and blue and red
marks show the starting and nal locations of each singer; (b) Trajectory schemes simplied from Darling et al. (2006).
Each code composed of a letter (or a letter and a number) represents one dierent individual.
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
Mother and calf pairs are most likely found in shallow
waters (Martins et al., 2001; Félix and Botero-Acosta,
2011) and the presence of calves not only has an
eect on singing, but also on distribution of hump-
back whales. Shallow waters are ideal for mothers to
care for their calves, but the small water column is
not adequate for courting males (Smultea, 1994; Ersts
and Rosenbaum, 2003). Mothers might prefer shal-
low waters possibly to avoid harassment by males,
disruption of nursing, and injury or separation from
calves (Smultea, 1994; Elwen and Best, 2004). Félix
and Botero-Acosta (2011) suggest that dierent groups
may show discrete reproductive strategies when
responding to social and environmental conditions.
Even though females mate post partum, they are not
the ideal partner for courting males (Smultea, 1994).
Locations in which receptive females congregate may
determine the main singing areas (Frankel et al., 1995).
Figure 9.
Figure 9. Distribution of humpback whale groups on the Abrolhos Bank, Brazil.
Figure 10.
Figure 10. Number of 2-minute segments with detections of singing activity around the Abrolhos archipelago, Brazil
in the years 2003, 2004 and 2005 (in two dierent areas) recorded with arrays of marine acoustic recorder units
(MARUs) plotted in 24 hour panels. The width of the panel corresponds to the period during the winter season that
the recordings were made.
34 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
Listening to identify the temporal patterns
of male humpback singing behavior
Much investigation has taken place on the occurrence
of a temporal pattern in vocal activity of humpback
whale males, and how endogenous and exogenous
factors would act on its expression. Sousa-Lima and
Clark (2008) and Casagrande (2016) investigated
the existence of a daily variation pattern in which
there is high vocal activity during the night until
early morning, showing a decrease in the aernoon
(Fig. 10). This decrease in vocal activity by hump-
back whales during the day may be a behavioral
response to an external stimulus that creates a tem-
poral reorganization in song performance. However,
the pattern of less vocal activity during the day loses
its intensity throughout the months, being more
evident at the beginning rather than the end of the
reproductive season.
Other observations show that even though the num-
ber of individual animals on AB reaches its highest
density between the months of August and Septem-
ber, and decreases until November (Martins et al.,
2001; Morete et al., 2008), singing activity of hump-
back males increases as the season progresses (Que-
iróz, 2010; Cerchio et al., 2014) (Fig. 11).
Humpback whales remained in AB for up to 71 days
(Wedekin et al., 2010), and during this period and
throughout the season, males were observed produc-
ing songs and in physical combat with other males
over access to females, in addition to the energetic
cost of the journey towards the reproductive area
(Dawbin, 1966; Craig and Herman, 1997). Spending
energy on physical combat at the end of their period
in the breeding area may pose higher costs and result-
ing survival risks, making them use a less costly strat-
egy at this time; that of singing.
Listening to the interaction between
singing male humpback whales and noise
While listening for humpback whales, other environ-
mental sounds present in the area were also recorded.
The Abrolhos archipelago is an important tourist
destination in Brazil, and boats take tourists to div-
ing spots as well as to watch whales. Tracks of tourism
boats obtained with GPSs in the area during the winter
of 2005 are shown in Figure 12.
The ocean is certainly not a silent environment. Bio-
logical sounds, waves, tides, earthquakes and wind
play important roles in the acoustic ecology of the
seas. This constant background noise has modulated
the communication systems of several aquatic spe-
cies and organized their acoustic niches accordingly.
Only with the advent of the Industrial Revolution did
human activities begin to contribute energy to the
acoustic seascape of the oceans. Examples of anthro-
pogenic noise in AB include shipping and recreational
boat trac, which generate low-frequency noises that
overlap in time and in frequency with many marine
mammal sounds, and these noises oen aect the
Figure 11.
Figure 11. Number of humpback whale singers (0 to 4 or more) counted in 2004 o the Abrolhos archipelago showing an
increase in singing activity as the season progresses.
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
animals negatively (Richardson et al., 1995). Shipping
is the greatest source of man-made low-frequency
noise in the ocean (Richardson et al., 1995; McDonald
et al., 2006). Vessels create noise through their engines,
bearing changes, vibrations of the hull, and propeller
cavitation (Urick, 1983; Richardson et al., 1995). Docu-
mented short-term displacement of marine mammals
exposed to these noise events (reviewed in Richardson
et al., 1995) includes disruption of important activities
that may result in loss of food or mating opportunities
for the animals involved. Further, a sustained increase
in vessel noise can result in avoidance of the aected
area temporarily or even permanently, as suggested
by Bryant et al. (1984) for gray whales.
Advanced technology now provides the unique
opportunity to follow the movements of these ani-
mals by sequential localization of their sounds,
as shown above, as well as a tool to investigate the
eects of noise-producing anthropogenic activities
on their movements and behavior. A major new
contribution of passive acoustic tracking technol-
ogy is that it enables simultaneous follows of mul-
tiple “focal” singers. This greatly increases the e-
ciency of assessing the eects of boats by locating
and discriminating multiple vocally active animals
and their relative distance to an approaching boat
(Sousa-Lima and Clark, 2009). Song cessation (Fig.
13) and displacement were detected by Sousa-Lima
and Clark (2009). Masking is another important
issue and in AB, MARU recordings show the same
individual song can be masked at dierent levels
depending on the relative distance between boat and
singing male (Fig. 14).
Listening to humpback whales beyond
the Abrolhos bank
With the increasing number of humpback whales o
the Brazilian coast (Bortolotto et al., 2016; Pavanato et
al., 2017), the population is re-occupying areas used
before being aected by the whaling period (Ros-
si-Santos et al., 2008; Andriolo et al., 2010). Few studies
have been carried out in coastal areas other than the
Abrolhos bank (Baracho-Neto et al., 2012; Lunardi et
al., 2008; Gonçalves et al., 2018).
Passive acoustic monitoring was conducted approxi-
mately 400 km north of Abrolhos Bank in Serra Grande
(Bahia, Brazil) from July to October of 2014 and 2015
(Gonçalves, 2017). Oceanpods, autonomous underwa-
ter sound recorders developed by LADIN from São
Paulo University (Sánchez-Gendriz and Padovese,
2016), were deployed at depths of 16 to 22 m, up to 3
km away from the coast of Serra Grande to listen for
humpback whales. Vocal and non-vocal activity was
recorded, including song and percussive sounds pro-
duced by the whale body’s impact with the surface of
the water through breaching, ipper and tail slapping.
A preliminary description of song lineages from the
Serra Grande region identied eight themes, includ-
ing static, shiing, and non-patterned theme types
Figure 12.
Figure 12. GPS tracks of tourism boats that operate trips to the Abrolhos archipelago.
36 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
(Payne et al., 1983). New units appeared, existing units
were modied, and themes were subtracted and added
over a two year period. The Levenshtein distance sim-
ilarity index between Serra Grande songs from the
years 2014 and 2015 was 50%.
Males also use areas north of Abrolhos during the
breeding season to display vocally. These lower den-
sity areas could be essential for males that cannot
successfully compete directly with other males, and
theoretically contain less mates, but also contain less
Figure 14.
Figure 14. Spectrogram of four channels representing four synchronized MARUs showing a humpback whale song session in the
Abrolhos archipelago, masked in the 3rd channel by a boat noise.
Figure 13.
Figure 13. Spectrogram of four channels representing four synchronized MARUs showing the rst third of the duration of a
humpback whale song session, followed by a boat noise, and then showing cessation of song in the Abrolhos archipelago.
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
competitors (Clapham, 2000). Employing basic and
advanced tools to investigate how singing activity is
distributed along the entire distribution of humpback
whales o Brazil is a unique opportunity to further
explore this complex behavior at a larger scale, more
appropriate for the humpback whale.
This work was supported by Fundação O Boticário de
Proteção à Natureza / MacArthur Foundation, Soci-
ety for Marine Mammalogy (Small-Grants-in-Aid of
Research to RSL), Coordination of Improvement of
Higher Education Personnel (PhD scholarships to RSL
and MICG, and Masters scholarships to DPF, PSH, TC
and LKH), The Canon National Parks Science Schol-
ars Program (Technological Innovation Award to RSL),
Animal Behavior Society (Cetacean Behavior and Con-
servation Award to RSL), The Graduate School (Field
of Zoology), the International Students and Scholars
Oce, NY Cooperative Research Unit and the Lab of
Ornithology at Cornell University (RSL), Universidade
Estadual de Santa Cruz, Cetacean Society International
(research grants to MICG) and Arim Componentes. We
thank Alexandre D. Paro, RodrigoS. Amaral, Márcia F.
Araujo, and Lucas G. Collares, for eld assistance, and
Isadora M. Carletti for helping in song analyses. We
thank Captains Roberto C. Fortes, Carlo L. D’Angelo
and Bernardo Cerqueira as well as the other members
of the crews of the boats Tomara, Coronado and Piloto.
We thank Instituto Baleia Jubarte and Projeto Baleia
Jubarte sponsored by Petróleo Brasileiro S.A. (PETRO-
BRAS) for logistic support.We also thank Dr. Fernando
Amaral da Silveira for obtaining research and impor-
tation permits with technical support from FUNDEP.
We want to thank to Professor Linilson Padovese (São
Paulo University) for the collaboration that allowed the
recordings in Serra Grande, and to Alexánder Rosa-
rio and Ignacio Sánchez-Gendriz for the support with
Oceanpods. We also thank Rafael Murakami and Fer-
nando Murakami from Água Viva Sub Ilhéus, and
Erik Tedesco for the help in planning, organizing and
conducting the eld work in Serra Grande.
Alves LCPS, Andriolo A, Zerbini AN, Pizzorno JLA,
Clapham PJ (2009) Record of feeding by humpback
whales (Megaptera novaeangliae) in tropical waters
o Brazil. Marine Mammal Science 25: 416-419
Andriolo A, Martins CCA, Engel MH, PizzornoJL, Más-
Rosa S, Freitas AC, Morete ME, Kinas PG (2006) The
rst aerial survey of humpback whales (Megaptera
novaeangliae) to estimate abundance in the breed-
ing ground o Brazil (Breeding Stock A). Journal of
Cetacean Research and Management 8: 307-311
Andriolo A, Kinas PG, Engel MH, Martins CCA, Runo
AM (2010) Humpback whales within the Brazilian
breeding ground: distribution and population size
estimate. Endangered Species Research 11: 233-243
[doi: 10.3354/esr00282]
Baracho-Neto CG, Neto ES, Rossi-Santos MR, Wedekin
LL, Neves MC, Lima F, Faria D (2012) Site delity
and residence times of humpback whales (Megaptera
novaeangliae) on the Brazilian coast. Journal of the
Marine Biological Association of the United King-
dom 92: 1783-179 [doi: 10.1017/s0025315411002074]
Bortolotto GA, Danilewicz D, Andriolo A, Secchi ER,
Zerbini AN (2016) Whale, Whale, Everywhere:
Increasing Abundance of Western South Atlantic
Humpback Whales (Megaptera novaeangliae) in Their
Wintering Grounds. PLoS ONE 11: e0164596. [doi:
10.1371/journal. pone.0164596]
Brito MRM, Sousa-Lima RS (2014) Progressive changes in
the songs of humpback whales (Megaptera novaeangliae)
in the Abrolhos Bank between the years 2000 and
2002. Anais do XXXII Encontro Anual de Etologia and
V Simpósio Latino-Americano de Etologia 1: 96-97
Bryant PJ, Laerty CM, Laerty SK (1984). Reoccupation
of Laguna Guerrero Negro, Baja California, Mexico,
by gray whales. In: Jones ML, Swartz SL, Leather-
wood S (eds.) The gray whale Eschrichtius robustus.
Academic Press, Orlando, FL, pp. 375–387
Broughton WB (1963) Glossarial index. In: Busnel R (ed.)
Acoustic behavior of animals. Elsevier, New York,
NY, pp.824-911
Broughton, W. B. 1963. Glossarial index. Pages 824–911 in
R. Busnel, ed. Acoustic behavior of animals. Elsevier,
New York, NY.
Broughton, W. B. 1963. Glossarial index. Pages 824–911 in
R. Busnel, ed. Acoustic behavior of animals. Elsevier,
New York, NY.
Casagrande T (2016) Ritmo de atividade vocal de machos de
Baleia Jubarte (Megaptera novaeangliae). MSc thesis. Uni-
versidade Federal do Rio Grande do Norte, Natal, RN
Cerchio S, Jacobsen JK, Norris TF (2001) Temporal
and geographical variation in songs of hump-
back whales, Megaptera novaeangliae: synchronous
change in Hawaiian and Mexican breeding assem-
blages. Animal Behaviour 62: 313-329 [doi: 10.1006/
Cerchio S, Strindberg S, Collins T, Bennett C, Rosenbaum
H (2014) Seismic surveys negatively aect humpback
whale singing activity o northern Angola. PLoS
ONE 9: e86464 [doi: 10.1371/journal.pone.0086464]
38 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
Cholewiak DM, Sousa-Lima RS, Cerchio S (2012) Hump-
back whale song hierarchical structure: Histori-
cal context and discussion of current classication
issues. Marine Mammal Science 29: 312-332 [doi:
Clapham PJ (2000) The Humpback Whale: Seasonal
Feeding and Breeding in a Baleen Whale. In: Mann J,
Connor RC, Tyack PL, Whitehead H (eds) Cetacean
Societies: Field Studies of Dolphins and Whales. The
University of Chicago Press, Chicago, pp 173-196
[ISBN 978-0226503417]
Clapham PJ, Palsboll PJ, Mattila DK, Vasquez O (1992)
Composition and dynamics of humpback whale
competitive groups in the West Indies. Behavior 122:
182-194 [doi: 10.1163/156853992x00507]
Clapham PJ, Bara LS, Carlson CA, Christian MA, Mattila
DK, Mayo CA, Murphy MA, Pittman S (1993) Sea-
sonal occurrence and annual return of humpback
whales, Megaptera novaeangliae, in the southern Gulf
of Maine. Canadian Journal of Zoology 71 (2): 440-
443 [doi: 10.1139/z93-063]
Craig AS, Herman LM (1997) Sex dierences in site delity
and migration of humpback whales (Megaptera novae-
angliae) to the Hawaiian Islands.Canadian Journal of
Zoology75: 1923-1933 [doi: 10.1139/z97-822]
Curie J, Curie P (1880a) Développement, par pression,
de l’électricité polaire dans les cristaux hémièdres à
faces inclinées. Comptes Rendus de l’Académie des
Sciences 91: 294-295
Curie J, Curie P (1880b) Sur l’électricité polaire dans les
cristaux hémièdres à faces inclinées. Comptes Ren-
dus de l’Académie des Sciences 91: 383-386
Danilewicz D, Tavares M, Moreno IB, Ott PH, Trigo CC
(2009) Evidence of feeding by the humpback whale
(Megaptera novaeangliae) in mid-latitude waters of the
western South Atlantic. Marine Biodiversity Records
2 [doi:10.1017/S1755267209000943]
Darling JD, Sousa-Lima RS (2005) Songs indicate interac-
tion between humpback whale (Megaptera novaean-
gliae) populations in the western and eastern south
Atlantic Ocean. Marine Mammal Science 21: 557-566
[doi: 10.1111/j.1748-7692.2005.tb01249.x]
Darling JD, Jones ME, Nicklin CP (2006) Humpback whale
songs: Do they organize males during the breeding
season? Behaviour 143: 1051-1101
Dawbin WH (1966) The seasonal migratory cycle of
humpback whale. In: Norris KS (ed) Whales, dol-
phins, and porpoises. The University of California
Press, Berkeley, pp 146-170
Dawbin WH (1997) Temporal segregation of humpback
whales during migration in southern hemisphere
waters. Memoirs of the Queensland Museum 42:
Elwen SH, Best PB (2004) Environmental factors inuenc-
ing the distribution of southern right whales (Eubal-
aena australis) on the south coast of South Africa I:
broad scale patterns. Marine Mammal Science 20:
567-582 [doi:10.1111/j.1748-7692.2004.tb01180.x]
Engel MH, Martin AR (2009) Feeding grounds of the
western South Atlantic humpback whale population.
Marine Mammal Science 25: 964-969 [doi:10.1111/
Eriksen N, Miller LA, Tougaard J, Helweg DA (2005) Cul-
tural change in the songs of humpback whales (Meg-
aptera novaeangliae) from Tonga. Behaviour 142: 305-
328 [doi: 10.1163/1568539053778283]
Ersts P, Rosenbaum HC (2003) Habitat preference reects
social organization of humpback whales (Megaptera
novaeangliae) on a wintering ground. Journal of
Zoology 260: 337-345
Fainstein R, Summerhayes CP (1982) Structure and origin
of marginal banks o eastern Brazil. Marine Geology
46 (3-4): 199-215 [doi: 10.1016/0025-3227(82)90080-9]
Félix F, Botero-Acosta N (2011) Distribution and behaviour
of humpback whale mother–calf pairs during the
breeding season o Ecuador. Marine Ecology Pro-
gress Series 426: 277-287 [doi:10.3354/meps08984]
Frankel AS, Clark CW, Herman LM, Gabriele CM (1995)
Spatial distribution, habitat utilization, and social
interactions of humpback whales, Megaptera novaean-
gliae, o Hawaii, determined using acoustic and visual
techniques. Canadian Journal of Zoology 73: 1134-1146
Garland EC, Goldizen AW, Rekdahl ML, Constantine
R, Garrigue C, Hauser ND, Poole MM, Robbins J,
Noad MJ (2011) Dynamic horizontal cultural trans-
mission of humpback whale song at the ocean basin
scale. Current Biology 21: 687-691 [doi: 10.1016/j.
Gonçalves MIC (2017) Uso de habitat, comportamento
e emissões acústicas das baleias-jubarte (Megaptera
novaeangliae) na região de Serra Grande - Bahia.
Doctoral Thesis. Universidade Estadual de Santa
Cruz, Ilhéus, BA
Gonçalves MIC, Sousa-Lima RS, Teixeira NN, Morete ME,
Carvalho GH, Ferreira HM, Baumgarten JE (2018)
Low latitude habitat use patterns of a recovering
population of humpback whales. Journal of the
Marine Biological Association of the United King-
dom [doi:10.1017/S0025315418000255]
Herman LM (2016) The multiple functions of male song
within the humpback whale (Megaptera novaean-
gliae) mating system: review, evaluation, and syn-
thesis. Biological Reviews 92: 1795-1818 [doi:10.1111/
R. Sousa-Lima | WIO Journal of Marine Science Special Issue 1 / 2018 23-40
Horton TW, Holdaway RN, Zerbini AN, Hauser N, Gar-
rigue C, Andriolo A, Clapham PJ (2011) Straight as
an arrow: humpback whales swim constant course
tracks during long-distance migration. Biology Let-
ters 7: 674-679 [doi: 10.1098/rsbl.2011.0279]
IBAMA/FUNATURA (1991) Parque Nacional Marinho de
Abrolhos: Plano de Manejo. Instituto Brasileiro do
Meio Ambiente e dos Recursos Renováveis e Funda-
ção Pró-Natureza, Brasília, pp 96
Kennedy AS, Zerbini AN, Rone BK, Clapham PJ (2014) Indi-
vidual variation in movements of satellite-tracked
humpback whales Megaptera novaeangliae in the east-
ern Aleutian Islands and Bering Sea. Endangered
Species Research 23: 187-195 [doi:10.3354/esr00570]
Laland KN,Janik VM (2006) The animal cultures debate.
Trends in Ecology and Evolution 21: 542-547
Lima BR, Sousa-Lima RS (2012) Onde começa o canto
das baleias jubarte. Proceedings of the 15a Reunión
de Trabajo de Expertos en Mamíferos Acuáticos de
América del Sur
Lunardi DG, Engel MH, Macedo RHF (2008) Behavior of
humpback whales, Megaptera novaeangliae (Cetacea:
Balaenopteridae): comparisons between two coastal
areas of Brazil. Revista Brasileira de Zoologia 25:
Martins CCA (2004) O uso sistema de informações geo-
grácas como ferramenta na identição de áreas
prioritarias para a conservação da população de
baleia jubarte, Megaptera novaeangliae, em seu sítio
reprodutivo na costa leste do Brasil. MSc thesis. Uni-
versidade de Brasília, Brasília, DF
Martins CCA, Morete ME, Engel MH, Freitas AC, Secchi
ER, Kinas PG (2001) Aspects of habitat use patterns
of humpback whales in the Abrolhos Bank, Bra-
zil, breeding ground. Memoirs of the Queensland
Museum 47: 563-570
Mate B, Gisiner R, Mobley J (1998) Local and migratory
movements of Hawaiian humpback whales tracked
by satellite telemetry. Canadian Journal of Zoology
76: 863-868
Mattila DK, Clapham PJ, Vásquez O, Bowman RS (1994)
Occurrence, population composition, and habitat
use of humpback whales in Samana Bay, Dominican
Republic. Canadian Journal of Zoology 72: 1898-1907
McDonald MA, Hildebrand JA, Webb SC (1995) Blue and
n whales observed on a seaoor array in the North-
east Pacic. The Journal of the Acoustical Society of
America 98: 712-721
McDonald MA, Hildebrand JA, Wiggins SM (2006)
Increases in deep ocean ambient noise in the North-
east Pacic west of San Nicolas Island, California.
The Journal of the Acoustical Society of America
120: 711-718
Mobley JR, Herman LM (1985) Transience of social ali-
ations among humpback whales (Megaptera novaean-
gliae) on the Hawaiian wintering grounds. Canadian
Journal of Zoology 63: 762-772
Morete ME, Bisi TL, Pace RM, Rosso S (2008) Fluctuating
abundance of humpback whales (Megaptera novaean-
gliae) in a calving ground o coastal Brazil. Journal
of Marine Biological Association of the United King-
dom 88: 1229-1235
Noad MJ, Cato DH (2007) Swimming speeds of sing-
ing and non-singing humpback whales during
migration. Marine Mammal Science 23: 481-495
Noad MJ, Cato DH, Bryden MM, Jenner M-N, Jenner KCS
(2000) Cultural revolution in whale songs. Nature
408: 537 [doi: 10.1038/35046199]
Payne RS, McVay S (1971) Songs of humpback whales. Sci-
ence 173: 585-597 [doi: 10.1126/science.173.3997.585]
Payne K, Payne R (1985) Large scale changes over 19 years
in songs of humpback whales in Bermuda. Zeitschri
für Tierpsychologie 68: 89-114 [doi: 10.1111/j.1439-
Payne K, Tyack P, Payne R (1983) Progressive changes
in the song of humpback whales songs (Megaptera
novaeangliae): A detailed analysis of two seasons
in Hawaii. In: Payne R (ed.) Communication and
behavior of whales. AAAS Selected Symposium 76,
Colorado, pp 9-57
Pavanato HJ, Wedekin LL, Guilherme-Silveira FR, Engel
MH, Kinas PG (2017) Estimating humpback whale
abundance using hierarchical distance sampling.
Ecological Modelling 358: 10-18 [doi: 10.1016/j.
Queiróz TSM (2010). Atividade vocal de baleias jubarte,
Megaptera novaeangliae, na estação reprodutiva de
2004 no Banco dos Abrolhos (Bahia, Brasil) (Bache-
lor thesis). Universidade Federal de Minas Gerais,
Minas Gerais, Brazil
Richardson WJ, Greene CR, Malme Jr. CI, Thomson DH
(1995) Marine mammals and noise. Academic Press,
San Diego, California. 576 pp
Rossi-Santos MR, Neto ES, Baracho CG, Cipolotti SR,
Marcovaldi E, Engel MH (2008) Occurrence and dis-
tribution of humpback whales (Megaptera novaean-
gliae) on the north coast of the State of Bahia, Brazil,
2000-2006. ICES Journal of Marine Science 65: 667-
673 [doi: 10.1093/icesjms/fsn034]
Sánchez-Gendriz I, Padovese LR (2016) Underwater
soundscape of marine protected areas in the south
40 WIO Journal of Marine Science Special Issue 1 / 2018 23-40 | R. Sousa-Lima
Brazilian coast. Marine Pollution Bulletin 105: 65-72
[doi: 10.1016/j.marpolbul.2016.02.055]
Schevill WE (1964) Underwater sounds of cetaceans. In:
Tavolga WN (ed) Marine Bioacoustics. Pergamon
Press, Oxford, UK, 307-316
Schevill WE, Watkins WA (1962) Whale and porpoise
voices. Woods Hole Oceanographic Institution,
Woods Hole, Massachusetts. 24pp
Schreiber OW (1952) Some sounds from marine life in
the Hawaiian area. The Journal of the Acoustical
Society of America 24: 116
Siciliano S (1997) Características da população de baleias-
-jubarte (Megaptera novaeangliae) da costa brasileira,
com especial referência aos Bancos de Abrolhos.
Universidade Federal Rural do Rio de Janeiro, Rio
de Janeiro. 113 pp
Simão M, Moreira SC (2005) Vocalizations of a female
humpback whale in Arraial do Cabo (RJ, Brazil).
Marine Mammal Science 21: 150-153
Smultea MA (1994) Segregation by humpback whale
(Megaptera novaeangliae) cows with a calf in coastal
habitat near the island of Hawaii. Canadian Journal
of Zoology 72: 805-811
Sousa-Lima RS, Morete ME, Fortes RC, Freitas AC, Engel
MH (2002) Impact of boats on the vocal behavior
of humpback whales o Brazil. The Journal of the
Acoustical Society of America 112: 2430-2431
Sousa-Lima RS (2007) Acoustic ecology of humpback
whales (Megaptera novaeangliae) in the Abrolhos
National Marine Park, Brazil (Doctoral dissertation).
Cornell University, Ithaca, USA, 205 pp
Sousa-Lima RS, Clark CW (2008) Modelling the eects of
boat trac on the uctuations of singing activity of
humpback whales in the Abrolhos National Marine
Park, Brazil. Canadian Acoustics 36: 174-181
Sousa-Lima RS, Clark CW (2009) Whale sound recording
technology as a tool for assessing the eects of boat
noise in a Brazilian Marine Park. Park Science 26:
Sousa-Lima RS, Norris T, Oswald J, Fernandes DP (2013)
A review and inventory of xed autonomous record-
ers for passive acoustic monitoring of marine mam-
mals. Aquatic Mammals 39: 23-53
Stevick PT, Godoy LP, Mcosker M, Engel MH, Allen J
(2006) Movement of a humpback whale from Abrol-
hos Bank, Brazil to South Georgia. Journal of Ceta-
cean Research and Management 8: 297-300
Tchernichovski O, Lints TJ, Deregnaucourt S, Cimenser
A, Mitra PP (2004) Studying the song develop-
ment process: rationale and methods. Annals of
the New York Academy of Sciences 1016: 348-363
Tyack P (1981) Interactions between singing Hawaiian
humpback whales and conspecics nearby. Behav-
ioral Ecology and Sociobiology 8: 105-116 [doi:
Tyack P, Whitehead HP (1983) Male competition in large
groups of wintering humpback whales. Behaviour
83: 132-154 [doi: 10.1163/156853982X00067]
Urick RJ (1983) Principles of Underwater Sound. Penin-
sula Pub, McGraw-Hill, New York. 444 pp
Videsen SKA, Bejder L, Johnson M, Madsen PT (2017)
High suckling rates and acoustic crypsis of hump-
back whale neonates maximise potential for
mother–calf energy transfer. Functional Ecology 31:
1561-1573 [doi:10.1111/1365-2435.12871]
Watkins WA (1967) Air-borne sounds of the humpback
whale, Megaptera novaeangliae. Journal of Mammal-
ogy 48: 573-578
Wedekin LL, Neves MC, Marcondes MC, Baracho C,
Rossi-Santos MR, Engel MH, Simões-Lopes PC
(2010) Site delity and movements of humpback
whales (Megaptera novaeangliae) on the Brazilian
breeding ground, southwestern Atlantic. Marine
Mammal Science 26: 787-802 [doi: 10.1111/j.1748-
Whitehead HP (1983) Structure and stability of humpback
whale groups o Newfoundland. Canadian Journal of
Zoology 61: 1391-1397 [doi:]
Whitehead HP (1985) Why whales leap. Scientic Ameri-
can 252: 84-93
Winn HE, Winn LK (1978) The Song of the Humpback
Whale Megaptera novaeangliae in the West Indies.
Marine Biology 47:97-114
Zerbini AN, Andriolo A, Heide-Jørgensen MP, Pizzorno
JL, Maia YG, Van Blaricom GR, De Master DP,
Simões-Lopes PC, Moreira S, Bathlem C (2006) Sat-
ellite monitored movements of humpback whales
Megaptera novaeangliae in the Southwest Atlantic
Ocean. Marine Ecology Progress Series 313: 295-304
Zerbini AN, Ward EJ, Kinas PG, Engel MH, Andriolo A
(2011) A Bayesian assessment of the conservation
status of humpback whales (Megaptera novaeangliae)
in the western South Atlantic Ocean. Journal of
Cetacean Research and Management, Special Issue
3: 131-144
Zoidis AM, Smultea MA, Frankel AS, Hopkins JL, Day
AJ, McFarland AS, Whitt AD, Fertl D (2008) Vocal-
izations produced by humpback whale (Megaptera
novaeangliae) calves recorded in Hawaii. The Journal
of the Acoustical Society of America 123: 1737-1746
... Les odontocètes (cétacés à dents), utilisent même un système de sonar (envoi et réception d'ondes acoustiques) pour sonder leur environnement. La bioacoustique marine s'est développée depuis l'avènement d'appareils capables d'écouter dans l'eau (en général nommés hydrophones, variante du microphone adaptée à l'impédance acoustique de l'eau), ainsi que de systèmes de stockage et d'analyse de l'information (ordinateurs essentiellement de nos jours) -voir pour un exemple de suivi à long terme l'article de Sousa-Lima et al. 2018 [130]. La bioacoustique actuelle est multidisciplinaire, incluant des domaines tels que la biologie naturellement, la physique, l'informatique, le traitement du signal ... Ce champ dispose désormais d'ouvrages de références complets tels que celui de Au et Hastings "Principles of marine bioacoustics" [7] ou celui de Zimmer consacré au suivi des cétacés par la bioacoustique [157]. ...
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La surveillance par acoustique passive est un outil d'importance croissante pour l'étude des mammifèresmarins. Cette thèse pose des nouveaux modèles pour l'étude du plus grand d'entre eux, la baleine bleue(Balaenoptera musculus). Pour ce faire, nous avons enregistré un corpus inédit dans l'archipel de Humboldt aunord du Chili. Nos données révèlent un chant caractéristique de la baleine bleue 'chilienne', dont nous étudionsla structure pulsée et l'évolution au cours des dernières décennies. Le classement en signal tonal ou non-tonalnous permet, en nous focalisant sur la fréquence fondamentale mise à jour, de quantifier la baisse en fréquencedes chants et d'effectuer une comparaison au niveau mondial. Notre troisième contribution est une méthode delocalisation mono-hydrophone basée sur des simulations de propagation par éléments spectraux. C’est à notreconnaissance le premier modèle de ce type, implémenté en milliers d’heures de calcul haute performance.
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Summary 1. The migration of humpback whales to and from their breeding grounds results in a short, critical time period during which neonatal calves must acquire sufficient energy via suckling from their fasting mothers to survive the long return journey. 2. Understanding neonate suckling behaviour is critical for understanding the energetics and evolution of humpback whale migratory behaviour and for informing conservation efforts, but despite its importance, very little is known about the details, rate and behavioural context of this critical energy transfer. 3. To address this pertinent data gap on calf suckling behaviour, we deployed multi-sensor Dtags on eight humpback whale calves and two mothers allowing us to analyse detailed suckling and acoustic behaviour for a total of 68�8 h. 4. Suckling dives were performed 20�7 � 7% of the total tagging time with the mothers either resting at the surface or at depth with the calves hanging motionless with roll and pitch angles close to zero. 5. Vocalisations between mother and calf, which included very weak tonal and grunting sounds, were produced more frequently during active dives than suckling dives, suggesting that mechanical stimuli rather than acoustic cues are used to initiate nursing. 6. Use of mechanical cues for initiating suckling and low level vocalisations with an active space of <100 m indicate a strong selection pressure for acoustic crypsis. 7. Such inconspicuous behaviour likely reduces the risk of exposure to eavesdropping predators and male humpback whale escorts that may disrupt the high proportion of time spent nursing and resting, and hence ultimately compromise calf fitness. 8. The small active space of the weak calls between mother and calf is very sensitive to increases in ambient noise from human encroachment thereby increasing the risk of mother– calf separation.
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The western South Atlantic (WSA) humpback whale population inhabits the coast of Brazil during the breeding and calving season in winter and spring. This population was depleted to near extinction by whaling in the mid-twentieth century. Despite recent signs of recovery, increasing coastal and offshore development pose potential threats to these animals. Therefore, continuous monitoring is needed to assess population status and support conservation strategies. The aim of this work was to present ship-based line-transect estimates of abundance for humpback whales in their WSA breeding ground and to investigate potential changes in population size. Two cruises surveyed the coast of Brazil during August-September in 2008 and 2012. The area surveyed in 2008 corresponded to the currently recognized population breeding area; effort in 2012 was limited due to unfavorable weather conditions. WSA humpback whale population size in 2008 was estimated at 16,410 (CV = 0.228, 95% CI = 10,563–25,495) animals. In order to compare abundance between 2008 and 2012, estimates for the area between Salvador and Cabo Frio, which were consistently covered in the two years, were computed at 15,332 (CV = 0.243, 95% CI = 9,595–24,500) and 19,429 (CV = 0.101, 95% CI = 15,958–23,654) whales, respectively. The difference in the two estimates represents an increase of 26.7% in whale numbers in a 4-year period. The estimated abundance for 2008 is considered the most robust for the WSA humpback whale population because the ship survey conducted in that year minimized bias from various sources. Results presented here indicate that in 2008, the WSA humpback whale population was at least around 60% of its estimated pre-modern whaling abundance and that it may recover to its pre-exploitation size sooner than previously estimated.
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Fixed autonomous acoustic recording devices (autonomous recorders [ARs]) are defined as any electronic recording system that acquires and stores acoustic data internally (i.e., without a cable or radio link to transmit data to a receiving station), is deployed semi-permanently underwater (via a mooring, buoy, or attached to the sea floor), and must be retrieved to access the data. More than 30 ARs were reviewed. They varied greatly in capabilities and costs, from small, hand-deployable units for detecting dolphin and porpoise clicks in shallow water to larger units that can be deployed in deep water and can record at high-frequency bandwidths for over a year, but must be deployed from a large vessel. The capabilities and limitations of the systems reviewed herein are discussed in terms of their effectiveness in monitoring and studying marine mammals.
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Calling blue and fin whales have been tracked using relative travel times and amplitudes from both direct and multipath arrivals to a seafloor array of seismometers. Calls of three fin whales swimming in the same general direction, but several kilometers apart, are believed to represent communication between the whales because of signature differences in call character, an alternating call pattern, and coordination of call and respiration times. Whale call tracks, call patterns, call character, and swimming speeds were examined during periods with and without the presence of noise. Noise sources included airguns, when the whales were subject to sound levels of up to 143 dB P-P (peak-to-peak) re: 1 pPa over the 10 to 60-Hz band, and transits of merchant ships, when the whales received continuous levels up to 106 dB rms re: I / • Pa over the 10 to 60-Hz band (115 dB P-P). Whale responses associated with these noises remain arguable. ¸ 1995 Acoustical Society of America.
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Experiments were performed to evaluate the impact of boat approaches on the vocal behavior of humpback whales that breed around the Abrolhos archipelago off the Brazilian coast. Vocalizing whales were located by monitoring the amplitude of each individual’s sounds. Silent approaches to focal singers were performed using a small zodiac with an improvised sail. Songs were recorded with one hydrophone connected to a portable DAT recorder before and during the approach of a vessel. Spectrograms were correlated to each whale’s activity and position with respect to the vessel. Differences in song variables of two individuals were tested when the motor was ON and OFF. Both whales sang shorter versions of their songs when exposed to engine noise. No alteration in mean phrase duration was detected, but the number of phrases in each theme decreased. Three individuals interrupted their songs after a motor boat switched gears within 300 m, and resumed singing when the engine was returned to neutral. The limited number of observables calls for further investigation to evaluate the consequences of boat impact. More reliable information will allow regulation to achieve sustainable tourism activity in the area. [Work supported by FBPN, MacArthur Foundation, Society for Marine Mammalogy, Instituto Baleia Jubarte.]
Many marine mammals communicate by emitting sounds that pass through water. Such sounds can be received across great distances and can influence the behavior of these undersea creatures. In the past few decades, the oceans have become increasingly noisy, as underwater sounds from propellers, sonars, and other human activities make it difficult for marine mammals to communicate. This book discusses, among many other topics, just how well marine mammals hear, how noisy the oceans have become, and what effects these new sounds have on marine mammals. The baseline of ambient noise, the sounds produced by machines and mammals, the sensitivity of marine mammal hearing, and the reactions of marine mammals are also examined. An essential addition to any marine biologists library, Marine Mammals and Noise will be especially appealing to marine mammalogists, researchers, policy makers and regulators, and marine biologists and oceanographers using sound in their research.
Unusual wheezing blows were recorded from humpback whales. This sound was audible both underwater and in air, and appeared to be produced at the blowhole during exhalation. The wheezing blow was composed of frequencies up to 2 kcps and lasted about 2 sec. The in-air and underwater components of this sound are compared. The wheezing blow is contrasted to normal blows, which can be plainly heard in air but are not audible underwater, and to the usual underwater calls, which can not be heard in air. Spectrographic analyses of the three types of sounds are presented. The sounds of normal whale blows are described as variable; this is reflected in the variety of opinion in the literature on whales.