Grande parte das interações entre os animais envolve algum tipo de

Transcription

Universidade Federal do Rio Grande do Norte
Centro de Biociências
Programa de Pós-Graduação em Psicobiologia
Comportamento e ecologia acústica da baleia jubarte (Megaptera novaeangliae)
na região Nordeste do Brasil
Marcos Roberto Rossi-Santos
Natal
2012
MARCOS ROBERTO ROSSI-SANTOS
Tese apresentada à Universidade
Federal do Rio Grande do Norte,
para obtenção do título de Doutor
em Psicobiologia.
Natal
2012
1
MARCOS ROBERTO ROSSI-SANTOS
Tese apresentada à Universidade
Federal do Rio Grande do Norte,
para obtenção do título de Doutor
em Psicobiologia.
Orientador: Dr. Flávio José de Lima
Silva
Ficha Catalográfica preparada pela
Biblioteca Central
Natal
2012
2
É com grande respeito que dedico
esse trabalho à memória de
meu avô Antonio Carlos Ottoni Rossi
e à amorosa presença de minha avó
Maria de Lourdes Bueno Rossi,
que me iniciaram no caminho da
admiração pela natureza e pela música
4
Baleia...
Você conheceu todos
Os poderosos oceanos.
O segredo dos tempos pretéritos
Pode ser ouvido em seu canto.
Ensina-me sua linguagem
Para que eu possa compreender
As raízes da história
Da gênese de nosso mundo.
Sams & Carson, 2000
Sams, J. & Carson, D. 2000. Cartas xamânicas:
A descoberta do poder através da energia dos animais. Rio de Janeiro: Rocco.
5
TÍTULO: Comportamento e ecologia acústica da baleia jubarte (Megaptera
novaeangliae) na região Nordeste do Brasil
PALAVRAS-CHAVE: comportamento de canto, ecologia acústica, baleia jubarte,
ruídos antropogênicos, estoque reprodutivo A, nordeste do Brasil
RESUMO: O conceito de ecologia acústica envolve a relação entre os organismos
vivos e o seu ambiente sonoro e é aplicado no presente trabalho para estudar o
contexto no qual ocorreu o comportamento de canto da baleia jubarte (Megaptera
novaeangliae), considerado o mais complexo comportamento reprodutivo (display)
da natureza, na costa nordeste do Brasil, fora da concentração reprodutiva do Banco
de Abrolhos, entre os anos de 2005 e 2010. Analiso a ocorrência de machos
cantores em diferentes estruturas de grupo, sua distribuição espacial e prováveis
relações com fatores oceanográficos, como profundidade, regime de marés e fases
da lua. Também descrevo a estrutura acústica e a variação temporal do
comportamento de canto, baseado em medições de frequência e tempo dos cantos,
fora do Banco de Abrolhos, além de comparar a complexidade do canto, registrada
no mesmo período de estudo, entre o Banco de Abrolhos (16°- 19° S, 37°- 39° W), e
a Costa Norte adjacente, aqui considerada desde Itacaré (14° S, 38° W) a Aracajú
(11° S, 37° W). Ainda busco descrever e analisar as fontes de ruídos antropogênicos
no ambiente marinho da área de estudo, produzidos pela atividade de exploração de
petroleo e gás e também pelo turismo de observação de baleias, relacionando-os
com o nicho acústico utilizado pela jubarte. Os resultados indicaram uma grande
plasticidade no comportamento de canto, evidenciado pela ocorrência dos cantores
em diversas estruturas sociais, de indivíduos solitários a grupos contendo outros
6
animais, inclusive fêmeas com filhotes, bem como pela diversidade que compõe o
canto da espécie, quando comparado entre duas regiões dentro da mesma área de
reprodução, como o Banco de Abrolhos e a Costa Norte, que apresenta
características oceanográficas distintas. A distribuição dos machos cantores parece
estar relacionada com a extensão da plataforma continental na área de estudo. Os
ruídos antropogênicos produzidos demonstraram uma faixa de frequências,
amplitude
sonora
e
intensidade
capazes
de
interferir
acusticamente
no
comportamento de canto da espécie, podendo resultar em distúrbios durante o
período de reprodução da espécie na costa brasileira. Implicações sobre os
resultados obtidos na teoria do sistema de acasamento da espécie são discutidas.
Dessa forma, pretendo contribuir com o tema da ecologia acustica e gerar
informações que subsidiem a conservação da baleia jubarte.
7
ABSTRACT:
The acoustic ecology concept involve the relation between the live organisms and
their sound environment and is applied in the present work to study the context in
which the humpback whale (Megaptera novaeangliae) singing behavior, known as
the most complex display in the nature, occurred in the northeastern Brazilian coast,
outside the core area of Abrolhos Bank, between 2005 and 2010.I analyze the singer
male occurrence , their spatial distribution and probable relations with oceanographic
features, such as depth, tide regimen and moon phases. I also describe the acoustic
structure and temporal variation of the singing behavior, based on song frequency
and time measurements outside the Abrolhos Bank, and further compare the song
complexity, registered in the same period, between Abrolhos Bank (16°- 19° S, 37°39° W) and the adjacent North Coast, herein considered from Itacaré (14° S, 38° W)
to Aracaju (11° S, 37° W). Additionally, I look for describe and analyze anthropogenic
noise sources in the marine environment of the study area, produced by the oil
industry as well as by the whale watching operation, relating their frequencies to the
acoustic niche utilized by the humpbacks. The results indicated a great plasticity in
the singing behavior, evidenced by the occurrence of singer males in diverse social
structures, from solitary individuals to other groups, even containing females and
calves, as well as by the diversity which compound the song, when compared
between two regions inside the same breeding area, which present distinct
oceanographic characteristics. The singer male distribution may be related with the
continental shelf extent along the study area. The anthropogenic noise presented
frequency range, amplitude and sound intensity in potential to interfere acoustically in
the singing behavior of the species, may resulting in disturbance during the breeding
season in the Brazilian coast. Implications about the obtained results in the
8
humpback whale mating system are discussed. In this way, I pretend to contribute
with the acoustic ecology subject and provide information to subsidize humpback
whale conservation.
Key-words: singing behavior, acoustic ecology, humpback whale, anthropogenic
noise, Breeding Stock A, Northeastern Brazil
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SUMÁRIO
i. Resumo............................................................................................
06
ii. Abstract...........................................................................................
08
iii. Agradecimentos...............................................................................
12
1- Introdução........................................................................................
13
1.1) Comunicação animal e ecologia.....................................................
16
1.2) Ruídos e impactos sonoros no ambiente marinho.........................
18
1.3) Caracterização da espécie.............................................................
19
1.3.1) Ocorrência e Distribuição.............................................................
22
1.3.2) Ameaças e Status de Conservação da espécie...........................
24
1.4) Expansão da população de baleias jubarte no Brasil......................
25
1.5) Ecologia acústica, comportamento e seleção sexual......................
26
2- Objetivos, Hipóteses e Predições.................................................
27
2.1- Ojetivos.......................................................................................
2.1.1- Objetivo Geral..................................................................
27
2.1.2- Objetivos específicos.......................................................
27
2.2- Hipóteses e predições...............................................................
28
3- Materiais e Método...........................................................................
29
3.1- Área de Estudo...................................................................
29
3.2- Coleta de Dados..................................................................
32
3.2.1- Cruzeiros de Pesquisa.....................................................
32
3.2.2- Bioacústica.......................................................................
34
3.2.3 - Sistema de Informações Geográficas..............................
35
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4- Resultados.........................................................................................
4.1-Artigo 1................................................................................
36
37
Ecologia comportamental de canto em baleias jubarte (Megaptera
novaeangliae) na região Nordeste do Brasil
4.2- Artigo 2................................................................................
71
Estrutura acústica e variação temporal do comportamento de canto
em baleias jubarte (Megaptera novaeangliae) na área de reprodução
da costa do Brasil.
4.3- Artigo 3...............................................................................
102
Industria do Petróleo e poluição acústica na área de reprodução da
baleia jubarte (Megaptera novaeangliae) no Oceano Atlantico sul
ocidental.
4.4- Artigo 4...............................................................................
135
Efeitos dos ruídos produzidos pelo turismo de observação no
comportamento da baleia jubarte (Megaptera novaeangliae) na área
de reprodução na costa do Brasil
5- Considerações finais....................................................................
156
6- Referências Bibliográficas...........................................................
160
7-Anexo.................................................................................................
168
11
Agradecimentos
Primeiramente, às baleias-jubarte que ainda guardam o mistério de sua
mensagem no mar e refletem no seu olhar introspectivo o espelho do próprio mundo
exterior.
Muitas pessoas contribuíram com a construção desse trabalho, de diversas
formas. Algumas com intenso apoio, enquanto outras aumentando o desafio em
concretizá-lo. Sou grato a todos, pois me deram força para vencer mais essa etapa.
Agradeço o apoio incondicional de minha família – meus pais e irmãos, e
especialmente minha mulher amada e companheira Renata e nossa querida filha
Moara.
Tenho o prazer de contar como membros da banca, algumas pessoas que
muito colaboraram para minha formação profissional. Obrigado Jeff Podos e
Emygdio Monteiro Filho pelos muitos ensinamentos, oportunidades e vivências
compartilhadas. Obrigado também ao Flávio Lima pela orientação e pelo
aprendizado nestes anos recentes.
Agradeço o suporte financeiro dos patrocinadores do Instituto Baleia Jubarte
durante os anos deste trabalho: Petrobras Ambiental, Aracruz Celulose, Fundação
AVINA e Fundação Garcia D´Ávila. Também à CAPES pela concessão da bolsa de
doutorado.
William Rossiter, da Cetacean Society International, vem fornecendo
inestimável apoio a muitas viagens internacionais que contribuíram com minha
formação, enquanto David Janiger se tornou um grande guardião de artigos
científicos fornecendo prontamente desde publicações atuais e outras de antigas
datas.
Por fim, agradeço à Mãe Natureza e ao Deus Pai, por nos ensinar a respeitar
todos os seres que habitam esse planeta azul.
Todos juntos somos um!
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1. INTRODUÇÃO
A comunicação animal sempre exerceu um grande fascínio na humanidade.
Na história da ciência, a civilização grega avançou muito acerca do conhecimento
natural, pois integravam suas descobertas à visão global do Universo ou Cosmo.
Suas perguntas sempre se dirigiam à “essência” da questão e nunca ao
funcionamento, com forte característica no empirismo, enfatisando o fenômeno,
como faria Johan Von Goethe séculos depois, ao invés de valorizar as medições
precisas e teorias como na ciência moderna (vide anexo 1).
Assim, a ciência na Grécia impregnava-se do espírito de admiração e de
veneração diante dos enigmas do mundo, onde tudo tinha um sentido. Pitágoras,
pensador grego característico, acreditava que por trás da realidade material existia
um mundo espiritual, cujos seres e forças plasmavam o mundo físico, permeado
pelo que ele chamava de “música das esferas”: um fluir de harmonias, uma ordem
de relações numéricas e proporções que teriam afinidade com a música. Ainda
reencontramos tais relações, por exemplo, entre o comprimento de cordas cuja
vibração produz sons considerados harmônicos. Os números não eram apenas
designações de quantidade, mas possuiam um conteúdo espiritual próprio (Lanz,
2004).
Neste contexto, vem da Grécia a própria denominação do grupo dos
cetáceos: Ketus, significando “grande peixe”, ao mesmo tempo “monstro marinho”,
tamanho era o fascínio que estes animais exerciam na mente humana, sendo
habitantes de um domínio sagrado e misterioso para o homem, como os oceanos.
13
Depois de centenas de anos, esses animais ainda nos maravilham, pelo seu
modo de vida, por sua inteligência, por seus mistérios. O canto da baleia jubarte é
um dos mais complexos comportamentos acústicos do reino animal (Wilson, 1975),
e vem despertando fascínio tanto em admiradores quanto para o meio científico.
Embora provavelmente ouvido por marinheiros durante séculos, as primeiras
gravações de canto das jubarte foram feitas por navios da Marinha dos EUA no final
dos anos 1950. Os cientistas reconheceram esses sons como vindos de baleias
jubarte na década de 1960,ea primeira descrição técnica do canto foi publicado por
Payne & McVay (1971).
Desde então, a estrutura geral do canto, bem como as características básicas
de machos cantores têm sido descritas (ex.: Tyack, 1981; Payne & Payne, 1985;
Darling et al., 2006). Essas características, combinadas com observações de baleias
cantando levaram a várias ideias sobre a função ou o papel do canto nas áreas de
reprodução, entretanto correlações com a paisagem acústica onde se inserem essas
baleias têm sido pouco abordadas. O impacto de sons antropogênicos sobre a
comunicação dos cetáceos é um assunto emergente, de crescente interesse (ex:
Hatch & Wrigth, 2007).
Nesse estudo, pretendo contribuir com esse tema de ecologia acústica da
baleia jubarte, contextualizando o comportamento de canto na estrutura social
dentro da área de reprodução desses animais na costa do Brasil. Pretendo também
investigar a relação entre o comportamento de canto e características ambientais,
como profundidade e extensão da plataforma continental, regionalizadas dentro
dessa área. Ainda busco descrever e analisar fontes de ruídos produzidos pelo
homem no ambiente marinho da área de estudo, relacionando-os com o nicho
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acústico utilizado pela jubarte. Considero aqui como conceito de ecologia acústica o
estudo da relação entre os organismos vivos e o seu ambiente sônico (paisagem
sonora ou soundscape), em uma adaptação de Truax (1999).
Esse trabalho está organizado em quatro artigos independentes, cada qual
com sua estrutura integral (apresentação de tema, métodos, resultados e
discussões), mas que se complementam para compor uma visão mais ampliada dos
resultados desse tema de estudo.
No Artigo 1 – Ecologia comportamental do canto em baleias jubarte
(Megaptera novaeanglie) na região nordeste do Brasil – estudo o comportamento de
machos cantores em diferentes estruturas de grupo, sua distribuição espacial e
possíveis relações com fatores oceanográficos, como profundidade, regime de
marés e fases da lua.
No Artigo 2 – Estrutura acústica e variação temporal do comportamento de
canto – descrevo a estrutura física baseado em medições de frequência e tempo dos
cantos, fora da área de concentração do Banco de Abrolhos. Também comparo a
complexidade do canto registrada no Banco de Abrolhos e Costa Norte adjacente.
No Artigo 3 – Indústria do Petróleo e poluição acústica na área de reprodução
da baleia jubarte – caracterizo os ruídos produzidos dentro do contexto da
exploração de óleo e gás no ambiente marinho da região de estudo, principalmente
advindos de plataformas e embarcações petrolíferas.
No Artigo 4 – Efeitos dos ruídos produzidos pelo turismo de observação no
comportamento da baleia jubarte – descrevo as embarcações destinadas ao whale
watching em Praia do Forte, litoral norte do Estado da Bahia, assim como a emissão
de ruídos gerados por elas durante a aproximação aos grupos de jubarte. Busco
15
discutir o impacto desses sons antropogênicos no comportamento das baleias
durante a época reprodutiva.
Nas minhas considerações finais, trago um alinhamento entre as discussões
apresentadas em cada um dos artigos.
Ainda em caráter introdutório, contextualizando o tema de comunicação
animal, trago referências sobre o histórico da pesquisa na área; apresento
informações sobre ruídos e impactos sonoros em ambiente marinho e trago a
caracterização, a ocorrência e distribuição, as ameaças e status de conservação da
espécie e a expansão da população de baleias jubarte no Brasil. Ainda introduzo
conceitos sobre ecologia acústica, comportamento e seleção sexual.
Por fim, em anexo, trago uma reflexão sobre uma outra abordagem na
concepção científica – a ciência Goetheana – sustentada pelo desenvolvimento da
observação fenomenológica no cientista.
1.1) Comunicação animal e ecologia
Parte da teoria sobre comunicação animal a descreve como um processo de
transmissão de informações que envolve um indivíduo emissor emitindo algum tipo
de sinal para outro indivíduo receptor, onde supostamente este sinal envolve algo
desconhecido para este. A informação contida é definida pela habilidade do sinal em
reduzir incerteza ao indivíduo receptor (ex: Bradbury & Vehrencamp, 1998). Essa
visão clássica de comunicação envolvendo a redução de incertezas é similar ao
nosso típico uso sobre a comunicação humana de transmissão de conhecimento
através de uma linguagem.
16
Em contraste, para o estudo dos cetáceos vem se buscando uma perspectiva
mais ampla, que inclua feições complementares de comunicação não abordadas
nesta visão clássica, sendo uma delas a influência do ambiente no processo de
comunicação (ver Tyack, 2000). A maioria dos sinais é modificada assim que passa
pelo ambiente, desde o emissor ao receptor, o que implica em degradação inicial
deste sinal, mas que resulta em informação ao receptor. Por exemplo, alguns
pássaros podem estimar a distância de um indivíduo emissor pela degradação do
sinal (McGregor & Krebs, 1984; Naguib, 1998).
Sabe-se que animais como morcegos e golfinhos aprendem sobre seu
ambiente escutando os ecos dos sons que eles mesmos produzem, chamado
ecolocalização (ex: Tyack, 2000). Dentro dos estudos de comunicação animal em
cetáceos, abrem-se questões básicas de investigação, tais como as funções pelas
quais os animais desenvolvem sinais particulares e quais os fatores que fazem estes
sinais possuirem características peculiares. Tais questões são fundamentais para
decifrar como e para que os sinais de comunicação são elaborados e porque cada
um deles possui feições específicas. Isso se inclui na abordagem de ecologia e
comportamento do presente trabalho.
17
1.2) Ruídos e impactos sonoros no ambiente marinho
O ambiente acústico marinho por si já é uma fonte de ruído e poluição sonora
que reflete na percepção e resposta comportamental para diversos animais
(McCauley et al., 2000a, 2000b; Miller et al., 2000). O ambiente acústico marinho
que as baleias encontram hoje é diferente do que estavam habituadas há cerca de
50 anos atrás, principalmente em área de reprodução, onde, como animais
migratórios, passam cerca de seis meses por ano.
Um grande crescimento da zona costeira mundial, resultando em grande frota
de embarcações e da indústria do petróleo resultou em um ambiente onde os níveis
de poluição acústica podem chegar a molestar os indivíduos, causando danos
temporários ou até mesmo permanentes em sua fisiologia e comportamento (ex:
Richardson et al., 1995, Johnson et al., 2007).
Outra fonte em potencial de distúrbio acústico é a indústria de observação de
cetáceos (Whale-watching), que vem sendo fomentada por conservacionistas no
mundo todo como uma alternativa para o retorno da caça de baleias, além de fonte
de renda extra para populações locais. De forma ideal, o whale-watching deveria ser
conduzido dentro de um nível sustentável, maximizando os retornos potenciais ao
mesmo tempo que minimiza o impacto sobre as espécies observadas. Uma sobreexposição aos ruídos produzidos por embarcações pode resultar em abandono de
área pela espécie de interesse, levando, em ultima instância, ao colapso da
viabilidade local de operação da indústria de whale-watching (Higham & Lusseau,
2007).
18
1.3) Caracterização da espécie
A baleia jubarte, Megaptera novaeangliae (Cetacea, Balaenopteridae), é uma
espécie cosmopolita e distribui-se por todos os oceanos (Clapham & Mead, 1999).
É considerada um rorqual devido a presença de sulcos ventrais, estruturas
que se expandem durante a alimentação que se tornam de coloração avermelhada.
As principais características externas da jubarte são: número de pregas ventrais,
tamanho e forma da nadadeira peitoral, equivalente a aproximadamente um terço do
comprimento total do animal (figura 1), coloração e formato da nadadeira caudal
(Chittleborough, 1965). A jubarte também é chamada de baleia corcunda devido à
tendência de arquear o corpo quando mergulha.
A jubarte pode atingir até dezesseis metros de comprimento e pesar até
quarenta toneladas (Chittleborough, 1965; Clapham & Mead, 1999). A coloração do
dorso é preta, e a parte ventral varia de totalmente preta a totalmente branca. A
nadadeira dorsal é pequena e varia de formato, podendo ser falcada ou
arredondada. Na maioria dos animais ocorrem manchas brancas na face ventral da
nadadeira caudal, que variam de indivíduo para indivíduo, permitindo identificá-las
por fotografias (Katona & Whitehead, 1981).
19
Figura 1: A baleia jubarte (Megaptera novaeangliae), com detalhe para as pregas
ventrais e grandes nadadeiras peitorais, realizando comportamento de salto, no
litoral norte do estado da Bahia.
Jubartes
machos
e
fêmeas
atingem
a
maturidade
sexual
com
aproximadamente 2 a 5 anos de idade e a maturidade física 10 anos depois
(Chittleborough, 1965; Clapham, 1992). A única diferença anatômica externamente
visível entre machos e fêmeas é a presença de um lobo hemisférico na região
urogenital das fêmeas localizada logo após a porção posterior da abertura genital
(True,1904).
As fêmeas em geral dão a luz a filhotes em intervalos de 2 ou 3 anos
(Clapham & Mayo, 1987), embora a ovulação pós-parto seja comum (Chittleborough,
1965). A gestação dura de 11 a 12 meses, sendo que aos seis meses de idade os
20
filhotes começam a desmamar, tornando-se inteiramente independentes ao final do
primeiro ano de vida (Clapham & Mayo, 1987).
Nas áreas de alimentação e reprodução, as jubartes apresentam organização
social caracterizada por grupos instáveis e pequenos (2 a 3 animais). Grandes
grupos podem, entretanto, se formar temporariamente durante comportamento
alimentar, ou relacionados com a disputa agressiva entre machos durante a
temporada reprodutiva (Clapham & Mead, 1999).
Os machos da espécie produzem um conjunto de sons complexos,
denominados “canto”, durante a temporada reprodutiva, provavelmente com a
função de atrair as fêmeas e/ou afastar outros machos (Tyack, 2000). O canto tem
uma estrutura previsível, com uma série de sons (unidades), repetida ao longo do
tempo nos padrões (frases), com cada frase repetida várias vezes para compor um
"tema" (Payne & McVay, 1971).
Um canto típico é então composto por 5-7 temas que geralmente são
repetidos em uma ordem seqüencial, durando tipicamente 8-15 minutos (embora
possa variar de 5-30 minutos) e depois repete-se sobre e ao longo de uma sessão,
que pode durar várias horas (Payne & McVay, 1971).
Uma característica marcante do canto é que ele gradualmente muda ou evolui
ao longo do tempo (Payne & Payne, 1985). A cada ano, diferentes sons se formam
para criar novas frases ou temas. Estas mudanças são lentamente incorporadas ao
canto, enquanto alguns padrões mais antigos são perdidos completamente. A
mudança no tema do canto parece ocorrer de forma coletiva ou comum a toda a
população (Winn & Winn, 1978; Matilla et al., 1987). Normalmente, após um período
21
de vários anos, o canto é praticamente irreconhecível a partir da versão original
(Payne et al., 1983). Em alguns casos, observa-se que a música é completamente
outra no espaço de apenas dois anos (Noad et al., 2000).
1.3.1) Ocorrência e Distribuição
As jubartes são animais migratórios, deslocando-se anualmente das áreas de
alimentação em altas latitudes, onde permanecem durante o outono e verão, para as
áreas de reprodução nos trópicos e sub-trópicos, onde permanecem durante o
inverno e primavera (Clapham & Mead, 1999). As áreas de reprodução da espécie
são tipicamente entre ilhas e/ou associadas a sistemas coralíneos(Whitehead, 1981;
Whitehead & Moore, 1982) (figura 2).
Uma população no Mar da Arábia é a única que aparentemente não migra em
busca de alta produtividade das águas frias para se alimentar, sendo observada
durante todo o ano em águas tropicais (Mikhalev, 1997).
Atualmente existem sete sub-populações (ou “stocks”) de baleias jubarte no
Hemisfério Sul (IWC, 1998), uma das quais migra anualmente para a costa do Brasil,
onde permanecem por aproximadamente cinco meses (de julho a novembro).
22
Figura 2: Ocorrência mundial e padrão migratório da baleia jubarte (Megaptera
novaeangliae).
Apesar de ocorrer ao longo de toda a costa brasileira desde o Estado do Rio
Grande do Sul até Fernando de Noronha (Towsend, 1935; Lodi, 1994), sua principal
área de reprodução e cria no Atlântico Sul Ocidental é o Banco dos Abrolhos, sul do
Estado da Bahia (ex. Andriolo et al., 2006; Wedekin et al., 2010). Entretanto, nos
últimos anos, as avistagens de jubartes no litoral norte do Estado da Bahia, incluindo
a região metropolitana de Salvador passaram a aumentar (figura 3), sugerindo a
recuperação desta população e o repovoamento de uma antiga área utilizada pela
espécie antes da época da caça, quando foram quase dizimadas (Rossi-Santos et
al., 2008).
23
Figura 3: A baleia jubarte (Megaptera novaeangliae) ocupando a região
metropolitana de Salvador, Estado da Bahia (Banco de Imagens- IBJ).
1.3.2) Ameaças e Status de Conservação da espécie
A queda brutal da população destas baleias devido à caça comercial levou a
Comissão Internacional da Baleia/ Internacional Whaling Commission (IWC), órgão
criado em 1946 para regulamentar o manejo dos grandes cetáceos no mundo, a
protegê-las internacionalmente da caça desde 1966. No Brasil, elas são protegidas
através do Decreto Lei n° 7643 de 18/12/87 e pela Portaria 117/96 que regulamenta
a avistagem de baleias em território brasileiro.
24
A baleia jubarte está presente em todas as listas oficiais de espécies
ameaçadas, entre as quais a Lista Oficial de Espécies da Fauna Brasileira
Ameaçadas de Extinção (Portaria IBAMA 1522 de 10/12/89) e no Apêndice I da
Convenção sobre o Comércio Internacional de Espécies Ameaçadas da Fauna
Selvagens (CITES). Segundo a IUCN (Reeves et al., 2003) e o Plano de Ação para
Mamíferos Aquáticos do Brasil (IBAMA, 2001), a espécie está classificada como
espécie vulnerável à extinção.
Atualmente as baleias estão protegidas da caça comercial, mas sofrem
ameaças por diversas atividades desenvolvidas pelo homem como o emalhamento
em redes de pesca, a poluição dos oceanos, atropelamento e colisões com
embarcações e atividades relacionadas à exploração de petróleo.
1.4) Expansão da população de baleias jubarte no Brasil
As avistagens de baleias jubarte (Megaptera novaeangliae) na costa do Brasil
voltaram a ocorrer em 1988, depois de um longo período de caça destes animais,
próximo ao estabelecimento do Parque Nacional Marinho de Abrolhos, sul do Estado
da Bahia quando iniciou-se um programa de pesquisa de longa duração para esta
espécie de baleia (IBAMA/NEMA, 1990). Desde então, o Banco de Abrolhos tem
sido considerado como a principal concentração reprodutiva para a espécie no
Oceano Atlântico Sul Ocidental (Engel, 1996; Martins et al., 2001; Martins, 2004;
Andriolo et al., 2006a,b; Morete et al, 2007; Wedekin et al., 2010) e a população que
frequenta esta área foi denominada como “Breeding Stock A” (BSA) ou “Estoque
Reprodutivo A” (IWC, 1998).
25
Atualmente, a população de baleias jubarte (Megaptera novaeangliae) do
“BSA” vem crescendo naturalmente, aliado ao resultado da paralização, na década
de 1960, da caça comercial da espécie. Recentes estudos sobre modelagens
numéricas (Zerbini et al, 2006, Ward et al., 2006) e avistagens ao longo da costa
brasileira (Andriolo et al., 2006a,b; Rossi-Santos et al., 2008; Wedekin et al, 2010)
contribuem com essa afirmação, demonstrando que a população vem reocupando
áreas que historicamente já utilizaram, como, por exemplo, a Baía de Todos os
Santos, onde eram abundantes no passado (Tavares, 1916; Tollenare, 1961).
1.5) Ecologia acústica, Comportamento e Seleção Sexual
A baleia jubarte é também conhecida com baleia-cantora por sua
característica reprodutiva de apresentar um comportamento acústico, exercido pelos
machos sexualmente maduros da população. Desde a década de 1970, muitos
estudos já descreveram a estrutura fisica dos sons (eg. Payne e Mc Vay, 1971;
Payne et al., 1983; Helweg et al., 1998; Maeda et al., 2000; Arraut & Vielliard, 2004)
e mesmo suas prováveis funções em nível de ecologia populacional (eg.
McSweeney et al., 1989; Dawbin & Eyre, 1991; Darling & Sousa-Lima, 2005; Eriksen
et al., 2005), entretanto, muitos outros aspectos da ecologia acústica que envolvem
as jubartes durante o canto ainda permanecem desconhecidos, como a sua relação
com o ambiente onde é produzido e com os outros sons, que não são naturais,
produzidos pelo homem no ambiente marinho, durante a temporada reprodutiva
anual.
26
Além disso, dentro da abordagem ecológica, abrem-se outras questões como,
por exemplo, a comparação entre a concentração reprodutiva com outras áreas ao
longo da costa e o contexto social-ecológico onde os machos cantam (quais os
grupos sociais onde ocorrem com mais frequência, quais as características
ambientais destes locais e suas prováveis relações com o comportamento de canto
da espécie), que serão abordadas no presente trabalho.
2. OBJETIVOS, HIPÓTESES E PREDIÇÕES
2.1) Objetivos
2.1.1) Objetivo Geral
Caracterizar a ecologia acústica do comportamento conhecido como “canto”,
da baleia jubarte, M. novaeangliae, na região nordeste do Brasil, fora de sua
concentração reprodutiva no Banco de Abrolhos, entre os anos de 2005 a 2009.
2.1.2) Objetivos específicos
a. Descrever e analisar a distribuição espacial dos machos cantores e o
contexto ecológico-social no qual este comportamento ocorre fora de sua
área de concentração reprodutiva (artigo 1);
27
b. Descrever a estrutura físico-acústica do canto da baleias jubarte fora de
sua área de concentração reprodutiva (artigo 2);
c. Descrever e analisar as fontes de ruídos antropogênicos provenientes da
indústria do petróleo no ambiente acústico utilizado pela baleia jubarte
(artigo 3)
d. Descrever e analisar as fontes de ruídos antropogênicos provenientes do
turismo de observação de baleias no ambiente acústico utilizado pela
baleia jubarte (artigo 4)
2.2) Hipóteses
Hipótese 1: Existe uma relação entre a complexidade da estrutura de grupo no
qual o macho cantor está inserido e o contexto ecológico no qual este
comportamento ocorre, sendo que fora da área de concentração reprodutiva a
estrutura do canto das baleias jubarte tende a se diferenciar.
Predição 1: os grupos com machos cantores apresentam estrutura social
diferenciada quando inserido em um cenário ecológico distinto da concentração
reprodutiva.
Hipótese 2: Existe uma relação entre a complexidade do canto e a
caracterização oceanográfica no qual este comportamento ocorre, sendo que
fora da área de concentração reprodutiva a estrutura do canto das baleias jubarte
tende a se diferenciar.
Predição 1: o canto da baleia jubarte é diferente quando inserido em um cenário
ecológico distinto da concentração reprodutiva.
28
Hipótese 3: Existe a sobreposição de nicho acústico, onde ruídos provocados
por atividades humanas causam interferências no comportamento das baleias
jubarte.
Predição 1: Os ruídos provocados por atividades humanas no ambiente marinho
estão dentro da faixa de frequência utilizada pela baleia jubarte no seu processo
de comunicação.
3. MATERIAL E MÉTODOS
3.1) Área de estudo
A área do presente estudo inclui o litoral do Estado da Bahia, desde Itacaré
(14° S, 38° W) a Aracajú (11° S, 37° W), no litoral do Estado de Sergipe (figura 4),
por ser uma região adjacente ao norte da concentração reprodutiva da espécie com
facilidades logísticas nos portos de Itacaré (cerca de 300 km ao sul de Salvador), da
própria capital, Salvador, de Praia do Forte, no município de Mata de São João, a 55
km ao norte.
Este trecho de costa é caracterizado por praias de areia de quartzo fina a
grosseira. As barras parcialmente submersas de rocha ocorrem alternadamente no
sublitoral e os recifes costeiros em franja, dominados por algas calcárias e
briozoários, com poucos corais celenterados encontrados fora, aproximadamente a
12 km da praia. A praia supralitoral é caracterizada por um cordão de dunas
29
crescendo em altura na direção norte e por praias de baixo declive e de maior
extensão ao sul.
Dentro da área de estudo também ocorrem grandes baías e estuários
costeiros, de importância para a navegação, como a Baía de Todos os Santos, no
Estado da Bahia e os estuários do Rio Vaza-Barris e do Rio Sergipe, no estado de
mesmo nome.
A principal característica desta região, em geral, é a presença de uma
plataforma continental estreita, cuja extensão corresponde a aproximadamente 15
km (figura 4). A média de profundidade ao longo da plataforma é de 20-70 metros e
a amplitude de maré varia entre 0.1 a 2.6m (Carta náutica – Diretoria de Hidrologia e
Navegação DHN- da Marinha do Brasil.).
Além da pressão antropogênica, resultante principalmente da presença de
grandes portos, como o de Salvador e de Aracajú, e do tráfego de navios resultante,
de atividades de exploração de petróleo e gás, com a presença de plataformas
costeiras, a região abriga diversas colônias de pesca artesanal, intensa atividade
turística e ocupação espacial desordenada, além do maior Pólo Petroquímico do
Hemisfério Sul, no município de Camaçari, Estado da Bahia.
30
Figura 4: Área de estudo, desde Itacaré (BA) 14° S, 38° a Aracajú 11° S, 37° W (SE),
durante a temporada reprodutiva de baleia-jubarte (Megapteranovaeangliae), entre
julho e outubro.
31
3.2) Coleta de dados
3.2.1) Cruzeiros de pesquisa
Para os cruzeiros de pesquisa utilizou-se uma embarcação de madeira, do tipo
saveiro (caracterizada por possuir somente um mastro central) de 15 metros e motor
díesel de 250 hp (figura 5).
Figura 5: Embarcação (Saveiro) utilizada durante os cruzeiros de pesquisa durante a
temporada reprodutiva de baleia-jubarte (Megaptera novaeangliae), entre julho e
outubro, com referência aos observadores na proa.
32
A equipe de campo, composta por três observadores, permanece na proa da
embarcação para cobrir um ângulo de 180° de campo visual. As observações são
feitas a olho nu, eventualmente auxiliadas por binóculos, buscando-se identificar
sinais de baleias (borrifo, dorsos, saltos e outros comportamentos) na superfície da
água próxima ao horizonte.
Utilizamos uma ficha diária de amostragem, com os dados gerais da
expedição, como duração, participantes, número de baleias avistadas, bem como os
dados ambientais (velocidade e direção do vento, visibilidade, escala Beaufort do
mar, profundidade, entre outros) que poderiam influenciar nas condições de
avistabilidade. Para as tomadas de horário da maré correlacionada aos grupos de
baleias avistados, foi utilizada a Tábua de Marés fornecida pela Diretoria de
Hidrologia e Navegação (DHN) da Marinha do Brasil.
Os grupos de baleias-jubarte avistados foram registrados em outra ficha de
campo, onde constam informações como coordenadas geográficas, tamanho e
composição do grupo, horário da avistagem, comportamentos observados antes e
durante a aproximação do barco, além de outras informações.
A aproximação aos grupos foi realizada de maneira gradual, com o motor em
marcha média e constante, procurando chegar junto aos animais por um dos bordos.
A embarcação de pesquisa permaneceu, em média, 30 minutos com cada grupo de
baleias para a coleta dos dados de comportamento e bioacústica, entretanto,
quando as condições climáticas são favoráveis, durante um comportamento de
canto observado, este período pode ser extendido até cerca de 60 minutos.
33
4.2.5) Bioacústica
Ao longo dos anos o equipamento de gravação variou em função do
crescente avanço tecnológico que derivou nos sistemas de aquisição de áudio e
vídeo digital. Entre os anos 2005 a 2007, os cantos de baleia foram gravados
utilizando um sistema analógico (gravador cassete Sony TCD-5M – resposta de
frequência de 24 kHz) ou, eventualmente um sistema analógico-digital (vídeocamêra Sony VX-1000) sempre plugados ao mesmo hidrofone (HTI SSQ-94). A
partir de 2008 passou-se a utilizar um sistema digital (mini-gravador digital M-Audio
MicroTrack II), resultando em um ganho da resposta de frequência para 48 kHz.
Posteriormente, as gravações obtidas nos sistemas analógico e analógicodigital foram digitalizadas, exportanto os dados brutos para o programa onde seriam
feitas as análises, o RAVEN 1.3 (Universidade Cornell/EUA). Os dados do sistema
digital já eram obtidos em formato sem compressão (WAV), selecionado no
gravador, e salvos em um banco de dados de áudio.
Depois de digitalizados os sons foram analisados, no programa RAVEN,
quanto aos parâmetros de frequência física tais como: frequência inicial, frequência
final, frequência média, frequência máxima, frequência mínima, amplitude, duração,
energia. Estes dados foram medidos, utilizando o cursor para a seleção do sinal
acústico, através de espectrogramas digitalizados (gráficos com eixos em freqüência
(Hz) e tempo (seg)). Uma vez medidos, os dados foram exportados para o programa
Microsoft Excel para compor um banco de dados para análises posteriores.
34
Para os cantos das baleias jubarte, também analisamos a complexidade de
partes da estrutura dos cantos, agrupadas em unidades sonoras ou notas, frases e
temas, seguindo a classificação de trabalhos anteriores (revisado em Tyack, 2000,
Souza-Lima, 2007 e Parsons, 2008)
4.2.6) Sistema de Informações Geográficas
As rotas dos cruzeiros de pesquisa e avistagens dos grupos de baleias
jubarte
observados,
armazenadas
em
bem
um
como
as
tomadas
ambientais
Sistema
de
Informações
coletadas, foram
Geográficas
para
serem
posteriormente plotadas em mapas de cartas náuticas pré-digitalizadas, utilizando o
programa Arcview 3.2 (ESRI, Headland, Califórnia). Estes mapas, então, incluem a
batimetria da área de estudo e a distribuição das avistagens de baleias jubarte.
35
4) RESULTADOS
36
Artigo 1 – Ecologia comportamental do canto em baleias jubarte (Megaptera
novaeangliae), na região nordeste do Brasil.
Marcos R. Rossi-Santos
1,2
, Elitieri Santos-Neto1, Clarêncio G. Baracho-Neto1,
Sérgio R. Cipolotti1, Enrico G. Marcovaldi1, Flávio J. L. Silva2,3
1-
Instituto Baleia Jubarte
2-
3-
Universidade Estadual do Rio Grande do Norte\ Centro Golfinho Rotador
BEHAVIORAL ECOLOGY (A1 – Fator Impacto 3,083)
A ser submetido
37
RESUMO
Nós estudamos a ecologia comportamental de machos cantores de baleias jubarte
(Megaptera novaeangliae) entre Itacaré/ Bahia (14°S, 38°W) a Aracaju/ Sergipe
(11°S, 37°W), dentro da sua área de reprodução no Brasil, entre os anos de 2005 e
2009. Foram analisados aspectos sociais e ecológicos tais como composição de
grupo, distribuição espacial, influência de profundidade, marés e fases da lua.
Saídas utilizando embarcação foram realizadas para avistagem e aproximação das
baleias, para a coleta de dados como localização geográfica, comportamento e
gravações bioacústicas. Um total de 912 horas de esforço amostral foi obtido em
123 dias de saídas, avistando 370 grupos de baleias. Em 36 dias (41 horas de
observação direta), 29% dos grupos (n=44; 82 indivíduos) foram identificados
contendo ao menos um macho cantor, confirmado por gravações subaquáticas.
Grupos com machos cantores foram avistados ao longo de toda a área de estudo,
na maioria das vezes como indivíduos solitários (n=21 grupos, 48%), seguido por
grupos contendo dois (n=8; 18%), três (n=3, 7%), quatro (n=2, 4,5%) indivíduos
adultos e grupos contendo pares de fêmea com filhote, acompanhados por um
macho cantor (n=4, 9%) ou fêmeas com filhotes acompanhadas de dois machos
cantores (n=1, 2%). Grupos com machos cantores foram avistados em uma variação
de profundidade entre 16 e 173 metros (média = 54,6/ desv.pad.= 34,2). A
plataforma continental estreita associada com a distribuição costeira da baleia
jubarte na região de estudo pode influenciar na formação das diferentes estruturas
de grupo contendo machos cantores. Trazemos, assim, uma visão mais ampla dos
aspectos ecológicos do comportamento de canto nesta espécie, em uma nova
região de estudo, alem de sua concentração reprodutiva do Banco de Abrolhos.
38
Palavras-chave: Baleias jubarte, machos cantores, ecologia comportamental,
distribuição
39
BEHAVIORAL ECOLOGY OF THE SONG IN HUMPBACK WHALES
(MEGAPTERA NOVAEANGLIAE), FROM THE SOUTHWESTERN ATLANTIC
OCEAN
ABSTRACT
We studied the behavioral ecology involving singer humpback whales (Megaptera
novaeangliae) from Itacaré/ Bahia state (14°S, 38°W) to Aracaju/ Sergipe state
(11°S, 37°W), in the Brazilian breeding ground, between 2005 and 2009 (July to
October). Behavioral and ecological aspects such as group composition, spatial
distribution, depth, tides and moon were analyzed, through boat surveys. We sighted
370 whale groups in 123 days, during a total of 912 hours of sampling effort. In 36
days, 29% of the groups (n=44; 82 individuals) were identified containing at least one
singer male. Such groups were sighted along all the study area, mostly like alone
individuals (n=21 groups, 48%), followed by groups with two (n=8; 18%), three (n=3,
7%), four (n=2, 4,5%) individuals and also groups with female-calf pairs with one
escort male (n=4, 9%) or female-calf pairs plus two males (n=1, 2%). Groups with
singer males were sighted in a depth range of 16 and 173 meters (mean = 54,6 ±
34,2 SD). The narrow continental shelf associated with the coastal distribution of the
whales in the study area may influence in the group compositions containing singer
males. So on, this work bring for the first time an ecological perspective of this
recognized important singing behavior in this species, and also show the expansion
of the acoustic activity, during the Brazilian breeding season, going far beyond the
core area of Abrolhos Bank.
Keywords: Humpback whales, singer males, behavioral ecology, distribution
40
1) INTRODUCTION
1.1) Ecology and animal communication
The most of the acoustic signals are modified when the pass by the
environment since the sender to the receiver, which transforms and depredates this
signal, but even so, results in information to the receiver, as some bird species who
can estimate the distance from a sender individual through the signal degradation
(McGregor & Krebs, 1984; Naguib, 1998).
Furthermore, the environment may shape evolutionary changes which may
result in specific vocal adaptations in close related vertebrate species, and even
inside the same species, leading to differences in sound repertoire which reflect their
ecological habits (Podos, 2001; Podos et al., 2004).
Dolphins and bats track their environment listening to the echoes which
themselves produces, a process called echolocation (eg: Tyack, 2000). Thus, in the
field of cetacean communication there are some basic questions that still could be
answered, such as what are the features that make this signal unique. Those
questions are crucial to understand whether these signals are elaborated and have
their specific usage. Part of this subject is included in the behavioral ecology context
of the present work.
We studied the behavioral ecology of the singer male humpback whale
(Megaptera novaeangliae) in their breeding ground at northeastern Brazilian coast
and discussed diverse parameters, such as singers’ group structure, behavior,
distribution and their possible relations with oceanographic features as depth, tide
and moon phases influences on the humpback whale song inside the breeding
season.
41
1.2) Species Characterization
The humpback whale Megaptera novaeangliae (Cetacea, Balaenopteridae), is
a cosmopolitan species distributed along all the oceans worldwide (Clapham &
Mead, 1999), moving every year from high latitude feeding areas, staying during the
autumn and summer, to the breeding areas in the tropics, staying during the spring
and summer (Clapham & Mead, 1999). These breeding areas are typically between
islands and/or associated with coral systems (Whitehead, 1981; Whitehead & Moore,
1982).
In the feeding and breeding area, the humpback whale present a social
organization characterized by unstable and small groups (2 to 3 animals). However,
larger groups can be found during the feeding behavior or related to the aggressive
competition between males during the breeding season (Clapham, 1996).
1.2.1) Ocurrence and Distribution
Nowadays, there are seven humpback whale sub-populations (or stocks) in
the southern hemisphere (IWC, 1998), one of those, named by IWC “Breeding Stock
A/ BSA” to migrate to the Brazilian coast, where they breed from July to November.
Despite their occurrence along a large range in Brazil, from Rio Grande do Sul
state, southern Brazil, to the Fernando de Noronha Archipelago, northeastern Brazil,
(Towsend, 1935; Lodi, 1994), its core breeding area is the Abrolhos Bank, Bahia
state (Wedekin et al., 2010). However, the increase of humpback whale sightings
northwards from the Abrolhos Bank, including the Bahia state capital, Salvador and
the north coast of the state, suggest the population recovery in this historical area,
occupied by the whales prior the whaling period (Tavares, 1916; Tollenare, 1961;
Rossi-Santos et al., 2008).
42
1.3) Ecology and Acoustic Behavior
The humpback whale is also known as singer whale because its unique
characteristic of to exhibit a singing behavior, performed only by males, during their
breeding season. Since the 1970ths, many studies described the physic structure of
the songs (eg. Payne e Mc Vay, 1971; Helweg et al., 1998; Maeda et al., 2000;
Arraut & Vielliard, 2004) and even their probable functions at the population ecology
level, such as female attraction, male-male competition and cultural exchange (eg.
McSweeney et al., 1989; Dawbin & Eyre, 1991; Darling & Sousa-Lima, 2005; Eriksen
et al., 2005), however many other aspects of the acoustic ecology of the species
during the singing behavior is still unknown, such as the socio-ecological context in
which the males sing, bringing spatial information (eg. where do they sing?, what
depth?) and variations of this context inside the breeding season.
2) MATERIAL AND METHODS
2.1) Study area
For this work we encompassed a stretch of coast between the northeast states
of Bahia and Sergipe, naming it North Coast, going from Itacaré (14° S, 38° W) to
Aracaju (11° S, 37° W), with main departing location at Praia do Forte, (13° S, 38° W)
placed in the center of this area (figure 1). The main oceanographic characteristic for
this area is a narrow continental shelf, with approximately 15 km of extension, with
average depth of 40 meters and the tide amplitude varying between 0.1 to 2.6m
(DHN, 1995; Ekau & Knoppers, 1999).
43
This region is characterized by two remarkable environments, being the
presence of large bays and estuaries from Itacaré to Salvador, capital of Bahia state,
and by long sand beaches, with large dune formation fringing the coast line, between
Praia do Forte and Aracaju (Hatge & Andrade, 2009).
Figure 1 – Study area, named North coast, located between Itacaré and Aracaju,
Northeastern Brazil. For reference, southwards it is located the Abrolhos Bank, core
area of humpback whale (Megaptera novaeangliae) distribution in Brazil. The line
represents the 200 meters isobath, demarking the Brazilian continental shelf.
2.2) Data collection and behavioral observations
44
We carried out boat based surveys searching for whales in a determined
route, approaching animals when sighted to collect data such as number of
individuals, composition of the groups, behavior observed before and after approach,
dive patterns, time of beginning and end of the sightings and bioacoustic recordings.
Behavioral observations followed a combined Focal Group and Ad libitum
methods (see Mann et al., 2000) registering a sequence of a certain behavior during
the observation time of each group, broadly employed in the cetacean studies.
Behavior and group structure nomenclature and definitions followed extensive
previous works worldwide (Clapham, 1996, Clapham & Mead, 1999, Clapham 2000)
and locally (Engel, 1996, Lunardi et al., 2010).
2.3) Sex Determination of Individuals
Genetic studies of humpback whales worldwide have shown that singing and
escorting are behavioral roles performed only by males and that a whale closely
associated with a calf is its mother, an adult female (eg. Palsboll et al, 1997; Darling
& Berube, 2001).
An ‘escort’ is defined as a whale that is associating with another adult whale
known to be female or with a mother-calf pair. When two males are engaged in
dispute behavior in the presence of a female, both are considered escorts (Herman &
Tavolga 1980).
In this study, we assume the sex of observed animals in these behavioral roles
following these convictions. The term ‘calf’ refers to calves of that year. It was not
possible to visually differentiate between immature or sub-adult and adult whales,
therefore the term ‘whale’ refers to all non-calf whales.
45
2.4) Geographic Information System (GIS)
For the record of the geographic position of sighted animals, with reference to
the boat position, we utilized a GPS Map 76 and a GPS Map 60c (Garmin), in the
way-point function. For posterior analysis and studies of the humpback whale
distribution along the time in the study area, we created a GIS environment modeling,
including important features such as the Brazilian coast line, bathymetry and the
plotted geographic coordinates of each sighting, in a digital nautical charter, using the
software Arc View GIS (version 3.1).
2.5) Dive Time
Dive time were systematically registered during 2008 and 2009 breeding
seasons, utilizing a digital chronometer, in order to measure and compare breathing
behavior of small groups (less than 4 individuals), to date, Alone Males (solitary),
Couples, Female with calf pairs, Female with Calf plus one escort male.
We organized dive time data into the following definitions: (D.O.- minutes) =
Direct Observation (the time spent observing humpback whale groups); (D.P. range –
seconds) = Dive time – the time whales spent underwater; (Mean range D.P > 100
sec) = mean number of Dive time larger than 100 seconds; (# of measur.) = number
of dive measurements; (# measure. > 100 sec) = number of dive measurements
larger than 100 seconds; (Fe-Ca pairs) = female and calf pairs; (FeCa-E1) = female
and calf pairs plus one escort male.
46
2.6) Tide and moon analysis
We divided tidal states into 8 different classes, looking for a similar time
division and fine scale during the tidal regimen. Significant differences in tide and
moon phases categories were analyzed utilizing the Chi-Square test (5%).
3) RESULTS
Between 2005 and 2009, we performed a total of 912 hours of sampling effort,
distributed in 123 days, sighting 370 groups during our systematic field work (table
1). About 29% of the groups (n=44; 82 individuals), in 36 days (41 hours of direct
observations), were identified containing at least one singer male in the group, with
singing behavior confirmed by underwater recording.
47
Table 1: Number of boat surveys, sampling effort (hours), covered distance (nautical
miles), number of sighted whales, number of groups and direct observation (hours) of
humpback whales in the northeastern Brazilian coast, between 2005 and 2009.
Seasons
Survey n Sampling Direct
Covered
effort
observation distance
(hs)
(hs)
(Nm)
Whales
Groups
observed
2005
17
118,5
34,7
699
104
53
2006
37
266,6
109,4
1667
317
151
2007
7
51,7
18,8
339
58
26
2008
32
235,7
96,5
1463
291
21
2009
30
240
77
981
275
119
Total
123
912,3
336,4
5179
1045
370
3.1) Distribution
Humpback whale groups with singer males were sighted along the study area,
from the southern sighting in Itacaré/Bahia state (14° S, 38° W) to the northern
sighting in Aracaju/Sergipe state (11° S, 37° W) (Figure 2), despite a small gap noted
North of Praia do Forte towards Aracaju.
48
Figure 2: Distribution of humpback whale (Megaptera novaeangliae) groups with
singer males, in the study area, Brazilian breeding ground, between 2005 and 2009
3.2) Group structure
Regarding group structure, singer whales were sighted mostly alone (n=21
groups, 48%), followed by groups containing two (n=8, 18%), three (n=3, 7%), four
(n=2, 4,5%) adult individuals and groups with mother-calf pairs plus the singer male
(n=4, 9%) or mother-calf pairs plus two more males (n=1, 2%) (Figure 3).
49
Figure 3: Frequency of different group structure of humpback whales with singer
males, between 2005 and 2009, in the Northeastern Brazilian coast. 1 Ad = 1 adult
individual, 2 Ad = 2 adult individuals, 3 Ad = 3 adult individuals, 4 Ad = 4 adult
individuals, FefiEp = female and calf pair plus one escort male, FefiEpE = female and
calf pair plus two escort males.
During 2005 and 2006, singer males were observed in all mentioned
categories, excepting three or four adults. In 2008 and 2009 these groups occurred.
That may indicate a variation in singer male group composition along the time, with
more singers in a certain area, maximizing the singing behavior with diverse potential
groups for mating.
50
3.3) Behavioral observations
Alone individuals (n= 21) are generally observed floating on the surface, with
slow movements and performing resting behavioral events related to diving, such as
tail-up and dorsum arching, with minor frequency of snaking (tail and peduncle
shaking before dive) and breaching, both noted only for 3 individuals. Couples
exhibited more active behaviors than alone animals, being observed breaching (3
individuals), tail slapping (2 individuals), diving and resting (2 individuals).
Competitive groups including singer males were registered on four occasions,
exhibiting active behaviors. In Oct, 1, 2005, during 40 minutes of direct observation
we sighted 4 animals performing behaviors of consecutive tail-up for short dives,
dorsum arching, belly exposition, breaching and bubble exhalation on the sea
surface.
In Jul, 31, 2008, we sighted 3 animals during 41 minutes of direct observation
showing head slapping, dorsum arching, rolling, breaching (n=13), tail-up for diving
(n=12) and tail slapping (n=2). In this sighting, we observed one whale-watching
zodiac boat (about 9m long with outboard engine of 250 Hp) near to the humpback
group.
In Aug, 7, 2008, for 85 minutes we observed 4 animals with behavior such as
breaching (n=4) and tail-up during short dives (n=37) and in Aug, 30, 2008, during 70
minutes, we sighted 4 animals performing head exposition (n=2), tail-up during dives
(n=11) and pectoral fin slapping (n=2).
51
3.4) Dive time
We obtained 956 measurements for 52 humpback whale observed groups
(Table 2). The time at the sea surface, indicated a general pattern of few (2-5) very
short breathings (less than 30 seconds) and one longer dive (> 30 to 780 seconds).
Four groups of alone males were singing while measured, confirmed by
underwater recordings. In Aug, 10, 2008, the singer male was at 51 meters deep,
showing long dive patterns and performed fluke exhibition in travelling behavior.
Another sighting, in Aug, 30, 2008, we observed a sequence of long dives (7
measurements > 200 seconds) of the male at 40 m deep. Again, we observed 5 fluke
exhibitions in displacement behavior. In Aug, 28, we observed a singer male in active
behavior with breaching and singing while showed a dive pattern of 4 dives less than
60 sec and then one long (>100sec). Depth was not registered. In the last
observation, during the research cruise of Jul, 14, 2009, a singer male was in rest
behavior at 36 meters deep, and the song caption was intense, suggesting the
proximity to our boat. This animal presented long dives, being the maximum value
registered for the total sample of 780 seconds (13 minutes), and performed the same
fluke exhibition than the other observed males.
The smallest dive range was registered for FeCa pairs (maximum of 132 sec 2,2 min). Couples were the second category in long dive patterns (2-660 sec) and the
first in number of measurements larger than 100 seconds (n=88) (table 2).
52
Table 2 – Summary of humpback whale dive time from the study area in the Brazilian
coast between 2008 and 2009 *.
Group
#
Depth
(D.O.)
(D.P)
Mean range #
Structure
Groups
range
(min)
range
D.P
(m)
(sec)
100sec
.
> 100sec
21
8,7-126 977
2-780
134,3-780
278
59
Couples
18
49-126
810
2-660
125,6-540
389
88
FeCa
3
-
120
5-132
116-166,3
59
7
FeCa-E1
10
66-155
500
2-349
122,3-479,5
230
31
Total
52
8,7-155 2407
956
185
Alone
of #
> measur
measur.
Males
pairs
2-780
* Definitions: (D.O.- minutes) = Direct Observation (the time spent observing humpback whale groups);
(D.P. range – seconds) = Dive Pattern – the time whales spent underwater; (Mean range D.P > 100
sec) = mean number of Dive Patterns larger than 100 seconds; (# of measur.) = number of dive
measurements; (# measure. > 100sec) = number of dive measurements larger than 100 seconds; (FeCa pairs) = female and calf pairs; (FeCa-E1) = female and calf pairs plus one escort male.
3.5) Environmental features
3.5.1) Depth
Sightings of humpback groups with singer males occurred between 16 and
173 meters (mean = 54,6 ; ± 34,2 SD). We grouped depth values into different
classes (Figure 4). For depth range 1 (0 to 20m), we found only one competitive
group of 4 animals at a 16 m location. For depth range 2 (21 to 30m) we sighted 3
53
whale groups, for depth range 3 (31 to 40m) we observed 5 groups, for depth range
4 (41 to 50m) we sighted 7 whale groups, while for depth range 5 (51 to 70m) we
registered 3 groups. For depth range 6 (71 to 100m) we observed 3 whale groups
and for depth range 7 (> 100m) we sighted 2 groups, being one with a alone
individual at 126m and a competitive group of 4 animals at 173 meters deep.
Figure 4: Frequency (number of sightings) of humpback whale groups with singer
males in different depth range, between 2005 and 2009, in the North Coast, Brazilian
breeding ground.
54
3.5.2) Tide
Even dividing the tidal states into time similar categories, and apparently
diverse in the frequency distribution (Figure 5), the Chi-Square test showed no
statistical differences between singer male occurrence in the tidal classes (ChiSquare 5% =11,55556; df = 7; p= 0,12).
Figure 5: Frequency of humpback whale groups with singer males in different tidal
classes, between 2005 and 2009, in the North Coast, Brazilian breeding ground. (HgHigh, Hg/Eb - High/Ebbing, Half Eb- Half Ebbing, Eb/Lw- Ebbing/Low, Lw- Low,
Lw/Rs - Low/Rising, Half Rs- Half Rising, Rs/Hg - Rising/High).
55
3.5.3) Moon Phases
Singer males were sighted in all moon phases, but despite small differences
(figure 6) there was no statistical differences between the four classes (Chi-Square
5% = 2,0; df = 3 p= 0,57), indicating no evident influences of this environmental
feature in the singing behavior along the study area.
Figure 6: Frequency of humpback whale (Megaptera novaeangliae) groups with
singer males in different moon phases, between 2005 and 2009, in the North Coast,
Brazilian breeding ground.
56
4) DISCUSSION
During five years we found humpback whale groups containing singer males in
all the extension of our study area, being about 520 km of coast. This confirm the
large distribution of the humpbacks in the Northeastern region of Brazil, going farther
than the core area of Abrolhos Bank, as previously commented (Rossi-Santos et al.,
2008; Wedekin et al., 2010).
The lack of sightings in the stretch of coast between north of Praia do Forte to
south of Aracaju may be probably due to the sampling route, always passing there
during the night, because navigating conditions in those cruises, which depart from
Praia do Forte to reach Aracaju during the early morning of the next day. However,
the sightings north and southwards of this place attest the presence of the
humpbacks, and because its high mobility we assume they do occur along all that
part of coast.
Despite the singer animals being typically described as alone males (eg.
Payne & Mc Vay, 1971; Clapham, 1996; Darling & Berube, 2001), singing behavior
may occur in other group composition, as the occasional escort males (eg. Baker and
Herman, 1984; Frankel et al., 1995; Darling & Berube, 2001), whose may sing while
escorting females with or without calves. Darling & Berube (2001) also reported
about 14 occasions where another male approached singer males.
In the present work we found singer males mostly as alone individuals.
However singer males also occurred in groups varying from two to four individuals,
besides males accompanying females and calves. In one occasion two singers in the
same group were confirmed by bioacoustic recordings. This show a large behavioral
57
flexibility from humpback whales in increase the chances to find a mate partner
during the breeding season.
During many occasions we noted singer males typically smaller (referenced to
the boat as 8-9m long animals), suggesting that young animals are using the study
area as a way to search for new territories even less competitive than the core area
of Abrolhos Bank, where traditionally large and old singer males utilize during the
breeding season. We suggest the employ of the photogrammetry method (eg. Spitz
et al., 2002) to access this hypothesis in next studies concerning body size
estimation.
Humpback whale distribution in the study area may be related to ecological
features such as oceanographic parameters of depth, continental shelf extension,
while tide and moon seems do not influence singer male distribution.
Meanwhile, behavioral factors such as female distribution are theorized in the
literature and may be determinant in the singer male occurrence during the breeding
season. As humpback whale apparently do not feed in the breeding areas, females
tend to move intensely, avoiding to meet with other female while, simultaneously,
looking for increase their mate chances. Pos-partum ovulation, common in this
species, also benefits this high mobile female behavior and these factors together
result in an irregular female distribution (Clapham, 1996; Clapham & Mead, 1999).
The fact of the study area be located in a continental region, different from the
most of the described breeding areas, such as the Hawaiian Archipelago, (Au, et al.,
2006), South Pacific Ocean islands (Helweg et al., 1998), Panama Gulf (Olviedo et
al., 2008), may result on differences in their acoustic signals.
As the oceanic dynamic between continental areas and islands is different, the
influence of environmental parameters in continental areas may be different and
58
provide the development of different acoustic signals that may be more efficient in a
certain environment.
Further studies should develop efforts in ecological comparisons between
coastal and oceanic areas which may be affecting male distribution and singing
behavior in a fine scale.
We registered an increase in behavioral activity according to the increase in
the group size and composition, with larger groups presenting a broader behavioral
repertoire, in accordance with literature descriptions to other breeding areas (eg.
Clapham, 1996) and to the same breeding stock A, in the Abrolhos Bank (Morete et
al., 2007), which may contribute with the complex group structure during the breeding
season and may reflex in complexity of communicative skills (Freeberg et al., 2012).
The largest dive, of 13 minutes, was found for a singer male, very similar to
the results from a recent study in the Abrolhos Bank, which analyzed the same 4
group categories and registered the largest time of 13,13 minutes, coming from a
singer male (Benzamat et al., 2010), indicating a probable general pattern for areas
as distant as 500 km, in the same breeding stock.
Humpback whales sometimes show avoidance to boat approaching increasing
their dive patterns (Hoyt, 2001). During many years researchers from both Abrolhos
Bank and North Coast of Bahia state, noted that the whales in North Coast are more
difficult to approach than in the core area of Abrolhos. The present data on the mean
percentage of time spend by diving whales was 85% in relation to the direct
observation time. This value was more than double than previous studies from the
Abrolhos Bank, 42 % in Peres (2006) and 30,1% in Benzamat et al. (2010).
The north coast do not present genetic differences from the Abrolhos Bank
(Cypriano-Souza et al., 2010) but is being considered as an area of more dynamic
59
movements of whales (Wedekin et al., 2010; Baracho-Neto et al., 2012), and this
could lead, in consequence, in more travelling behavior and even boat avoidance
through less time in the surface.
The narrow continental shelf in the North Coast also can play a role in the dive
patterns, making individuals travel more in a north-south direction to keep in shallow
waters characteristic of their distribution, while in the Abrolhos Bank, the core area in
the Brazilian coast, more than double of density of whales (Andriolo et al., 2006a;
2006b; Wedekin et al., 2010).
As the whole breathing behavior of humpbacks do include those very short
intervals, we decided to keep them all in the analyzes, different from Benzamat et al.
(2010) which only included intervals larger than 60 seconds, even considering that
smaller intervals prevailed, being 68% of their sampling.
Concluding, singer males are longer divers than other analyzed group
structure, presenting similar values, of 13 minutes, to the Abrolhos Bank, distant
about 500 Km from our study area in the North Coast of Bahia state. Humpback
whales in North Coast spent about 85% of the direct observation in underwater
activities, more than the double of time found for the Abrolhos Bank, which could
indicate longer underwater occurrence due by distinct habitat use, once the north
coast is seen as an area of greater movement than the Abrolhos Bank. However,
even with distinct environmental features as the deeper areas of the North Coast, it
does not seem to present a strong influence on dive patterns of the humpback whale
in the Brazilian Breeding ground.
60
4.1) Mating System
Polygyny is a mating system in which one male mates with several females
during a breeding season. “Lek” is defined as a traditional display site where males
gather to defend small territories that lack resources useful to females, which
nevertheless visit the site to mate. Therefore, lek polygyny occurs when a
polygynous male use displays to attract several females to them at small display sites
(Alcock, 1993).
It is well studied for other mammals such those closely related to cetaceans,
the ungulates, beyond 35 bird species, frogs and even insects (see Krebs & Davies,
1993, Alcock, 1993). Clapham (1996) suggested the term ‘floating lek’ to the
humpback whale mating system, emphasizing the high mobility of the singer males,
in contrast with the traditional lek which present a fixed territoriality.
In the present study, we present some spatial (presence of multiple group
composition) and behavioral (diverse repertoire while singing) features found that
support the “lek polygyny” as the mating system for the humpback whale. The singer
male distribution along the study area indicate that a broad area in the breeding
ground is being utilized for displaying, refusing lek influenced by “hotspot”, in which
males compete for the most attractive site to display, while fitting better to lek by
“hotshot” males, which may choose any place to sing and then attract females to
mate and more “satellite” males, coming to maximize their mate chances by staying
as close as the hotshot male (Krebs & Davies, 1993; Alcock, 1993).
Connor et al. (2000) discussing on male reproductive strategies in cetaceans,
state that humpback whale seems to follow the restrictive definition of lekking: (1) no
male parental care, (2) an arena where males gather and females come to mate, (3)
resource-free display sites, and (4) opportunities for females to exercise mate choice
61
(Clapham, 1996). However, instead to emphasize only the male-male dominance
and territoriality, Connor et al. (2000) also include a broader view in which lekking
behavior is found in association with other male mating strategies, as the example of
male-male combat in competitive alternatively to displaying. Tyack (2000) suggest
that humpback whale song plays a role in both male-male competitions and female
choice, showing attributes associated with both intra and intersexual selection.
To determine a precise mating system for the humpbacks is a complex task,
once we still do not know many basic issues as the ideal breeding area size for any
population. Thinking broader, the Brazilian population increase (Ward et al., 2006;
Zerbini et al., 2006, Andriolo et al., 2006b) could lead to dispersion of young females,
whose would attract different males, then forming the floating lek, either by hotspot or
hotshot, and colonizing favorable adjacent areas.
At the same time that in the core area, the Abrolhos Bank, male arenas would
be much more competitive, then causing younger males to move northwards and
search for new areas to aggregate, through singing, and then maximize mate.
Furthermore, reflecting on the multi faced hypothesis of a mating system,
would be important to analyze that the humpback whale population using the
Brazilian breeding ground have a sex-ratio of 1.2:1, similar to the expected rate of
1:1, determined genetically by Cypriano-Souza et al. (2010). Baracho-Neto et al.
(2012) also support the site fidelity similarity between genders through a long term
photoidentification study in Praia o Forte, same than the present study.
All these pieces together may help to create a scenario suggesting a mating
system more complex than previously reported, with more fluidity of individuals,
females and males, along a broad area in the Brazilian coast and ideal breeding sites
62
possibly influenced by some environmental features as the extent of the continental
shelf, consequently depth gradient.
Furthermore, the diversity in singer male occurrence and behavior between
different group compositions could be related to the complex communicative system
in humpback whales, as recently described by Freeberg et al. (2012). Future studies
should include environmental and whale occurrence data in a broader temporal scale
to test specifically each one of these factors and their influence in the acoustic
ecology and behavior of humpback whales.
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70
Artigo 2 – Estrutura acústica e variação temporal do comportamento de canto
em baleias jubarte (Megaptera novaeangliae), na área de reprodução da costa
do Brasil.
Marcos R. Rossi-Santos
1,2
, Leonardo L. Wedekin1, Elitieri Santos-Neto1,
Clarêncio G. Baracho-Neto1, Sérgio R. Cipolotti1, Enrico G. Marcovaldi1, Flávio
J. L. Silva2,3
1-
2-
3-
Universidade Estadual do Rio Grande do Norte
ANIMAL BEHAVIOR (A1 – Fator Impacto 2,926)
A ser submetido
71
RESUMO
Em áreas tropicais de acasalamento, o macho da baleia jubarte produz sons
estereotipados e repetidos que combinados formam o canto, um dos mais
complexos comportamentos do reino animal. Há muito tempo é desenvolvido um
esforço de pesquisa sobre qual é a função do som no comportamento reprodutivo da
espécie, comumente atribuído a servir como um comportamento acústico para a
seleção intra e intersexual. Apesar de décadas de estudos sobre o canto da baleia
jubarte no mundo, algumas características básicas como a variação de parâmetros
de tempo e frequência em uma escala ampla, incluindo as unidades sonoras ou
notas que servem como base para serem agrupadas em frase e estas em temas,
formando o canto, são pouco discutidas. Este trabalho tem como objetivo descrever
os cantos da baleia jubarte em uma ampla escala na área de reprodução do Brasil,
que inclui a área de concentração do Banco de Abrolhos (16-19º S, 37-39º W) e a
Costa Norte adjacente (11-14º S, 37-38º W) aplicando o conceito de ecologia
acústica, nas comparações da complexidade do canto em duas regiões da mesma
área de reprodução. A freqüência do canto da baleia jubarte variou de 20 a 24000
Hz, com a freqüência central média de 596 Hz. A variação temporal para as notas do
canto foi de 0,13 a 6,55 segundos, enquanto a energia sonora foi registrada entre 62
e 130 dB (re SNR). Nós também encontramos uma alta diversidade na forma do
canto dentro e entre as duas regiões analisadas. No Banco de Abrolhos, o número
de diferentes tipos de notas variou de 14 a 40 e o numero de temas em um canto
variou de 7 a 15, enquanto na Costa Norte os tipos de nota variaram entre 10 a 21 e
os temas entre 6 e 8. Mais de um macho cantor foram registrados in 58% das
gravações analisadas (n=12), algumas vezes evidenciando o comportamento de
coro. Nós discutimos sobre a alta diversidade na forma dos cantos e amplo espectro
72
de freqüência, relacionados com características ecológicas evidentes, como a
profundidade e a plataforma continental e o coro como uma parte da arena de
reprodução necessária para engatilhar alguns dos comportamentos da baleia jubarte
durante seu período de reprodução no Brasil.
Palavras-chave: Baleia jubarte, Megaptera novaeangliae, estrutura do canto, área de
reprodução no Brasil.
73
Acoustic structure and temporal variation in the song of humpback whales
(Megaptera novaeangliae) from the Brazilian Breeding Ground
ABSTRACT
In tropical breeding areas, the male humpback whale produces highly
stereotyped and repeated sounds which combined form the song, one of the most
complex animal displays. There is a long time research effort in decipher the role of
songs in the reproductive behavior of the species, commonly attributed to serve as
an acoustic display for intra and inter-sexual selection. Despite the decades of
humpback song studies around the world, some basic characteristics, such as their
temporal and frequency parameters in a broad range, including different song units
or notes, which serve as the basis to be grouped into phrases and then to themes,
forming the song, are barely discussed. This work aims to describe humpback whale
songs in a wide geographic scale in the Brazilian breeding ground, which includes
the core area of Abrolhos Bank (16-19º S, 37-39º W) and the adjacent North Coast
(11-14º S, 37-38º W), applying the concept of acoustic ecology in the comparisons of
song complexity into two regions of the same breeding area. Humpback whale song
frequency varied from 20 to 24000 Hz, with mean central frequency of 596 Hz.
Temporal variation for song notes ranged from 0,13 to 6,55 seconds, while sound
energy was registered between 62 and 130 dB (re SNR). We also found a high
diversity in the song form, within and between the two analyzed regions. In Abrolhos
Bank, the number of different note types which composed a song changed from 14 to
40 and the number of themes in a song varied from 7 to 15, while in North Coast note
types varied from 10 to 21 and themes from 6 to 8. More than one singer male were
registered in 58% of the recordings (n=12), sometimes evidencing the chorus
74
behavior. We discuss about the high diversity on song form and broad frequency
range related to ecological remarkable features such as depth and continental shelf,
and the chorus as a part of the breeding arena necessary to trigger some of the
humpback behavior during their breeding season in Brazil.
Key words: Humpback whale, Megaptera novaeangliae, song form, acoustic ecology,
Brazilian breeding ground
75
1) INTRODUCTION
Humpback whale song was described as the most elaborated and spectacular
single display of any animal species (Wilson, 1975). The song was initially described
in detail by Payne & McVay (1971) and Winn et al (1971). Extensive analyses of this
unique vocal behavior have revealed that: (1) males produce stereotyped, ordered
sequences of sounds for long periods, (2) at any given time, sequences produced by
individuals within a breeding area are highly similar (Winn et al., 1981; Payne &
Guinee, 1983), and (3) whales continuously modify these sequences over time
(Payne et al., 1983; Payne & Payne, 1985). Explanations for the structural and
acoustic features of humpback whale songs remain speculative. Because most
researchers assume that songs are used primarily for long distance communication
(Payne & McVay, 1971; Winn & Winn, 1978; Tyack, 1981; Helweg et al., 1992;
Frankel et al., 1995; Cerchio et al., 2001; Darling & Bérubé, 2001), song features
often are interpreted in terms of how they might facilitate the transfer of information
among whales (Winn & Winn, 1978; Frankel, 1995). Additionally, song properties
could reflect strategies for collecting environmental information, if components of
songs are used as echolocation signals (Winn & Perkins, 1976; Winn & Winn, 1978;
Frazer & Mercado, 2000; Au et al., 2001).
Singers mostly appear as alone males (Winn and Winn 1978, Tyack 1981), yet
some have been documented as singing in groups (Baker and Herman 1984) and
while moving (Frankel et al. 1995). Singing appears to be most prevalent on the
winter breeding grounds, despite also recorded on the Alaskan (McSweeney et al.
1989) and Gulf of Maine (Mattila et al. 1987) feeding grounds and during migration
(Clapham, 1996, 2000).
76
Humpback whale songs show clear structure based on aural analysis, with
smaller repetitive units called “phrases” organized into larger “themes” which tend to
occur in specific sequence (Payne and McVay, 1971, Guinee et al., 1983) (figure 1).
The structure of song changes over the course of a winter season, yet at any given
time all singers appear to be singing the same version of a song (Guinee et al., 1983,
Payne et al., 1983, Payne and Payne, 1985).
The relationship between singing and seasonal gonadal activity suggests that
song production plays a role in the mating system. While humpback whale song
appears to be the result of strong sexual selection (Tyack, 1981, Smith, 2008), its
function in the mating system remains unclear. Helweg et al. (1992) presented a
detailed summary of current hypotheses regarding the role of humpback whale song,
but its role is still far from certain. A number of possible functions of song have been
proposed, including sexual advertisement to females (Payne and McVay, 1971; Winn
and Winn, 1978; Tyack 1981, 2000), maintenance of spacing and territorial defense
among singing males (Winn and Winn, 1978; Tyack, 1981; Frankel et al. 1995),
inducement or synchronization of ovulation in females (Baker and Herman 1984),
and a navigational “beacon” for migrating whales (Winn and Winn 1978).
Songs of humpback whales are typically recorded close to a whale in order to
maximize the signal-to-noise ratio. However, when sounds are recorded at large
distances from any whale, a number of whales singing may sound as in a chorus,
although they do not sing in unison on the same portion of a song (Au et al., 2000).
The most studies bring acoustic information only by spectrograms (eg. Payne
& McVay, 1971; Winn et al., 1981; Arraut & Velliard, 2004).The evolution in the study
of the humpback whale frequency range is proportional with the advance in
technology. The initial studies reported song range between up to 5-8 kHz (Payne &
77
Mac Vay, 1971; Winn et al., 1971), and thereafter it goes up to 15-24 kHz (Helweg et
al., 1992; Au et al., 2000, 2001, 2006; Fristrup et al., 2003). Mercado et al. (2003)
measured acoustic patterns in humpback whale songs recorded in Hawaiian waters
during four consecutive years (1992–1995) to determine whether subcomponents of
songs differ in their detectability after long-range propagation. Such analyses can
provide important insights into the functions of humpback whale songs.
Singing whales most often are reported to be alone (Winn & Winn, 1978;
Tyack, 1981) although there are exceptions (Baker & Herman, 1984). It is generally
accepted that singing is done by males where calves are being born and seasonal
gonadal activity is high (Chittleborough, 1955; Payne & McVay, 1971).
This work aims to describe humpback whale songs in a wide geographic scale
in the Brazilian breeding ground which includes the core area of Abrolhos Bank and
the adjacent North Coast, comparing song form in different marine landscapes,
adapting the Acoustic Ecology concept of Truax (1999), who define it as the study of
relations between biological organisms and their sonic environment, or soundscape.
78
79
Figure 1: Representation of the types of structural components typically present in
sequences of sounds produced by singing humpback whales (Megaptera
novaeangliae). Each letter represents one sound. Each individual sound is called a
unit (different letters correspond to aurally distinctive sound units). Repeated groups
of units are called phrases (black lines). A theme is a set of phrases (gray line).
Songs consist of repeated theme sequences within a song session (1 to 4 complete
the cycle, thereafter song session starts again).
2.1) Study Area and Population Stock
We conducted this study, from 2005 to 2010, at the Northeastern Brazilian
coast during the breeding season (July to October) of the Southwestern Atlantic
Ocean humpback whale population, known as Breeding Stock A (BSA) by the
International Whaling Commission (IWC, 1998). Humpback whale songs were
recorded along the study area, grouped in two main regions: Abrolhos Bank (16-19º
S, 37-39º W) and North Coast (11-14º S, 37-38º W) (figure 2).
80
Figure 2 – Humpback whale (Megaptera novaeangliae) study area off Northeastern
Brazil (Breeding Stock A), divided in two regions: a southern region, the Abrolhos
Bank and a northern region, named North coast, located between Itacaré (BA) and
Aracaju (SE). The line represents the 200 meters isobath, demarking the Brazilian
continental shelf.
Recordings were made by deploying a hydrophone from a small boat
positioned less than 50 m from the singing whale. During this period diverse
recording equipment was utilized, according to the increase of technology available
in Brazil. Therefore, sound data collected from 2005 to 2008 were made using an
uncalibrated HTI – SSQ 96 hydrophone (sensitive to 20 kHz) that was connected to a
Sony TCD5-M cassette recorder, frequency response up to 17 kHz). From 2008 to
2010 we utilized a CR 54 hydrophone connected to a digital recorder (M-Audio
Microtrack Pro-II), increasing the frequency response up to 96 kHz.
81
Analyzes were first made both by listening and by visually comparing
spectrograms, which are sound graphics with x-axis on time (seconds) and y-axis on
frequency (Hertz). Spectrographic analyzes were performed using software RAVEN
3.1, selecting the following frequency parameters (Hertz), relative sound intensity (dB
re SNR - referenced to the Signal to Noise Ratio) and time (seconds): minimum,
maximum, central frequency, frequency amplitude, energy and duration. Whenever
found, the harmonics and their intervals were also measured, as well as the visual
contour shape from each note.
3) RESULTS
During 6 years we obtained a record effort of more than 50 hours. From these
raw data, we selected “type” songs from each sampled year, for both areas of
Abrolhos Bank and the North Coast, chosen by containing all the characteristic
phrases of the song from that year, as well by presents the best signal to noise ratio.
In some years, like 2007, more than one song was selected, produced at different
time during the breeding season, due to its high quality to extract additional acoustic
information.
3.1) Acoustic parameters
We measured a sample of 2868 component notes to describe the acoustic
parameters of the humpback whale song in the Brazilian breeding ground. Data
showed a wide frequency variation, typical from the long and complex humpback
whale song, ranging from 20 Hz to the top of sampling rate (24,000 Hz), short
duration notes (mean = 1,06 sec) and sound energy from 60 to 130 dB re SNR (table
82
1). However some features are remarkable, such as the mean central frequency at
low frequency (596 Hz) (figure 3) and the intense sound energy putted into sound
transmission (mean= 105 dB).
Harmonics were registered in 2098, 73 % of the measured notes, varying in
number of 1 to 85 (mean = 10,4). Harmonic intervals ranged from 10,3 to 4309 Hz
(mean = 405).
Table 1: Acoustic parameters from the humpback whale (Megaptera novaeangliae)
song (sample = 2868 notes), in the study area, Northeastern Brazilian coast.
Sample = Minimum
2868
Maximum
Central
Frequency Duration
Frequency Frequency Frequency Amplitude
Energy
(s)
(dB)
(Hz)
(Hz)
(Hz)
(Hz)
20
110
21,5
80,2
0,13
62
Maximum 5245
24000
6421,9
24000
6,55
130,4
Mean
224,4
4422
596
4198
1,06
105
St.Dev.
391
4695
625
4658
736
8,7
Minimum
83
Figure 3: Combination of spectrograms, a sound graphic with x-axis on time
(seconds) and y-axis on frequency (kiloHertz), exemplifying some of the different
humpback whale (Megaptera novaeangliae) notes with its remarkable mean central
frequency around 500 Hz (indicated by black circles) Blue line graphs above
represent the respective oscilograms or waveforms, sound graphics with x-axis on
time (seconds) and y-axis on pressure (ku).
3.2) The humpback whale song form
The song form, with descriptive information on the total number of notes,
number of different notes and number of themes was represented by some best
quality recording of each year for the Abrolhos Bank (table 2) and for the North Coast
(table 3). Additionally, the number of singer males that could be heard at the
background noise without confuse the main singer was also recorded.
84
Table 2: Humpback whale (Megaptera novaeangliae) song characteristics from the
northeastern Brazil (Abrolhos Bank), between 2005 and 2008, showing recording
information –file identification and day-, file duration (minutes:seconds), total number
of notes, different note types, number of themes and number of singers registered in
each recording file.
SONG#
DAY
DURATION TOTAL
NOTE
N
N
(m:s)
NOTES
TYPES THEMES SINGERS
ABL 2005 26jul05
12:20
160
14
8
>3
ABL
11:20
200
16
10
2
24:12
290
21
8
2
20:00
151
39
12
1
16:25
220
40
15
3
21Out08 56:14
188
24
7
1
2006a
ABL
2006b
ABL2007- 10Jul07
1
ABL20072
ABL2008
85
Table 3: Humpback whale (Megaptera novaeangliae) song characteristics from the
northeastern Brazil (North Coast), between 2005 and 2010, showing recording
information –file identification and day-, file duration (minutes:seconds), total number
of notes, different note types, number of themes and number of singers registered in
each recording file.
SONG #
DAY
DURATION
TOTAL
NOTE
N
N
(m:s)
NOTES
TYPES
THEMES SINGERS
ITA2005
20Ago05
50:00
212
17
8
2
F_ITA2006
06Ago06
35:00
131
21
8
1
20:00
78
14
6
1
FtVD-2008
ITA2009
04Ago09
35:00
101
12
6
2
PF2009
18Ago09
35:00
180
15
7
2
PF2010
Ago10
30:00
85
10
6
1
The diversity in our recording systems evidenced that the humpback whale
song has a wider frequency range than previously commented, with some notes
exceeding the frequency response in some occasions (figure 4).
86
Figure 4: Spectrogram showing humpback whale (Megaptera novaeangliae) notes
surpassing the frequency response (24 kHz) of recording equipment (some evident
notes indicated by arrows) utilized in the acoustic study off Northeastern Brazil.
Behavioral observations of 50 minutes, simultaneous to the song recording of
FV_ITA2006 sequential files, made at 34 meters deep, indicated that the singer male
stops singing once blowing at the sea surface in short dive times (less than 30
seconds), when silent moments were registered (figure 5).
Figure 5: Spectrogram exemplifying one minute window from the FV_ITA2006
recording, indicating silent moments (black rectangles) once blowing at the sea
87
surface during short dives (less than 30 seconds) of the humpback whale (Megaptera
novaeangliae) in Northeastern Brazil.
3.3) Chorus behavior
During many times (66% = 7 from the 12 files presented in tables 2 and 3) we
could register the presence of more than one simultaneous singer male at the
recordings, identified by the different intensities in sound caption, plus overlay of
different song parts in the same file. More than two singer males, and even more
than 3, were registered only in the Abrolhos Bank in two occasions (33% of 6 files).
After sound analyzes it was interestingly remarkable that when more than one
male was singing, forming a chorus, the predominant song structure was much
simpler song part than during singing of only one male, and composed, for example,
by a long (4 sec) whistle and a short hiccup, or even a long moan (figure 6).
Figure 6: Spectrogram exemplifying multiple male singing of the humpback whale
(Megaptera novaeangliae), characterized by simpler parts of the song, in their
breeding area off Northeastern Brazil (different colors exemplify different singers).
88
4) DISCUSSION
4.1) Acoustic parameters
Despite the long list of studies in more than 40 years of research about the
singing behavior of humpback whales (eg. Payne & McVay, 1971; Tyack, 1981;
Payne & Payne 1985; Helweg et al., 1998; Mercado et al., 2003; Au et al., 2006), still
there are few descriptive studies that present numeric values for frequency, duration
and sound intensity. This work brings the first song description in the Brazilian coast,
outside the Abrolhos Bank, showing that humpbacks are utilizing a broader acoustic
environment for their breeding activities than previously reported.
Frequency parameters varied from 20 Hz (minimum) to 24000 Hz (maximum),
being the interval between mean frequencies of 224,4 a 4422 Hz, duration of 0,13 to
6,5 seconds (mean = 1,06) and sound energy ranging from 62 to 130,4 dB (re SNR)
(mean = 105).
Oviedo et al., (2008), studying at Las Perlas Archipelago, Panama Gulf,
reported frequency parameters for year 2006, such as the minimum frequency (129,2
to 575,7 Hz), maximum (1151,7 to 2879,6 Hz) and note duration (0,79 to 5,50 s) and,
for 2007, the minimum frequency (129 to 1076 Hz), maximum (2368 to 4866 Hz) and
note duration (0,66 to 11,4 s). Number of notes varied from 13 to 15. Same authors
also describe the environment as being calm and shallow waters, contributing to the
whale breeding cycle, similar to the oceanographic conditions we observe in the
Abrolhos Archipelago.
Arraut & Vielliard (2004), in Abrolhos Bank, reported 24 notes and 5 themes
as the humpback whale song structure, during the breeding season of 2000, bringing
89
only spectrograms as a physical reference for the acoustic parameters, with
frequency axis ranging from 500 to 2000 Hz.
Thus the present work show similar frequency values from other geographical
areas, such as the Panama Gulf (Olviedo et al., 2008), however, apparently by the
spectrograms reported by Arraut & Vielliard (2004), song varied temporally inside the
same breeding area off Brazil.
Another relevant finding from this study is the high frequency harmonic
occurrence reaching the top of the frequency response (24 kHz). Au et al., (2006)
reported high frequency harmonics for the humpbacks in the Hawaiian waters,
suggesting the species may show a upper hearing limit as high or higher than this
value.
The humpback whale song in this work seems to be more diverse and
complex than other reported areas, such as in Hawaii, where Au et al., (2006)
described 9 notes compounding the song of 2002. For the Brazilian coast, Arraut &
Vielliard (2004) identified a similar number of notes, grouped into 5 themes, in the
breeding season of 2000. This may represent the gradual modification described in
literature (eg. Payne et al., 1983; Payne & Payne, 1985) e o aporte de dados dos
anos subsequentes poderá contribuir com uma melhor interpretação deste resultado.
The values for maximum frequency were larger than previously reported,
which could indicate a better signal adaptation to the specific Brazilian acoustic
environment. In this case, there is a big difference between the depth gradient
utilized by the whales in places like the Abrolhos Bank and the environment of the
narrow continental shelf from Itacaré to Aracaju. This consideration is strengthen by
the harmonic values reported for Hawaii (Au et al., 2006), where the depth is similar
to part of our study area, which include deeper waters. Biological implication of this
90
would be a maximization of the reproductive signal travelling across the acoustic
environment to increase the mate opportunities during the time-limited breeding
season.
Thus, beyond the descriptive analyzes of the acoustic parameters for the
song, this work bring information of the relations between song frequency and
duration with the acoustic environment in which it is produced, stating that
differences may occur even in a smaller geographic area, such as inside the same
breeding area, where environmental differences may result in distinct song
components, as shown with the maximum frequency and note duration.
Also, seems to be obvious that the advance in technology in the last decades
have shown a broader frequency spectra utilized by humpback whales. In this way,
the first decade in the “boom” of humpback song research was the 70´s, where notes
were registered below 5 kHz (eg. Payne & Mac Vay, 1971, Winn, 1978) as well as
during the 80´s (eg. Payne & Payne, 1985). The digital recording “Era” increased
more than twice the previous frequency response, bringing the higher frequencies
identifiable to the humpback repertoire (eg. Au et al, 2006, Mercado et al., 2003,
present work).
4.2) Song form
We found a diverse and complex song structure along the time, resulting in
remarkable differences within a 6 years period of study (2005 to 2010). Such
differences are broader than previously commented, even considering the
differences inside the same breeding area, where environmental characteristics may
contribute with signal diversity and specificity.
91
Payne & Payne, 1985 analyzed and compared humpback whales songs in
Bermuda for 13 years, between 1957 and 1975. They found that song changed
conspicuously and progressively with time, being the songs separated by a number
of years were very different in content. Furthermore, all the songs showed basic
structural similarities making possible to define a song form which characterizes
songs from many years. Such analyses demonstrated high inter and intra-individual
variability, none of which is as great as the variation between songs of consecutive
years. Our study is the first long term acoustic description to both Atlantic and Pacific
coasts of South America, bringing important information on temporal variation in the
humpback whale songs to this area.
Winn & Winn (1978) suggested that because low frequencies within humpback
whale songs are attenuated less than high frequencies during propagation, higher
frequency units might be used for transmission over short ranges whereas lower
frequency units might be used for longer ranges. Mercado & Frazer (1999) add to
this notion that it also depends on the depth where whales sing, because in shallow
water environments in Hawaii, the lowest frequencies they produce do not propagate
as far as the higher frequencies they produce). Mercado et al (2003) also pointed out
that no single frequency will propagate optimally to all positions within the water
column. Thus, increasing the range of produced frequencies could increase the
number of positions within a shallow water environment from which the sound could
be detected.
Another possible argument to the high variability found in the form of
humpback whale song in the Brazilian coast (present study) could be related to the
high capacity of copying in humpbacks, controlling changes over time that can
abruptly be modified (Noad et al., 2000), which suggest that individual whales select
92
patterns and units to include in songs based on their recent experience, or kept in
use during next seasons (Payne & Payne, 1985; Cato, 1991; Mercado et al., 2005).
Furthermore, Mercado et al. (2005) discuss on song copying by humpback whales as
being an open process in the spectral domain in that specific frequencies could be
utilized by each different individual within or across years and that species-specific
constraints determine song form and regionalization. These affirmations could, in
part, explain the present results on the diversity of song structure between the two
regions, the Abrolhos Bank and the North Coast of our study area.
Sequences of alternating tonal and pulsed units in humpback whale songs
also could be possibly related to internalized ‘inspiration’ and ‘expiration’ of air during
sound production (Mercado et al., 2003). Further studies involving size estimation in
the two regions of our study area could help to elucidate the matter of body size and
song diversity, comparing song production among individuals of different sizes.
Despite the high variability within and between seasons, some song
components are said to recur for over decades (Payne & Payne, 1985; Mercado et
al., 2003) indicating important features which may be maintained during time to build
an effective communication system.
4.2.1) Song form diversity and function
It is still debated the complete role that songs serve for (revised in Parsons,
2008). The behavior that accompanies singing indicates that it probably plays a part
in courtship analogous to the role of singing in birds (Tyack 1981). Some authors say
that it is primarily for inter- and intra-sexual advertisement, informing females about
the location and reproductive fitness of singers, and informing other males about the
location of singers to produce spacing among multiple singers (reviewed by Helweg
93
et al., 1992; Clapham, 1996), or advertising the fitness of males (Darling & Bérubé,
2001). A different interpretation of the function of the song involving a cooperative
male behavior during group formation in discussed by Darling et al., (2006).
4.3) Chorus behavior
The chorus behavior is described as a part of the complex leking, where males
tend to defend resources to which females are attracted, in this last case gain from
stimulus pooling by displaying together and providing greater attraction for females
(Krebs & Davies, 1993). This strategy has been largely studied for ungulate, bats and
frogs (revised in Krebs & Davies, 1993).
While much attention has been given to the characteristics of songs, few
studies go into the chorus behavior by multiple humpback whales (Au et al., 2000).
Thompson and Friedl (1982) were the first to mention chorusing for the humpbacks in
Hawaii, finding seasonality and daytime preference for chorusing in a breeding area.
Au et al. (2000) described spectral features as well temporal utilization of the
chorus behavior in the humpbacks during the 1998 Hawaiian season, showing
spectral peaks at 315 Hz and 630 Hz. Their data also indicated a diurnal pattern in
the sound pressure level, with levels at night significantly louder than the daytime
levels, attributing different mating strategies to the species during a night and day
scale, in which competitive groups are more frequent during the day, requiring more
visual contact, while chorusing are more frequent during the night time.
Our study brought for the first time the chorus perspective to the humpback
whale acoustic ecology in the Brazilian waters. The higher occurrence of chorus
found in the Abrolhos Bank could indicate that this behavior should act as a trigger to
the female choice as described for the terrestrial leks (Alcock, 1993; Krebs & Davies,
94
1993). Listening to an intense chorus, females would be guided to a good area
concerning the search for a mate. Additionally, we are in accordance to the Au et al.
(2000) suggestion of the viability of using different levels of chorusing to monitor and
estimate the relative abundance of male humpback whales in the Brazilian breeding
ground.
Summarizing, there are numerous hypotheses on the implications of the
humpback whale song, many of which are not mutually exclusive. The fact is that
many aspects of the humpback whale song components remain unknown, such as
what are the reasons to keep for a longer time some components instead other and
what kind of significance it has on reproductive success over time.
The humpback whale, as a migratory animal, requires a broad geographic
scale to develop essential activities such as feeding and breeding, for consequence
implying on a huge logistical structure to access their habits in accordance to such
large scale.
The Ocean is a challenging environment to man, in the path of an ecological
comprehension and global vision. Therefore, we still know very few about the whole
implication of the humpback whale role in this broad oceanic scale. Perhaps in a near
future, besides with the necessary technology to the understanding of oceanic
processes in a deeper approach, we will find in the humpback whale song a key to
last a long time with respect to this planet.
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humpback whales: themes and variations. Animal Cognition, 8, 93-102
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in response to sonar. Nature, 405 (6789), 903.
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Whale (Megaptera novaeangliae) Song. .Journal of Marine Animals and Their
Ecology, 1 (1), 22-31.
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Payne, S., & Guinee, L. N. 1983. Humpback whale (Megaptera novaeangliae) songs
as an indicator of “stocks”. In. Communication and behavior of whales. (Ed R.
Payne), pp 333-358. Boulder, CO: Westview Press.
Payne, K. P., Tyack, D. R., Payne, R. 1983. Progressive changes in the songs of
humpback whales (Megaptera novaeangliae): A detailed analysis of two seasons in
Hawaii. In. Communication and behavior of whales. (Ed R. Payne), pp 9-57. Boulder,
CO: Westview Press.
Payne, K, & Payne, R. 1985. Large scale changes over 19 years in songs of
humpback whales in Bermuda. Zeitschrift fur Tierpsychologie, 68, 89-1 14.
Smith, J. N., Goldizen, A. W.; Dunlop, R. A. & Noad, M. J. 2008. Songs of male
humpback whales, Megaptera novaeangliae, are involved in intersexual interactions.
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from several species of whales off Oahu, Hawaii. Cetology, 45, 1-19.
Tyack, P. 1981. Interactions between singing Hawaiian humpback whales and
conspecifics nearby. Behavioral and Ecological Sociobiology, 8, 105-116.
Tyack, P. 2000. Functional aspects of cetacean communication. In: Cetacean
Societies: Field Studies of Dolphins and Whales (Ed Mann, J., Connor, R. C., Tyack,
P. L. & Whitehead, H), pp 270-307. Chicago, IL: Chicago Press.
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Winn, H, E., Perkins, P. & Poulter, T. 1971. Sounds of the humpback whale.
Proceedings of the 7th Annual Conference on Biological Sonar and Diving
Mammals.Menlo Park, California, 39-52.
Winn, H. E. & Perkins, P. 1976. Sounds of the minke whale, within a review of
misticete sounds. Cetology, 19, 1-12.
Winn, H. E. & Winn, L. K. 1978. The song of the humpback whale Megaptera
novaeangliae in the West Indies. Marine Biology, 47, 97-114.
Winn, H., E., Thompson, J. T., Cummings, W.C., Hans, J., Hudnall, J., Hays, J.,
Steiner, W. 1981. Song of the humpback whale: Population comparison. Behavioral
Ecology and Sociobiology, 8, 41-46.
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Artigo 3 – Indústria do Petróleo e poluição acústica na área de reprodução da
baleia jubarte (Megaptera novaeangliae), no Oceano Atlântico Sul ocidental.
Marcos R. Rossi-Santos 1,2
1-
2-
MARINE POLLUTION BULLETIN (A2, fator de impacto = 2,314)
A ser submetido
102
RESUMO
A poluição sonora marinha está constantemente aumentando no mundo e é
considerada como uma preocupante ameaça para toda a vida aquática. O presente
trabalho tem o objetivo de estudar a possível sobreposição acústica entre o canto da
baleia jubarte e os ruídos antropogênicos ao redor de plataformas de exploração de
petróleo e gás, através da descrição espectral e comparações de freqüência. Dentro
de um monitoramento sistemático na região Nordeste do Brasil (11° S, 37° W - 14°
S, 38° W), dados bioacústicos foram coletados entre 2007 e 2009, com foco na
ocorrência da baleia jubarte ao redor das plataformas localizadas na área de estudo.
Diversos ruídos antropogênicos foram encontrados, em freqüências similares
àquelas que são utilizadas pelas jubartes como parte de seu complexo
comportamento reprodutivo, o que sugere uma sobreposição de nicho acústico. A
poluição sonora originada da produção de petróleo e gás potencialmente pode afetar
a comunicação da espécie, com implicações em sua distribuição e comportamento
na área de reprodução. Este trabalho é o primeiro a reportar uma descrição e
comparação acústica entre plataformas e cetáceos para o Oceano Atlântico Sul
ocidental, clamando por esforços para o desenvolvimento e inserção da bioacústica
como ferramenta de monitoramento científico diante da crescente exploração de
petróleo e gás no mar do Brasil.
Palavras-chave: Cetáceos, baleia jubarte, ruído antropogênico, indústria do petróleo,
Brasil
103
Oil industry and noise pollution on the humpback whale (Megaptera
novaeangliae) acoustic environment in the Southwestern Atlantic breeding
ground
ABSTRACT
Marine noise pollution is constantly increasing around the world and recalled
as a concerning threat to the aquatic life. The present work aims to access acoustic
overlapping between the humpback whale song and anthropogenic sounds around
oil and gas platforms, through spectral description and frequency comparison. Within
a systematic whale monitoring in Northeastern Brazil (11° S, 37° W - 14° S, 38° W),
bioacoustic data was collected from 2007 to 2009, focusing on humpback occurrence
around oil platforms in the study area. Diverse anthropogenic noises were found, in a
similar frequency range than the recorded cetacean sounds, which suggests
overlapping of acoustic niches. Noise pollution from oil and gas production potentially
may affect the species communication, with implications on its distribution and
behavior in their breeding area. This paper is the first report of acoustics between oil
platforms and cetaceans for the Southwestern Atlantic Ocean, urging efforts to the
development and insertion of this research tool, facing the increase of gas and oil
exploitation.
Keywords: Cetaceans, humpback whales, anthropogenic noise, oil platform, Brazil
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1. INTRODUCTION
1.1)
Noise in the marine environment
Noise may be defined as a sound that interfere the signal reception or even
affect the animal ecology, disturbing their common behavior (Richardson et al, 1995).
The marine acoustic environment is formed by a diverse sources of noise, which
reflect in the perception and behavioral responses for different animal species,
mainly the vertebrates (McCauley et al., 2000a, 2000b; Miller et al., 2000; Cato &
McCauley, 2002).
So on, the acoustic environment that whales face today is different from they
faced about 50 years ago (eg. Andrew et al., 2002), prior the whaling period, even
more in the tropical breeding areas, much more populated and where the animals
spend about six months per year to find a reproductive partner, to breed, give birth
and take care of their young until the next migration to the poles (eg. Clapham,
1996).
The increase in the human population along the years, concentrated in the
coastal zone, have resulted in an increase of boat-ship traffic and the oil industry,
reaching certain acoustic pollution levels that can harm individual animals, causing
temporary or even permanent injuries in their physiology and behavior (eg:
Richardson et al., 1995, Johnson et al., 2007).
Signal detection by a marine mammal is affected by the noise interference in a
similar frequency band than any biological acoustic signal or by the individual hearing
sensitivity inside the same species (eg. Au & Moore 1990, Erbe & Farmer 1998,
Southall et al. 2001, Finneran et al. 2002).
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The effects of anthropogenic noise in marine mammals have been increasable
studied and revised in literature. (eg. Richardson et al, 1995, NRC 2000, 2003; Hatch
& Wrigth, 2007). Depending of the sound source features and the type of the
acoustic environment, which may affect sound propagation, sound may affect them in
a diverse way, as turning difficult the signal detection, causing masking of specific
signals, changing natural behavior or even causing hearing injuries (Richardson &
Wursig, 1997; Kastak & Schusterman 1999, Schlundt et al. 2000, Croll et al., 2001;
Nachtigall et al. 2003).
1.2)
The humpback whale
The humpback whale, Megaptera novaeangliae, (Cetacea, Balaenopteridae),
is a cosmopolitan cetacean species distributed along all the oceans worldwide
(Clapham & Mead, 1999). As migratory animals, they move yearly from high latitude
feeding areas, staying during the autumn and summer, to the breeding areas in the
tropics, staying during the spring and summer (Clapham & Mead, 1999). These
breeding areas are typically between islands and/or associated with coral systems
(Whitehead & Moore, 1982; Clapham, 1996).
In the feeding and breeding area, the humpback whale present a social
organization characterized by unstable and small groups (2 to 3 animals). However,
larger groups can be found during the feeding behavior or related to the aggressive
competition between males during the breeding season (Clapham, 1996).
1.2.1) Occurrence and Distribution
There are seven humpback whale sub-populations (or stocks) in the southern
hemisphere, one of these, named by International Whaling Commission “Breeding
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Stock A/ BSA” (IWC, 1998), migrates to the Brazilian coast, where they breed and
take care of their calves from July to November.
Humpback whales occur along a large range in Brazil, from Rio Grande do Sul
state to Maranhão state, including oceanic areas of the Atol das Rocas, Fernando de
Noronha and Trindade Islands (Tollenare, 1961; Lodi, 1994; Danilewicz et al., 2009;
Wedekin, 2011), with its core breeding area in the Abrolhos Bank, Bahia state
(Martins et al., 2001; Andriolo et al., 2006a,b; Wedekin et al., 2010). During the last
decade, an increase of humpback whale sightings northwards from the Abrolhos
Bank, including the Bahia capital, Salvador and the north coast of the state, was
reported, suggesting the effective population recovery in this historical area, occupied
by the whales prior the whaling period (Rossi-Santos et al., 2008).
Despite the apparent end of commercial whaling, most of the large whale
species are still threatened by anthropogenic activities such as fishing net
entanglement, collisions with vessels, oil/gas exploitation,
chemical and noise
pollution (for revision, see Clapham 1996; Hatch & Wrigth, 2007).
1.2.2) Acoustic Ecology and Behavior: importance of sounds
The humpback whale is also known as “singer whale” because its unique
characteristic of to exhibit a singing behavior, performed only by males, during their
breeding season. Since the 70ths, many studies described the physic structure of the
songs (eg. Payne e Mc Vay, 1971; Helweg et al., 1998; Maeda et al., 2000; Arraut &
Vielliard, 2004).
Males sing during the breeding season, probably with the function of attract
females (eg. Smith et al., 2008) and/or to repel other males (eg. Tyack & Whitehead,
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1983; Weinrich, 1995). The song is constituted by single notes which form repetitive
phrases called theme, and different themes form a song (Payne & McVay, 1971).
Generally, the singer males are observed alone, and individuals from different
populations produce different songs, what is being used to describe and differentiate
humpback whale populations wordwide (eg. Winn & Winn, 1978; Matilla et al., 1987).
The song is being slowly modified along the time, becoming a different song after
about five years ( Payne et al., 1983; Payne & Payne, 1985; Noad et al., 2000).
Probable functions at the population ecology level, such as stock recognition
by songs and cultural exchange between adjacent populations have been reported
(Winn et al., 1981; McSweeney et al., 1989; Dawbin & Eyre, 1991; Darling & SousaLima, 2005; Eriksen et al., 2005), however many other aspects of the acoustic
ecology of the species during the singing behavior is still unknown, including the
description of acoustic occurrence in diverse anthropogenic environment and
contexts.
The humpback whale song has a crucial importance in the reproductive
success of the species, when they are temporally engaged in mating activities, which
include the search of reproductive partners to perpetuate, in last instance, their
genes to the next generations in that local population. So on, any disturbance in this
delicate moment may affect individual reproductive success and, in a broader view
the success of an entire population.
1.3)
The Oil Industry in Brazil
The oil industry in Brazil was, in an early period, characterized by the
monopoly of Petrobras, created by the Brazilian government in 1954, as a State
company, to reduce economic risks derived from the oil crises worldwide since that
108
time (Kimura, 2005). Additionally, the post-war period, in the early 50s, was marked
by the discovery of many oil reserves around the globe, and in this context, Brazil did
not wake interests of foreign companies, despite the propitious conditions to oil
formation spread in 3 millions squared kilometers of sedimentary basins (Matz,
2000).
The international economic crises in the late 80s and early 90s caused a deep
change in the companies’ mentality, which start to focus their investment in their
core-business, the energy sector, initiating many fusions with other companies to
reduce costs and to enhance productive scale (Matz, 2000; Kimura, 2005).
The Brazilian law 9.478 retreat the monopoly of Petrobras, authorizing other
companies to exploit and explore in the national territory, attracting a competitive
market, which is increasing year by year (Machado, 2004; ANP, 2003).
1.4)
Objective
The present work aims to make an acoustic analysis of anthropogenic noise
originated from oil and gas exploitation activities in the Brazilian breeding ground for
the humpback whale, an endangered species considered as an important top
predator for the marine ecosystem. Potential overlapping of acoustic niche of the
whales and noises is also analyzed and discussed.
2.1) Study area
For this work we encompassed a stretch of coast between the northeast states
of Bahia and Sergipe, joining the North Coast of the State of the Bahia, with a littoral
109
band of approximately 14 km of extension, going from Itacaré (14° S, 38° W) to
Aracaju (11° S, 37° W), capital of Sergipe state, with Praia do Forte (12° S, 38° W)
placed in the center of this area, located about 60 km from the capital Salvador
(figure 1). The region between Praia do Forte and Aracaju , is characterized by long
sand beaches, with large dune formation fringing the coast line.
The main oceanographic characteristic for this total area (study area) is a
narrow continental platform, with approximately 15 km of extension. Throughout the
platform, its average of depth is of 40 meters and the amplitude of tide varies
between 0.1 2.6m (DHN, 1995).
This area also have large bays and estuaries, important to navigation, such as
the Baía de Todos os Santos, surrounding Salvador, Bahia state and the estuaries of
Vaza-Barris river and Sergipe river, near Aracaju, Sergipe state.
Beyond the anthropogenic pressing from large ports such as Salvador and
Aracaju, and the presence of traditional fishing communities, this area also hosts the
largest petrochemical industrial center of all the Southern Hemisphere, in Camaçari,
Bahia state. Equally important are the first established coastal oil platforms of the
Brazilian coast, in Aracaju, Sergipe state and some more platforms recently installed
in Bahia state, near touristic destinations of Morro de São Paulo and Itacaré
localities.
Some years ago, a consortium of organizations headed a public campaign to
exclude the Abrolhos Bank, the core area for the humpback whale distribution in
Brazil (Wedekin et al., 2010) from the increasing commerce of exploitation blocks
along the southeastern and northeastern coasts (figure 1), obtaining a temporary
success.
110
However, as the humpback whale stock A is increasing (eg., Zerbini et al
2006), other areas in the Brazilian coast have been occupied (Rossi-Santos et al.,
2008; Wedekin et al., 2010; Baracho-Neto et al., 2012) and the marine acoustic
landscape including whales and the Oil Industry became undeniable.
Figure 1 –
Study area, located between Itacaré, Bahia state (14°S, 38°W) and
Aracaju, Sergipe state (11°S, 37°W), Northeastern Brazil. Blue squares represent oil
exploitation blocks, while red dots represent the recorded platforms inside the study
111
area. The Abrolhos Bank is presented to reference the core area of humpback whale
(Megaptera novaeangliae) distribution in Brazil.
2.2) Data collection and analyses
2.2.1) Behavioral methods
To the behavioral observations during the sightings including platforms it was utilized
the combined Focal-group and Ad libitum method (see Mann et al., 2000) which
consists in registering a sequence of a certain behavior during the observation time,
broadly employed in the cetacean studies. To the group structure definitions and
classification we followed the nomenclature proposed by Clapham (1996) (to more
information about methods, see Rossi-Santos et al, 2008).
2.2.2) Research Cruises
Boat based surveys were utilized, searching for whales in a determined route,
approaching animals when sighted to collect general data such as geographic
location, behavior, photoidentification, skin biopsies and bioacoustic recordings,
following a standard protocol, including group structure definitions and classification
(see Rossi-Santos et al, 2008).
A laser range finder (Bushnell Elite 1500) was utilized by one team observer to
measure distances from the recorded objects, including whales, platform and supply
boats to the hydrophone.
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2.2.3) Bioacoustics
The recording equipment varied along the years according to the worldwide
increasing of technological advance in audio and video acquisition systems and its
availability in Brazil. In 2007 whale songs and noises were recorded utilizing an
analogical-digital system (Sony VX-1000 video-camera) always plugged to the same
hydrophone (HTI SSQ-94). Since 2008 a full digital system was adopted (M-Audio
MicroTrack Professional II digital recorder), resulting in an increased frequency
response of 48 kHz.
In the laboratory, analogical and analogical-digital tapes were digitized to
export the raw sound data to the analyze platform, the software RAVEN 1.3 (Cornell
University/USA). Once in a digital system, audio format was selected as
uncompressed WAV files and then saved in a data-base.
After digitized, the biological and the man-made sounds were analyzed,
through spectral visualization, to extract physical parameters such as: begin
frequency, end frequency, mean frequency, maximum frequency, minimum
frequency, amplitude, duration and energy (sound intensity).
Data were selected using the best quality to visualize the complete signal,
utilizing the screen cursor upon spectrograms, a sound graphic with axes on
frequency, measured in Hertz (Hz), and time, measured in seconds (sec). After a
signal is selected, the software provides the precise measurements and these
numeric values are exported to a data-base software for a posteriori analyzes.
Is notable to recall that the sound intensity measurement, the decibel (dB), is
considered a relative value to a certain energy source (Hatch & Wright, 2007) and, as
our recording systems were uncalibrated, we only had the reference of the Signal to
113
Noise Ratio (dB re - SNR) provided by RAVEN 3.1 to be utilized for the comparative
analyzes.
3) RESULTS
3.1) Behavioral observations
Between 2007 and 2009, it was performed a total of 527 h of sampling effort of
the humpback whale and environmental monitoring, distributed in 69 days, summing
166 sightings of whale groups during the systematic field work. Groups containing
any singer male were confirmed by close (no more than 100 m) underwater
recordings.
During the sampling effort, humpback whales were sighted in 6 occasions
around oil and gas platforms in distances less than 60 meters. Group composition
was defined as alone singer males in 3 sightings (122 minutes of observation and
recordings). In one occasion the singer was actively singing and presenting long and
similar breath intervals (14:00, 16:50, 16:43 minutes). Females with calves plus an
escort male were recorded in 2 sightings (75 minutes) constantly diving and avoiding
the supply boat around the platform. During one occasion a group of 3 adult animals,
including one singer was observed.
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3.2) Anthropogenic noises
Different categories of anthropogenic noises from oil and gas platform operation were
recorded and analyzed (figure 2).
Figure 2: Marine environment with the occurrence of anthropogenic noise from the oil
and gas industry, showing different noise sources, such as platforms and supply
boats, utilized in the daily operation.
During this period, 40 sound files were selected by the Best signal to noise
ratio (signal quality in relation to the background noise). For each measured acoustic
parameter were extracted the minimum, maximum, mean value and the standard
deviation, shown in the table 1.
115
Distinct noises were registered, varying from direct (figures 3, 4, 5) and
indirect (figure 6) from the physical structure of the platform properly. Noise varied in
frequency from 5 Hz to the top of the sampling rate of 48.000 Hz, and sound intensity
(energy) varied from 64 to 157 dB (re SNR) (table 1).
Table 1: Acoustic parameters from the platform operation noise, (n=40), in the study
area, recorded between 2007 and 2009. (* dB re SNR was the intensity reference
provided the software Raven 3.1).
Year
Minimum
Maximum
Central
Amplitude Energy
2007-
Frequency Frequency Frequency (Hz)
2009
(Hz)
(Hz)
(Hz)
Minimum
5
1009
23,4
1009
64
Maximum 5411
48000
6029
48000
157
Mean
415,3
19031
1710
17863
102
Standard
427
7948
5743
9476
9,3
(dB:reSNR*)
Deviation
116
Figure 3: Low frequency anthropogenic noise (< 1kHz), from the gas platform, with
pulsed vertical lines surpassing the recording limit of 48 kHz.
Figure 4: Continuous anthropogenic noise during gas platform perforation process,
with larger energy up to 15 kHz and horizontal harmonic bands, wave shaped,
surpassing the limit of 47 kHz.
117
Figure 5: Anthropogenic noise from a gas platform, concentrated in frequencies lower
than 8 kHz.
Figure 6: Anthropogenic noise indirect from the platform, formed by a pulsed and
“metallic” sound, with frequencies between 1 and 12 kHz.
118
3.3) Platform and humpback whale simultaneous sound files
In 10 recording sessions were possible to detect simultaneous sounds of
humpback whales during the emission of platform noise (figures 7, 8). Sixteen whale
sounds elements, also called notes, were identified and described, as part of the
complex humpback whale song ( table 2).
Table 2: Notes of the humpback whale (Megaptera novaeangliae) song (n=65)
recorded around oil platforms, off Brazilian Coast.
Minimum
Maximum
Central
Frequency
Time
Maximum
Frequency
Frequency
Frequency
Amplitude
Amplitude
Power
min
40
262
140
64
0.37
57
max
1092
10186
2584
10032
5.13
149
mean
220
3277
483
3057
1.82
92
* Frequency parameters in Hertz (Hz), time in seconds (s), Power/sound intensity in
Decibels (dB re SNR).
119
Figure 7: Anthropogenic noise from the gas platform expressed in a wave pattern,
simultaneous to the low frequency humpback whale notes (> 1 kHz). (red rectangle is
noise range and blue rectangle is a whale song part).
Figure 8: Anthropogenic noise from the gas platform, showing an horizontal pattern,
simultaneous to the low frequency humpback whale notes (> 1 kHz). (red rectangle is
noise range and blue rectangle is a whale song part).
120
Figure 9: Comparison between anthropogenic noises (red points) and humpback
whale (Megaptera novaeangliae) (blue points) acoustic parameters: A- frequency in
121
Hz (mean values from tables 1 and 2 to minimum, central and maximum
frequencies), B- Amplitude in Hz (Minimum, Mean and Maximum), C- Energy (sound
intensity) in dB re SNR (Minimum, Mean and Maximum).
Noise overlapping whale song can be attested in figure 9A, which compares
anthropogenic noises and humpback whale frequency parameters (mean values
from tables 1 and 2 to minimum, central and maximum frequencies). It is notable that
the noise frequency parameters are always in larger mean values than the whale
sounds (figure 9), implying that their frequencies would be masked by a broader
signal (the noise, in this case), in a progressive increase according to the noise
source.
4) DISCUSSION
According to previous studies (eg. Richardson et al., 1995; Wrigth et al.,
2007), the consequences of animal exposure to anthropogenic noise are evident and
generally bring into consideration the management of human activities that may
affect animal populations in the wild.
In terrestrial animals, such as songbirds, there is an increase of investigation
on the characteristics of sound production in anthropogenic areas (eg. Nemeth et al.,
2012), such the discovery that urban great tits (Parus major) sing with higher
minimum frequencies in cities (Slabberkoorn & den Boer-Visser, 2006) and in traffic
noise in particular (Slabberkoorn & Peet).
Excessive noise can mask important aspects of communication among
several aquatic species, (eg. Richardson et al., 1995; Southall et al., 2001; Hatch &
122
Wrigth, 2007), such as sexual and contact calls that enable individuals to meet and
mate; feeding calls that facilitate food resource utilization; and mother and calf calls
that enable maintenance of proximity). Thus, the potential of noise to impair survival,
reproduction and population growth demands attention (NRC, 2000; 2003).
The context of noise sources is important because it affect the cetacean
behavioral and even physiological responses. So on, young animals may be
particularly more sensitive to the acoustic stress for many reasons such as their brain
high sensitiveness under development and, therefore, short expositions to noise
sources may result in long-term consequences (Wrigth et al., 2007).
Despite the anthropogenic noise in the marine environment is being
considered a hot topic in the scientific community (eg. Hatch & Wright, 2007), the
majority of the published information is related to humpback whale behavioral
responses to whale-watching (tourism) industry worldwide, reporting on whale
avoidance or displacement way from a noise boat source (eg. Au & Green 2000;
Miller et al, 2000; Frankel & Clark 2002, Erbe 2003, Sousa-Lima & Clark (2009).
Furthermore, some results on active low frequency sonar exposure to
humpback whales, comparing their song duration before and after to sonar exposure,
showed that six animals produced shorter songs during the noise exposure (Miller et
al., 2000).
The results of the present work show that the operation of oil and gas
platforms in Brazil produce a broad spectrum of acoustic noise, reaching the extreme
limits of our recording equipment (0 to 48 kHz), suggesting the future utilization of a
broader frequency range gear.
Sound intensity of the platform noise, registered as “Energy” varied between
100 and 150 dB (re SNR), and are concentrated in low and medium frequencies (0 to
123
10 kHz), which is also a large part of the acoustic niche of the humpback whale.
Therefore, it was evident a frequency and sound intensity overlapping between the
humpback whale song and the anthropogenic noise. Increased sound intensity and
low frequency components allow noise to propagate farer in the ocean.
The observed behavior and group structure around the platforms clearly
indicate that humpback whales are utilizing anthropogenic environments inside their
whole breeding area in the Brazilian coast, exposing them to diverse sources of
human-made impacts (Neto et al., 2007; Marcondes & Engel, 2009; Rossi-Santos et
al., 2010).
The actual literature about the hearing capabilities of the humpback whale is
still inconclusive. Au et al., (2006) report sound intensity/energy values for the
species recorded in Hawaiian Waters between 151 and 173 db (re 1 µPa) and high
frequency harmonics surpassing 24 kHz, suggesting that the species may present an
upper hearing limit as high or even higher this value.
Scarce information about noise from oil and gas platforms is reported in the
literature. The present work fill this gap and show that the frequency variation overlap
in almost all analyzed spectrum and that the noise intensity may be stronger than
biological song intensity, which may allow to the sound masking, as largely
commented in previous studies (eg. Richardson et al., 1995; Foote et al., 2004;
Wright et al., 2007) and, in a last instance, causing a disturbance in the whale
breeding success around the noise source location, which may lead to the search for
quieter areas, decreasing the natural size of their seasonal breeding area
The results of the present work show that oil and gas platforms contribute to
the oceanic ensonification, by producing a broad noise spectrum, varying in all the
124
measured acoustic range (0 to 48 kHz), which may suggest the future use of a
broader recording system.
Sound intensity of platform noise, registered in the energy parameter, varied
from 100 to 150 dB (re SNR), and are concentrated in lower and mean frequencies
(0 a 10 kHz), which is a large part of the humpback whale acoustic niche. Thus a
frequency and energy overlapping between the humpback whale song and the
anthropogenic noise originated from the Oil Industry in the Brazilian breeding ground
was evidenced.
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134
Artigo 4 – Efeitos dos ruídos produzidos pelo turismo de observação no
comportamento da baleia jubarte (Megaptera novaeangliae) na área de
reprodução da costa do Brasil.
Marcos R. Rossi-Santos 1,2
1-
2-
BIODIVERSITY AND CONSERVATION (A2, fator de impacto 2,146)
A ser submetido
135
RESUMO
O turismo para observação de cetáceos (Whale watching) é uma das atividades que
mais cresce no mundo, grandemente devido ao carisma que estas espécies
exercem sobre o homem e também devido ao crescente apelo de conservacionistas
de todo o mundo que enxergam nesta atividade um poderoso argumento para que a
caça de baleias não seja retomada. Entretanto, se esta atividade não é feita de
maneira sustentável pode acarretar danos para as populações de cetáceos, que vão
desde alterações comportamentais a, até mesmo, danos fisiológicos. Dentro de um
estudo de longo prazo sobre a ecologia acústica da baleia jubarte (Megaptera
novaeangliae) na região nordeste do Brasil, dados comportamentais e acústicos
sobre a aproximação de embarcações durante a época de reprodução da jubarte
foram analisados para a localidade de Praia do Forte, tradicional centro do turismo
de observação. Medições de freqüência e intensidade sonora indicaram que a
atividade pode causar potenciais impactos no comportamento de superfície, bem
como acústico desta espécie. Implicações para a conservação da baleia jubarte e
seu ambiente são discutidas.
Palavras-chave: Turismo de Observação, Whale Watching, Baleia jubarte,
Megaptera novaeangliae, impactos acústicos, costa do Brasil
136
Whale-watching noise effects on the behavior of humpback whales (Megaptera
novaeangliae) in the Brazilian breeding ground.
ABSTRACT
Whale-watching tourism is increasingly growing in the world, mostly due to the
charisma that cetacean exert on humans, as well as due to the constant
conservationist appeal that shows a strong argument to the no return of the
commercial whaling. Nonetheless, if this activity is not sustainable may harm
cetacean populations, from behavioral changes to physiological injuries. In a long
term study about the acoustic ecology of the humpback whale (Megaptera
novaeangliae), in their breeding ground off northeastern Brazil, behavioral and
acoustic data were collected during whale watching boat approach in Praia do Forte,
a touristic traditional center. Frequency and sound energy measurements indicated
potential impacts in the surface and underwater behavior of the humpbacks.
Implications for the species as well the environment conservation are discussed.
Key-words: Tourism, Whale Watching, Humpback whale, Megaptera novaeangliae,
acoustic impacts, Brazil
137
1) INTRODUCTION
The whale-watching tourism is being for a long time considered as a great
allied in propagate conservation through experiencing whales in their natural habitat,
instead to use these animals in other lethal way such as whaling for sub-products, as
oil and even whale meat (see Hoyt, 2001). It seems that whale-watching is a growing
industry, bringing millions of dollars per year worldwide and spreading conservation
everywhere in the globe (Hoyt, 2001; IWC, 2008).
In South America, whale-watching began in the early 1980´s in the
Argentinean Patagonia (Hoyt 2001), where the southern right whales (Eubalaena
australis) go every year to breed in the shore, allied to the same coastal and calm
behavior that made this species easy to hunt, as the main target for whaling in the
past.
In Brazil, this activity was initiated in the 1990´s, simultaneously in the South,
in Santa Catarina state, where the same right whales also come for breeding in the
austral winter and spring (July to November) (Palazzo et al., 1994), and in the
Northeastern, in Bahia state, where humpback whales (Megaptera novaeangliae)
elected the shallow waters of the Abrolhos Bank to search for mates and give birth
and care of their young (Engel, 1996, Morete et al., 2008).
In the late 1990’s, as a result of the conservation efforts worldwide, the
humpback whale populations, have showed an increase in their numbers (Ward,
2006, Zerbini et al., 2006, Andriolo et al., 2006) and the past range, before the
whaling period, have being re-colonized, stated by constant observations and
systematic research (eg. Rossi-Santos et al., 2008, Wedekin et al.2010).
In this scenario, Praia do Forte became a strong whale-watching destination,
mainly because its proximity to the capital Salvador (55 Km), one of the most touristic
138
places in Brazil and by the very coastal occurrence of the whales, mainly due to the
narrow continental shelf (Rossi-Santos et al., 2008; Wedekin et al., 2010; BarachoNeto et al., 2012).
Together with the conservation purposes, whale watching industry is seen with
concern about the possible negative influences in the whale behavior and distribution
(eg. Simmonds 2003). This paper aims to describe the underwater noise originated
from whale-watching in Praia do Forte and to evaluate the possibility of masking
effect of the humpback whale song display.
2.1) Study area
This work was conducted in Praia do Forte (13° S, 38° W) (figure 1), where the
whale watching tourism is established since 2000 (Cipolotti et al., 2005). In the
region, this activity is, in part, favored by the large number of national and
international tourists who visited the place, clamored by the media as the “Brazilian
Polynesia”, due to the landscape including coastal coral reefs and sand beaches,
with tradition on coconut agriculture, composing the paradisiacal tropical scenario.
139
Figure 1 – Study site of whale watching effects on the humpback whale (Megaptera
novaeangliae) behavior at Praia do Forte, Bahia state, Northeastern Brazil, with
reference to tha capital, Salvador, at 55 Km south. The Abrolhos Bank, the core area
of humpback whale distribution in Brazil, is located about 300 Km south.
2.2) Whale watching operation
Three main operators conducted this activity, utilizing wooden made boats,
known as schooner, and fast boats, such as a 12 meters inflatable boat equipped
with a 250 Hp offboard engine (figure 2). Less frequently, there was a forth operator,
from the Praia do Forte Ecoresort, who performed whale watching using a fiberglass
fast boat with outboard engine of 200 Hp.
2.3) Visual and acoustic surveys
140
As part of a broad study about the acoustic ecology of the humpback whales
the region, data on whale watching boats approaching whales were visually and
acoustically during the breeding season (July to October), from 2005 to 2010.
A team of 3 to 5 observed was engaged into monitor whale watching boats,
registering distance and whale behavioral data, while another observer was
acoustically recording these events. Distance measurements from the research boat
to observed whales and whale watching boats were collected using a Bushnell Elite
1500 laser range-finder.
For the acoustic recordings it was utilized an system consisting of a CR 54
hydrophone connected to a digital recorder (M-Audio Microtrack Pro-II), with
frequency response up to 96 kHz. Spectrographic analyzes were performed utilizing
the software RAVEN 3.1 (Cornell University). As it was an uncalibrated system, for
the measurements on sound energy, signal to noise ratio was used as reference for
decibels (dB re SNR).
3) RESULTS
During the acoustic study of humpback whales in Brazil, 640 minutes of
sampling effort were extracted from 16 encounters with whale watching boats closely
monitored, since the first sighting of the boat towards whale groups until they going
away to observe some time after approach. Four boats of different types were
identified (figure 2), with their noise registered from diverse sources, such as
schooners and fast boats (summary in table 1).
We noted that the boat operators usually take care on the limits imposed by
the Federal Legislation (maximum approach of 100 meters away from the whale and
141
permanence time no longer than 30 minutes with each group. Despite this, engine
conditions and sudden departure from whale groups resulted in initial behavioral
disturbance of the animals.
Table 1: summary of data containing the description of whale-watching boats
operating in Praia do Forte, Bahia state, during 2009 (name, body type, engine
power (Hp), passenger capacity) and acoustic recording effort, in minutes.
Name
Body Type
Engine
Capacity
Recording
Power (Hp)
(persons)
effort (min.)
Mãe Dalva
Wood schooner
180
50
9
Cannes
Wood schooner
250
100
20
Bahia Adv
Inflatable
250
12
5
200
8
5
(fiberglass rigidbottom) boat
Angélica
Fiberglass fast
boat
142
Figure 2 – Examples of different boat types (such as schooners and fast boats)
registered in the whale watching operation for humpback whales (Megaptera
novaeangliae) in Praia do Forte, Bahia state, Brazilian breeding ground.
Noise range
Noise range was widely registered since infra (lower than 20 Hz) to ultra
(higher than 20000 Hz) sonic bands, mainly concentrated up to 15000 Hz, with sound
energy varying from 60 to 130 dB re SNR for both the schooners (figures 3, 4) and
fast boats (figure 5). This frequency range in also included in the acoustic niche of
the humpback whale and indicate the potential of masking on some song
components.
Behavioral Observations:
Important behavioral observations were obtained on whale movement and
reactions during whale watching approach. In Jul, 19, 2009, from 10:50 to 11:50 am
143
(60 minutes), we observed a group of 4 humpbacks at 50m deep. Before the
approach of the boat Mãe D'Alva whales performed 5 breachings while moving in an
erratic direction. Then, the boat Mãe D'Alva approached and it was recorded for 7
minutes. During this time, distance from the research boat was measured (228m – 30
sec; 180m - 1:30min; 69m - 3:10min) (figure 3). When the boat was at 69 m from the
whales, they disengaged in two couples and start to move away from the boat.
144
Figure 3 – Spectrogram showing the noise from the whale watching boat Mãe Dalva
(red retangles) approaching humpback whales (song parts represented inside the
blue retangles) in Praia do Forte, Bahia state, in the year 2009. (distance from the
145
research boat: 228m – 30 sec; 180m - 1:30min; 69m - 3:10min). Note that boat noise
starts overlapping the whale song and gradually, when it decrease speed and
consequently sound intensity, the song starts to be clearer.
In Jul, 21, 2009, from 14:00 to 14:55 am (55 minutes), we followed a solitary
individual, confirmed as a singer male through acoustic recordings, where more than
one animal was listened. After 20 minutes we sighted the schooner Cannes
approaching in the whale direction. Informing the Cannes captain by VHF radio about
our acoustic monitoring, we could obtain a controlled approach from the whale
watching boat, and as the boat come closer to the whale, the captain kept informing
by radio the engine rotation (RPM), while we measure its distance from the
hydrophone. The singer male stop singing after the approach and start to perform
fluke exhibition, diving and moving away from our view. The schooner Cannes tried
to follow this individual and we still could listen to its noise until more than 1 nautical
mile. In this context, we identified at the spectrogram the frequency range of the
noise (up to 8 kHz) and sound intensity (112 dB re SNR) in this event. Engine
rotation during boat displacement was 3000 RPM with distances varying from 44 to
208 meters to the research boat (figure 4).
146
Figure 4 – Spectrogram showing the noise evolution in time, from the whale watching
boat Cannes, operating in Praia do Forte, Bahia state, Brazilian breeding ground for
the humpback whale, Megaptera novaeangliae (engine rotation was 3000 RMP;
147
distance from the research boat: 44m - 1:30min; 69m - 1:34min; 170m - 2:10min;
208m - 2:23min).
The Bahia Adv fast boat approached the research boat, which was observing
a humpback whale group of 3 adult animals, reducing speed while coming closer,
then distance was registered while underwater recording, and a fast displacement
potential with noise staying for longer was noted: 34m - 1:30min; 69m - 1:40min;
172m - 1:50min; 321m - 2:00min; 580m - 2:10min.
Figure 5 – Spectrogram showing the noise evolution in time, from the whale watching
fast boat Bahia Adv, operating in Praia do Forte, Bahia state, Brazilian breeding
ground for the humpback whale, Megaptera novaeangliae (distance from the
research boat: 34m - 1:30min; 69m - 1:40min; 172m - 1:50min; 321m - 2:00min;
580m - 2:10min).
148
DISCUSSION
Our findings suggest that whale-watching operation produces a similar range
of noise than the biological song of the humpback whale (for details, see article 1)
and may result in masking of this important breeding display, during boat approach.
Given that marine mammals depend on the acoustic sensory channel for
many of their activities, forcing an animal to modify its vocal behavior or reducing its
hearing capability could reduce its ability to search for food, to navigate, or to contact
conspecifics (Richardson et al., 1995).
The effects of boat traffic on marine mammals in coastal areas are a topic of
growing concern. Most of the studies addressing this problem have used behavioral
attributes such as changes in site tenacity, dive patterns, swimming speed,
orientation of travel, group cohesion and dive synchrony to indicate possible
disturbance or stress caused by boat traffic (Richardson et al., 1995, Simmonds,
2003).
For some examples, in the Arctic, Belugas (Delphinapterus leucas) exposed to
a large ship and an icebreaker remained vocal and emitted a large proportion of
falling tonal and noisy pulsed calls, thought to be alarm calls, while narwhals
(Monodon monoceros) became silent when exposed to the same noise source
(Finley et al., 1990). Gray whales (Eschrichtius robustus) along the Mexican coast
reacted differently to outboard motor and drillship noise; their call rate increased in
the first case and decreased in the latter (Dahlheim 1987).
This variability in reactions could be due to a number of different physical and
biological factors, including noise characteristics and levels at whale locations, the
duration and predictability of the disturbance and, in the case of boats, the distance,
149
number, type, speed, and angle of approach. Biological factors would include the
hearing capability of the animals, their behavior, threshold of disturbance, degree of
habituation, and need to remain in the area (Watkins 1986, Richardson et al., 1995,
Simmonds, 2003). Foote et al (2000) showed that whale watching boats can mask in
the killer whale (Orcinus orca) influencing their surface and calling behavior.
Important findings are reported by Erbe (2002) on the effects of whale
watching boats in the killer whale acoustic behavior. By special modeling, it was
found that noise of fast boats may be audible to killer whales over I6 km, may mask
killer whale calls over 14 km, and may elicit a behavioral response over 200 m,
causing a temporary threshold shift (TTS) in hearing of 5 dB after 30-50 min within
450 m. For boats cruising at slow speeds, the predicted ranges were 1 km for
audibility and masking, 50 m for behavioral responses, and 20 m for TTS.
In Newfoundland and Labrador, Canada, a code of conduct was established to
minimize impacts from the whale watching operation on humpback whales, however
few operators (25%) have followed it strictly (Corbelli, 2006). This same work also
report negative behavioral response from the humpbacks, which avoided boats
changing their dive patterns and increasing other surface behaviors such as
trumpeting and tail slapping. Compliance with the code was found to have only little
effects, reducing these behavioral surface response.(Corbelli, 2006)
In the Brazilian breeding ground, previous investigations found a negative boat
effect in the humpback behavior of the Abrolhos Bank, which reflected in the singer
male displacement, stop singing and both factors concurrently (Sousa-Lima et al.,
2002; Sousa-Lima & Clark, 2008).
Whale-watching is a growing industry in the world (Hoyt, 2001), and Brazil is
being an increasing visited destination. During 2001-2009, 522 whale watching
150
cruises left from Praia do Forte to provide sensitization experience for 14.343 tourists
(Sousa-Lima et al., 2002; Sousa-Lima & Clark, 2009). (Cipolotti et al., 2005; Instituto
Baleia Jubarte, Unpubl. Data).
Brazilian legislation has a specific law to regulate whale watching (IBAMA 117/
96), limiting boat approach to 100 meters and time of permanence with whales in 30
minutes. Engines should be kept in neutral position during observations, then
stroking when the whale is sighted at more than 50 meters from the boat. The law
also says that is prohibited to produce excessive noise closer than 300 meters from
any cetacean species.
Meanwhile, today we know that 300 meters for a whale perceive sounds is
quite close, once they can hear across ocean basins (revised in Clark & Altmann,
2006). The presented results also support this affirmation, once boat noise, was
registered more than a nautical mile away from the hydrophone. A proper legislation
about acoustic disturbance should complement the present, including specification
about underwater noise levels and frequency range.
Furthermore, acoustic monitoring should be included in all aspects involving
marine enterprises and potential risks to marine life. Despite a growing interest in
acoustic technology around the world, in South America, especially in Brazil, is
necessary to improve the available acoustic equipments and scientific methods
which make it an ideal research tool for the future, by its large scale range, saving
time and costs to researchers.
Some practices also could be adopted by customers and companies aiming to
minimize noise propagation during whale watching, such as to give preference for
smaller boats, which uses smaller engines, require periodical maintenance process
to eliminate excessive noise from engines, have a specialist team always onboard,
151
which provide before during and after precise information about the animals and how
to reach them, and a careful captain which before everything is capable to observe
and perceive animal behavior.
Ideally, whale-watching should be conducted at a sustainable level,
maximizing the potential returns while minimizing the impact on the target species,
otherwise the exposure to noise from boats may result in abandonment of the area
by the species of interest, harming both the animals and the whale watching
operation (Higham & Lusseau 2007).
The International Whaling Commission initiated a cooperative study to map
whale watching impacts on cetaceans in the world (LAWE – Large Scale Whale
watching Experiment, 2008). Perhaps in the future would be possible to keep
enhancing people awareness through experiencing whales in the wild, and, at the
same time controlling disturbance in a world where noise is constant, winning respect
to the whales and their environment.
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155
5. CONSIDERAÇÕES FINAIS
5.1) Ecologia do comportamento de canto
Os grupos de baleias jubarte contendo machos cantores foram observados
durante todo o período do estudo (2005 a 2009) praticamente em toda a extensão
da área de estudo, de Itacaré/Bahia até Aracaju/Sergipe, cerca de 520 km de costa.
Dessa forma, comprova-se a extensão da distribuição de jubartes na região
Nordeste, ao norte do Banco de Abrolhos, reforçando a consideração de uma área
mais ampla de concentração reprodutiva na costa do Brasil, que vai de 10° a 20° S.
A ampla visão da paisagem marinha, parte do conceito de Ecologia Acústica
desenvolvido por Truax (1999) na qual os organismos desenvolvem suas
habilidades acústicas influenciados pelo ambiente que os cerca, colabora com a
diversidade encontrada de grupos contendo machos cantores.
Ademais, a distribuição extensa dos machos cantores na região de estudo,
demonstra a clara utilização da paisagem acústica local que, por sua vez, apresenta
influências de importantes parâmetros oceanográficos, como a plataforma
continental estreita e a consequente variação de profundidade. Fatores como o
regime de marés e fases da lua não demostraram aparente relação com a
distribuição de grupos com machos cantores na área de estudo.
Aliado a estes fatores, foi encontrada uma grande variação na estrutura de
grupos contendo machos cantores, mais complexa do que descrita anteriormente
para a mesma área de alimentação.
Dessa forma, suporta- se a hipótese 1, de que existe uma relação entre a
complexidade da estrutura de grupo no qual o macho cantor está inserido e o
156
contexto ecológico no qual este comportamento ocorre, sendo que fora da área de
concentração reprodutiva a estrutura do canto das baleias jubarte tende a se
diferenciar.
Tais diferenças também permitem avançar na discussão do sistema de
acasalamento da espécie, mais aceito como um sistema de poliginia que inclui o lek
flutuante, como proposto por (Clapham 1996). Outros autores trazem discussões
que complementam a visão de lek, sugerindo que o sistema deve ser mais complexo
do que pensado anteriormente (eg. Connor et al., 2000; Darling et al;. 2006). Os
resultados sobre as diferentes estruturas de grupos podem corroborar com essa
teoria da maior complexidade do sistema de acasalamento da baleia jubarte.
5.2) Descrição acústica do comportamento de canto
A primeira descrição do canto da baleia jubarte para a região de estudo,
demonstra que as baleias estão utilizando um amplo ambiente durante suas
atividades de reprodução, através de um amplo espectro de frequência (20 – 24,000
Hz), com maior energia entre as frequências médias de 224,4 a 4422 Hz, além da
duração bem variável de 0,13 a 6,5 segundos (média = 1,06) e intensidade sonora
de 62 a 130,4 dB (re SNR) (média = 105). Os harmônicos foram registrados em 73
% dos sinais medidos, sendo que muitos deles chegaram até o topo da resposta de
freqüência do sistema de gravação de 24 kHz.
Os valores de frequência máxima foram maiores do que os já reportados
anteriormente, podendo ser devido a uma resposta na melhor adaptação do sinal em
relação à profundidade do ambiente local que esta sendo utilizado. A ocorrência de
harmônicos de alta freqüência em área de profundidades semelhantes à nossa área
de estudo (Au et al., 2006) pode fortalecer essa interpretação.
157
A diversidade da forma dos cantos foi evidente entre duas regiões distintas na
mesma área de reprodução. O número de notas e de temas apresentou
complexidade maior no Banco de Abrolhos quando comparada à Costa Norte, assim
como o número de machos cantores registrados durante as gravações. Este
resultado suporta a hipótese 2 de que existe uma relação entre a complexidade do
canto e o contexto ecológico no qual este comportamento ocorre, sendo que fora da
área de concentração reprodutiva a estrutura do canto das baleias jubarte tende a se
diferenciar.
Aliado a este fato, a descrição do comportamento de coro, feita pela primeira vez
para a população de jubartes que freqüenta a costa do Brasil, dá forças para os
argumentos de um sistema de acasalamento mais complexo do que previamente
descrito, onde a aparente proporção sexual é igual (Cypriano-Souza et al., 2010),
assim como a fidelidade de área há longo prazo (Baracho-Neto et al., 2012)
resultando em maior mobilidade tanto de fêmeas como de machos da população e,
assim, desencadeando os processos formadores para o acasalamento sem levar em
conta somente a teoria de sucesso reprodutivo por “hotspot” ou por machos
“hotshot” (Krebs & Davies, 1993) e compondo, dessa forma, um sistema de
acasalamento que possa atuar com um maior dinamismo que requer uma espécie
de grande tamanho e grande movimentações periódicas, como a baleia jubarte.
5.3) Descrição acústica dos ruídos antropogênicos
Os resultados de dois artigos do presente trabalho (artigos 3 e 4) suportam a
hipótese 3 sobre a existência da sobreposição de nicho acústico, onde ruídos
158
provocados por atividades humanas causam interferências no comportamento das
baleias jubarte
No artigo 3 foi apresentado que as plataformas de óleo e gás produzem um
amplo espectro de ruídos acústicos, variando em toda a capacidade de nosso
sistema de gravação (0 a 48 kHz), sugerindo o uso futuro de um equipamento de
registro mais amplo de frequências.
A intensidade sonora dos ruídos de plataformas, registrada no parâmetro
“Energia”, variou entre 100 e 150 dB (re SNR), e estão concentradas em frequências
baixas e médias (0 a 10 kHz), as quais compõe grande parte do nicho acústico da
baleia jubarte.
De forma semelhante, constatou-se que o turismo de observação de baleias,
apesar de ser uma valorosa ferramenta para a conservação de muitas espécies de
cetáceos, pode produzir um amplo espectro de ruídos acústicos, cujas energias
centrais estão no mesmo nicho acústico utilizado pelas jubartes.
Desta forma, foi confirmada a sobreposição dos sons biológicos das baleias
quando as mesmas se aproximam destas fontes de ruídos antropogênicos
localizadas em sua área de reprodução.
159
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167
Anexo 1 - Natural Observation and Integration under the Goethean method:
New possibilities to the humpback whale song understanding
“If we want to attain a living understanding of nature, we must become as flexible
and mobile as nature herself”.
Johan Wolfang von Goethe
PREFACE
During my behavioral studies on whale songs, I have feeling the need of new
approaches to integrate a different nature conception to my inquisitive curiosity about
cetacean lives. Following this wish, I bring a brief reflection on another scientific
method I have recently known, and which I think may contribute to a next broader
step in the natural science.
Modern biology has increasingly moved out of nature and into the laboratory,
driven by a desire to find an underlying mechanistic basis of life. Despite all its
success, this approach is one-sided and urgently calls for a counterbalancing
movement toward nature (Skaftnesmo, 2009.) Only if we find ways of transforming
our propensity to reduce the world to parts and mechanisms, will we be able to see,
value, and protect the integrity of nature and the interconnectedness of all things.
This demands a new way of seeing.
168
THE GOETHEAN SCIENCE
Johann
Wolfgang
von
Goethe
(1749
—
1832)
developed
the
phenomenological method for scientific research a hundred years before
phenomenology was introduced as a philosophic discipline. (Skaftnesmo, 2009).
Most people know Goethe for his poetry, but he researched many areas of science,
like zoology, botany, meteorology and geology, optics and color. Today his methods
are naturally given more attention than his results. And that attention is increasing
(Skaftnesmo, 2009).
Instead of the dualist vision in which man, as observer and thinking subject
confronting nature only trough the cognitive effort from intellect, Goethe adopts that
man is part of the nature and nature is part of man. Through his approach, the
organism
teaches
us
about
itself,
revealing
its
characteristics
and
its
interconnectedness with the natural world that sustains it. This manner of doing
science enhances our sense of responsibility for nature.
In this way, Goethe’s vision is directly associated to phenomenology, which
designs theoretical concepts from the simple phenomenon itself, and not following a
forged and unperceptive reality beyond these concepts (Brady, 1998). The emphasis
here it is in the scientific capacity of perception and in the importance of sensorial
phenomena as a confident source of information, and as the observer gets more
experienced, he becomes the best research instrument (Hensel, 1998).
The use of equipments and instruments would not replace the personal
observation. For Goethe, this substitution would lead only to accumulate information,
but not conduct to the understanding of the phenomenon neither in any form of
169
interact with it. Following the experience, the investigative search would be for the
idea properly, or the basics of nature, in which the diversity of experiences expand in
the sensorial world.
Considering the phenomenological vision, the scientific research turns into a
process which is deeply dependent of the personal ability to observe patterns, forms
and archetypes within the multiplicity of nature (Zajonc, 2005). Goethe also assume
that this fact bring a larger responsibility to the scientist, as well as the opportunity to
self-knowing along the scientific process (Goethe 1988).
The questions of causality (cause and effect) do not invite us to dive down into
the qualities of the humpback whale song. Here the song is a part of the integral
scene. But Goethe’s path of inquiry is a science in which the questions what and how
come first (Head, 2005). The path to understand a phenomenon – who are you,
whale? – begins with the question: How are you expressing yourself? How is your
way of being? If we start with that question, we have to let the phenomena work into
us.
We need a science of nature that takes seriously the qualities of nature and
approach it as a whole. Goethe’s science is a deep ecological method that indicates
the next step science must take if life on earth is to survive: To begin to know the
inherent qualities of what we manipulate, preferably before we fire off our “gene
guns”:
So on, two centuries in front of his time, Goethe recalled about the urgency of
joining the human being and the natural world throughout the integral experience and
understanding. Based on Goethe´s method, perhaps we could develop ways of
170
thinking and perception that integrate self-reflective and critical thought, imagination,
and careful, detailed observation of the phenomena.
This vision will not replace the conventional scientific method, but it will allow
observing phenomena through a different point of view. Considering totality, we can
perceive intrinsically subtle relations inside a system and include ourselves as part of
it.
Environmental activities, where man interacts with the natural world, require
this skill to recover and preserve nature. In this context, the Ocean is open to this
approach and perhaps in a near future, developing a vision of an integrative
understanding of the Ocean, we will find in the humpback whale song a key to last a
long time with respect to this planet. Should not be by chance that the humpback
whale exert for a long time a fascination even in experienced scientists who
described it as the most spectacular display in the whole animal kingdom (Wilson
1975).
Rudolf Steiner (1985), based on Goethe studies says, that if the observer
reach to know the inherent principles manifested in the natural phenomena, it may
create forms with a inherent consistency. The result may not to be naturalism, as a
nature copy, but instead would be an expression of the formative principles that act in
nature (Riegner & Wilkes, 1998). If these activities are conducted within a conception
of totality, they belong to this totality and then serve perfectly to the human being and
to the environment it inhabits.
171
REFERENCES
Bortoft, H. 1996. The Wholeness of Nature: Goethe’s Way Toward a Science of
Conscious Participation in Nature. Hudson, NY: Lindisfarne Press.
Brady, R. H. 1998. The Idea in Nature: Rereading Goethe’s Organics. In Goethe’s
Way of Science: A Phenomenology of Nature, Albany: State University of New York
Press.
Goethe, J. 1988. Scientific Studies. Princeton: Princeton University Press.
Head, J. 2005. Doing Goethean Science. Trivium Publications, Amherst, MA. The
Nature Institute. 8 (1), 27-52.
Hensel, H. 1998. Goethe, Science, and Sensory Experience, In Goethe’s Way of
Science. A Phenomenology of Nature, Albany: State University of New York Press.
Riegner, M & Wilkes, J. 1998. Flowforms and the Language of Water. In Goethe’s
Way of Science: A Phenomenology of Nature, Albany: State University of New York
Press.
Skaftnesmo, T. 2009. Goethe’s Phenomenology of Nature: A Juvenilization of
Science. Rivista di Biologia / Biology Forum, 102, 169-198.
Steiner, R. 1985. Goethe’s World View. Spring Valley, NY: Mercury Press.
Wilson, E. O. 1975. Sociobiology: The New Synthesis. Cambridge, Mass.: Harvard
University Press.
172
Zajonc, A. 2005. Goethe and the Science of His Time: An Historical Introduction. In
Goethe’s Way of Science: A Phenomenology of Nature, Albany: State University of
New York Press.
173

Grande parte das interações entre os animais envolve algum tipo de

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