universidade federal do rio grande do norte centro de

Transcription

UNIVERSIDADE FEDERAL DO RIO GRANDE DO NORTE
CENTRO DE BIOCIÊNCIAS
PROGRAMA DE PÓS GRADUAÇÃO EM PSICOBIOLOGIA
JULIA RIBEIRO GUIMARÃES DOMBROSKI
ECOLOGIA ACÚSTICA DE PARES FÊMEA-FILHOTE DE BALEIA FRANCA
AUSTRAL (Eubalaena australis) (Desmoulins, 1822) EM ÁGUAS COSTEIRAS
DO ESTADO DE SANTA CATARINA, BRASIL
Dissertação apresentada à Universidade
Federal do Rio Grande do Norte para
obtenção do título de Mestre em
Psicobiologia.
Natal
2015
JULIA RIBEIRO GUIMARÃES DOMBROSKI
ECOLOGIA ACÚSTICA DE PARES FÊMEA-FILHOTE DE BALEIA FRANCA
AUSTRAL (Eubalaena australis) (Desmoulins, 1822) EM ÁGUAS COSTEIRAS
DO ESTADO DE SANTA CATARINA, BRASIL
Dissertação apresentada à Universidade
Federal do Rio Grande do Norte para
obtenção do título de Mestre em
Psicobiologia.
Orientadora: Dra Renata S. Sousa-Lima
Co-Orientadora: Dra Susan E. Parks
Natal
2015
Catalogação da Publicação na Fonte. UFRN / Biblioteca Setorial do Centro de Biociências
Dombroski, Julia Ribeiro Guimarães.
Ecologia acústica de pares fêmea-filhote de baleia franca austral (Eubalaena australis) (Desmoulins,
1822) em águas costeiras do estado de Santa Catarina, Brasil. / Julia Ribeiro Guimarães Dombroski. –
Natal, RN, 2015.
99 f.: il.
Orientadora: Profa. Dra. Renata S. Sousa-Lima.
Coorientadora: Profa. Dra. Susan E. Parks.
Dissertação (Mestrado) – Universidade Federal do Rio Grande do Norte. Centro de Biociências.
Programa de Pós-Graduação em Psicobiologia.
1. Ecologia comportamental. – Dissertação. 2. Comportamento vocal. – Dissertação. 3. Repertório
acústico. – Dissertação. I. Sousa-Lima, Renata S. II. Parks, Susan E. III. Universidade Federal do Rio
Grande do Norte. IV. Título.
RN/UF/BSE-CB
CDU 574
Título: Ecologia acústica de pares fêmea-filhote de baleia franca austral (Eubalaena
australis) (Desmoulins, 1822) em águas costeiras do estado de Santa Catarina, Brasil
Autor: Julia Ribeiro Guimarães Dombroski
Data da defesa: 27 de maio de 2015.
Banca Examinadora:
__________________________________________________
Prof. Dr. Artur Andriolo,
Universidade Federal de Juiz de Fora, MG
__________________________________________________
Profa. Dra. Maria Luisa da Silva
Universidade Federal do Pará, PA
__________________________________________________
Profa. Dra. Renata S. Sousa-Lima
Universidade Federal do Rio Grande do Norte, RN
__________________________________________________
Profa. Dra. Susan E. Parks
Syracuse University, NY
“Se você quiser ver uma baleia,
vai precisar de uma janela
e um oceano.
Vai precisar saber
para onde não olhar:
rosas cor-de-rosa,
pelicanos,
possíveis piratas.
Se você quiser ver uma baleia
vai precisar manter os olhos no mar
e esperar
esperar
esperar”
Julie Fogliano
Dedico este trabalho ás vozes que embalam meu coração:
minha amada família,
as águas do mar
as majestosas baleias.
Agradecimentos
Incrível, como este momento tão almejado, se tornou realidade num piscar de
olhos. A entrega desta dissertação não representa o fim, mas o início da concretização de
sonhos que vem sendo, pouco a pouco, transformados em realidade. São muitas as
pessoas direta ou indiretamente envolvidas neste processo e a cada uma delas eu digo
emocionada: muito obrigada!
Não tenho palavras para expressar minha profunda gratidão, admiração e paixão
pela minha família. Cada um de vocês faz de mim uma pessoa melhor a cada dia e meus
olhos se enchem de lacrimas quando penso na felicidade que vocês me proporcionam, dia
após dia, não importando o quão próximos ou distantes estamos. Mãe, você é minha alma
gêmea e sem você eu seria a pessoa mais solitária neste mundo. Lu, sem sua presença o
riso em nossa casa seria menos espontâneo e as manifestações de pura elegância e
delicadeza também. Pai, nesta mesma época, a um ano atrás, não sabia se você ainda
estaria presente hoje, conosco. O que posso fazer para agradecer sua força e coragem, e
simplesmente o fato de estares aqui, é dar-lhe de presente de aniversário uma filha mestre.
Vó, és o meu xodó mais querido, meu grande amor. Dinda, sempre amiga e companheira,
obrigada por todo carinho. Estar distante de vocês é um enorme desafio, maior do que
qualquer baleia azul.
Obrigada a todos os amigos, espalhados pelo Brasil a fora, que me acompanham
na trajetória da pesquisa de mamíferos aquáticos: Rodrigo, Israel, Gabriel boto, Angélica,
Louzinha, Diogo, Rihel, Ju Moron, Diogo Barcellos, Mia. Encontrei vocês em momentos
tão diferentes, mas de um jeito ou de outro vocês me deram forças para seguir para a etapa
seguinte deste caminho. Dani Abras, será que é coisa de vidas passadas? Talvez. Obrigada
pela paciência, pelo apoio, por compartilhar felicidades e desencantos, por ser um
exemplo de disposição e determinação e por ter existido em minha vida desde sempre,
desde aquele fatídico encontro em Puerto Mádrin. Ana, a você também agradeço pela
paciência e pelas recepções mais do que carinhosas a cada visita antes das inúmeras
partidas. Me sinto segura na tua presença, mesmo que esta presença não seja física em
todos os momentos. Preciso saber que você está por alí, e isso me dá forças. Digão,
obrigada por trocar mensagens comigo enquanto ninguém acordou ainda, pelos
momentos “chorar as pitangas”, pelas risadas e pelo imenso apresso e admiração que você
provoca em mim, com toda a sua gentileza e determinação.
Dudu a vida em Natal teria sido tão sem graça sem nossos incontáveis kebabs.
Dani encontrei em ti um irmão mais velho. Um tanto excêntrico é verdade, mas nossas
peculiaridades nos fazem adoráveis (e modestos). Carol, o que dizer... Como duas pessoas
tão diferentes podem se dar tão bem? Obrigada por ter saído da terrinha e ter vindo ser
parte vital da minha vida. Dividimos risadas, muitas risadas, lacrimas de tristeza, alegria,
desespero. Partilhamos casas, palavras, olhares, pensamentos (aliás, telepatia é o nosso
forte). Obrigada por fazer companhia a minha quietude e por me aceitar como eu sou.
Isadora, minha irmã de outra mãe. Que saudade e que orgulho de ti. Não tem como
explicar a falta que você tem feito. Você é minha versão melhorada e desbocada. Te amo
muito muito e conto os dias para poder fazer cafés da manhã e tê-la de volta para falarmos
sem parar durantes horas e horas a fio.
Queridos amigos do LaB: Deby, Paulinha, Lu, Thamires, Marcos, obrigada pelos
momentos educativos, pelas risadas e por estarem presentes no meu dia a dia, tornandoo mais alegre. Laura, que nossa amizade continue a crescer dentro e fora da profissão.
Narinha, que o brilho do seu sorriso continue iluminando os meus dias mais confusos.
Dani (Polari), depois de tudo o que passamos juntos fica até difícil colocar em palavras
minha infinita consideração por você. Um amigo de verdade que me fez companhia nos
dias solitários de LaB, para as pizzadas de quinta à noite, gargalhadas altas demais e muito
mais. Desde o dia que nos falamos pela primeira vez pelo Facebook, achei que já nos
conhecíamos de algum lugar. Eram tantas pessoas e vivencias em comum! Temos muito
trabalho pela frente e conte comigo para o que ser e vier. Além de tudo ainda me trouxe
a Agnes de presente! Doce, linda e forte foi um prazer ter compartilhado tanto com esse
casal lindo e peculiar que vocês formam.
Agradeço a todo o apoio do PPG Psicobiologia e de todo seu corpo docente. Ao
Prof. Arrilton Araújo, obrigada por realmente estar do lado dos alunos em meio a crises
existenciais e financeiras, para comemorar vitórias e dar concelhos construtivos.
Obrigada professora Fátima Arruda pela imensurável compreensão e sabedoria. Agradeço
ao CNPq pela bolsa de mestrado. Ao Bill Rossiter que por meio da Cetacean Society
International forneceu muito mais do que financiamentos para nosso projeto, nos deu
inspiração. A Rufford Fundation, pelo apoio financeiro fundamental para a realização
deste trabalho. A Karina Groch, que me recebeu de braços abertos no Projeto Baleia
Franca. A todos os estagiários do Projeto do ano de 2013 em especial Mariana Martins e
Fernanda França. Pela participação fundamental, agradeço a Camila Moraes, Dai Anzolin
e Carolina Bezamat. Pelo apoio logístico a Fundação Pro-TAMAR, em especial Juçara
Wanderlinde, Luiz Rodrigo Maçaneiro e Gustavo Stahelin; a APA Baleia Franca, APA
Anhatomirim, Rebio Arvoredo, Esec Carijós e ao ICMBio, a Polícia Ambiental de
Laguna, e a Murilo Ternes da Base Cangulo. Paulo Flores, obrigada por ser mais um
orientador para mim, por apontar meus erros (em geral bem alto para todo mundo ouvir)
e por recompensar meus acertos. Você é peça chave neste trabalho e com certeza tem
participação fundamental na minha formação como cientista criteriosa, rigorosa e
perfeccionista. Obrigada aos membros da banca pelos comentários fundamentais para a
consolidação deste projeto.
E finalmente obrigada as minhas orientadoras, Renata e Susan. Foi uma honra e
um desafio ter meu nome associado ao de vocês e trabalhei duro para fazer jus a confiança
que foi em mim depositada. Susan, obrigada por ter aberto as portas do seu laboratório e
por ter me recebido tão bem durante minha visita. Renata, ainda me lembro da sua
resposta ao primeiro e-mail que te enviei buscando um orientador para o mestrado: passe
na prova e conversamos. Estudei, passei, e nosso trabalho juntas teve início assim como
nossa amizade. Eu nunca poderei mensurar o quanto evolui trabalhando sob sua
orientação, estando você presente ou não. As portas que você me abriu, a confiança, os
conselhos estratégicos. Minha admiração por você é enorme. Espero tê-la ao meu lado
por muitos e muitos anos de trabalho e felicidades pela vida. Obrigada pelas grandes
oportunidades que você me proporcionou.
E claro, obrigada as baleias francas por existirem e por me permitirem mergulhar
em suas conversas. E peço que me desculpem por contar tudo o que eu vi e ouvi, por meio
deste trabalho... Não é fofoca! É adoração, respeito, e senso de responsabilidade. Trabalho
todos os dias da minha vida se necessário para protegê-las e para garantir a vocês o direito
de nadar pelos oceanos a fora em segurança, como vocês a milhões de anos fazem, antes
mesmo da nossa chegarmos neste mundo. Obrigada ás poderosas águas do mar, por
permitirem nossa presença em sua imensidão, e sempre nos trazerem de volta em
segurança.
Sumário
Resumo
p.1
Abstract
p.3
1. Introdução Geral
p.5
2. Objetivos
p.19
Artigo 1 - Vocalizations produced by Southern right whale (Eubalaena australis)
female-calf pairs in wintering area off Brazil.
p.21
I. Introduction
p.25
II. Material and Methods
p.27
III. Results
p.30
IV. Discussion
p.33
V. Conclusion
p.34
VI. Acknowledgments
p.36
VIII. References
p.37
Tables
p.43
Artigo 2 - Diel pattern in Eubalaena australis mother-calf pairs’ calling behavior
p.45
Acknowledgments
p.54
Literature Cited
p.55
Figures
p.60
Tables
p.63
Artigo 3 - Behavioural context of southern right whale (Eubalaena australis)
mother-calf vocalizations
Introduction
p. 64
p.68
Material and Methods
p.70
Results
p.74
Discussion
p.74
Conclusion
p.80
Acknowledgments
p.81
Figures
p.82
Tables
p.83
Literature Cited
p.84
3. Discussão geral e conclusões
p.90
4. Referências Bibliográficas
p.93
Resumo
O monitoramento acústico passivo (MAP) permite a convergência de soluções para questões
conservacionistas e científicas e vêm sendo utilizado com sucesso para a examinar diversos
aspectos da biologia de cetáceos. Todavia, sua aplicação para ambos os fins depende da correta
interpretação dos dados coletados e portanto de conhecimentos prévios sobre o comportamento
e o repertório acústico da(s) espécie(s) alvo(s). O sul do Brasil é uma importante área de
reprodução para baleias francas austrais (Eubalaena australis). Esta espécie ameaçada agregase anualmente entre Julho e Novembro principalmente no estado de Santa Catarina. Medidas
de proteção são necessárias para assegurar a recuperação e para mitigar os efeitos de atividades
antrópicas sobre esta população. Visando construir conhecimento necessário para
implementação de MAP como ferramenta de pesquisa e conservação da baleia franca no Brasil,
o objetivo deste trabalho é reunir informações sobre a ecologia acústica de pares-mãe filhote da
espécie. Sensores acústicos autônomos foram instalados em duas localidades na APA Baleia
Franca e continuamente monitoraram o ambiente e as vocalizações de baleias francas. 1427
chamados com SNR≥10dB foram classificados em 7 categorias: upcall (55.8%), downcall
(12.9%), down-upcall (12.3%), tonal constante (10.1%), tonal variável (6.7%), híbrido (1.6%)
e pulsado (0.6%). Valores médios de frequência inicial, final, máxima, mínima, banda de
frequência, frequência de pico e duração foram obtidos. A análise do padrão nictemeral do
comportamento vocal mostrou que este não varia significativamente (Kruskal-Wallis x2=5.86,
df=3, p=0.12) ao longo de 24hs. Provavelmente, estes resultados estão relacionados ao estado
comportamental predominante dos pares e refletem a relação espacial entre mães e seus
respectivos filhotes no período final de permanência na área de invernagem. Gravações
realizadas com um arranjo linear de hidrofones sincronicamente a observações
comportamentais, revelaram que a taxa de emissão de chamados está relacionada ao nível de
1
atividade em cada estado comportamental. Em estados de maior atividade, como durante
interações entre pares e entre mães e seus filhotes, a taxa de emissão de chamados foi
respectivamente 3.35 e 0.21 chamados/minuto. Por outro lado, enquanto se deslocando ou em
descanso, a taxa de vocalização foi de 0.12 e 0.02 chamados/minuto. Nenhuma vocalização foi
atribuída aos pares focais em mergulho ou amamentando. Classes de chamados distintas foram
emitidas em proporções diferentes em cada estado comportamental. O significado funcional
das classes de vocalização no contexto da comunicação de pares fêmea-filhote é semelhante a
aquele descrito em estudos prévios, realizados com outros tipos de grupo da espécie. A
composição de informações gerada por este trabalho constitui as bases do conhecimento acerca
da bioacústica da baleia franca no Brasil e serão fundamentais para a implementação de
ferramentas de monitoramento e preservação baseadas em princípios acústicos. Além disso,
este trabalho representa um importante passo para a expansão do conhecimento do
comportamento vocal de pares mão-filhote, um subgrupo vulnerável porém vital para as
populações.
Palavras-chave: Comportamento vocal, repertório acústico, ecologia comportamental, baleia
franca do Atlântico Sul, par mãe-filhote, monitoramento acústico passivo.
2
Abstract
Remote acoustic sensing has been used to investigate several aspects of cetacean ecology and
behaviour as occurrence, population density and impacts of anthropogenic sounds on
communication systems. Nonetheless, the efficiency of PAM methods depends on the ability
of researchers to detect and interpret acoustic signals and therefore on baseline information
about natural features of the target species’ vocal behaviour. The coastal waters off the state of
Santa Catarina, Brazil, are an important wintering ground for Southern right whales (Eubalaena
australis). Right whales aggregates in this area year after year, between July and November and
protection measures are due to ensure the safety and health of this population. Aiming to build
the required knowledge to use PAM as a right whale conservation and research tool in Brazil,
the objective of the present study is to gather information concerning the acoustic ecology of
right whale mother-calf pairs off Santa Catarina. Bottom-mounted archival acoustic recorders
were deployed in two locations at the Right Whale APA during the wintering season. 1427 right
whale calls with SNR≥ were classified in 7 call classes accordingly to visual and aural
characteristics: upcall (55.8%), downcall (12.9%), down-upcall (12.3%), tonal constant
(10.1%), tonal variable (6.7%), hybrid (1.6%) and pulsive (0.6%). Mean values of start, end,
maximum and minimum frequencies, frequency bandwidth, peak frequency and duration were
calculated. Temporal pattern analysis revealed no significant diel trend in the emission of
contact calls (Kruskal-Wallis test chi-square=5.86, df=3, P=0.12). Results may be linked to the
predominant behavioral of whale groups through the period of stay at the wintering area. Using
synched surface-behavioral observations and acoustic recordings, calling rates were obtained
and the use of call classes in different behavioral states was discussed. Calling rates (call/min)
were associated with the activity level of mo/ca pairs, greater in interactions and bonding and
lower during travelling and resting. No calls were attributed to diving or nursing pairs. Upcalls
and down-upcalls calls were attributed to resting pairs as well as traveling pairs. Constant calls
3
were detected when a pair was swimming toward the research boat and pulsive calls were
detected in the presence of dolphins in close proximity to the dislocating focal group.
Interestingly, mo/ca pairs spend 20% of the sampling time interacting with other pairs and the
greatest diversity of calls was recorded during such events. Pulsive (12%) and hybrid calls (13%
- exclusively recorded during mo/ca interactions) are characteristics of agonistic behavior
between whales. When bonding, mother and/or calves produced exclusively upcalls. The
adaptative significance of previously described calls in mother-calf pair´s communication is
similar to what has been described for other whale groups. This dissertation brings significant
information that constitutes bases of right whale bioacoustics in Brazil, and therefore will be
vital for the implementation of mitigation, monitoring and investigation tools based on acoustic
principles. Moreover, it contributed to fulfil the lack of behavioural and acoustic data of mothercalf pairs a highly vulnerable and vital subgroup for all right whale populations.
Keywords:
Vocal behaviour, vocal repertoire, behavioural ecology, southern right whales,
mother-calf pair, passive acoustic monitoring.
4
1. Introdução Geral
1.1 Comunicação animal
“Nothing would work in the absence of communication...”
(Hauser, 1997)
A comunicação é uma interação inerente aos seres vivos. Desde organismos solitários e
simples, até animais cognitivamente desenvolvidos cujas relações sociais são extremamente
complexas, todos podem se beneficiar da comunicação, qualquer que seja a escala em que ela
ocorra (Hauser 1997).
A investigação da comunicação é importante por uma série de razões. Do ponto de vista
comportamental e evolutivo a comunicação é a base das relações sociais e das sociedades
animais e é um produto da adaptação das espécies (Bradbury & Vehrencamp, 1998). O
conhecimento acerca das informações trocadas pelos indivíduos pode elucidar questões sobre
os fatores que influenciaram a evolução do comportamento das espécies. Em espécies sexuadas,
a reprodução é altamente dependente da comunicação e seu estudo é ferramenta para
compreensão das relações entre parceiros reprodutivos (Bradbury & Vehrencamp, 1998). Além
disso, o entendimento da comunicação animal pode e deve ser aplicado em prol do bem-estar
de animais em cativeiro assim como para a conservação de espécimes selvagens (Bradbury &
Vehrencamp, 1998).
A comunicação pode ser definida como o processo pelo qual emissores empregam sinais
especialmente projetados, ou displays, para modificar o comportamento dos receptores (Krebs
et al. 2012). A comunicação portanto envolve a transmissão de uma informação provisionada a
um receptor por um emissor. O receptor por sua vez deve ser capaz de captar, interpretar e
tomar decisões baseando-se nas informações contidas nos sinais recebidos (Endler 1993). O
“veículo” de transmissão destas informações através do meio é denominado sinal (Fig.1).
5
Fig.1 – Exemplificação dos elementos envolvidos na comunicação entre dois indivíduos. Um emissor produz um
sinal. O sinal carrega uma mensagem através do meio. Esta mensagem, se recebida e processada, produzirá uma
resposta comportamental no receptor gerando benefícios ao emissor.
O sinal altera o comportamento de outro organismo e este evolui justamente por causa
de seu efeito e da coevolução da resposta apresentada pelo receptor (Smith & Harper 2003).
Sinais podem conter informações sobre identidade e localização do emissor e a eles podem ser
atribuídos significados contextualizados na resolução de conflitos, defesa de território,
interações sexuais, sociais, na autocomunicação e interações pais-prole (Hauser 1997; Bradbury
& Vehrencamp 1998; Smith & Harper 2003).
A evolução dos sinais depende de constrições fisiológicas, morfológicas e cognitivas
dos envolvidos no processo de geração e recepção do sinal e das características do meio no qual
a comunicação ocorre (Endler 1993; Bradbury & Vehrencamp 1998). A natureza dos estímulos
informativos pode ser química, visual, elétrica, tátil e/ou acústica de modo a obter-se
maximização e otimização da transferência da informação conforme as pressões evolutivas de
cada ambiente (Bradbury & Vehrencamp 1998; Smith & Harper 2003).
Sinais acústicos são empregados por uma grande variedade de espécies e muitas delas
utilizam displays vocais, vocalizações, para a transmissão de informações (Bradbury &
Vehrencamp 1998; Smith & Harper 2003). Vocalizações são produzidas por anfíbios anuros
6
(Kelley 2004), répteis quelônios e crocodilianos (Vergne et al. 2009; Ferrara et al. 2013) e
diversos mamíferos como quirópteros, elefantídeos e primatas (Rübsamen 1987; Boughman &
Wikison 1998; Arnold & Zuberbühler 2008; Soltis 2010). Porém, a vocalização mais bem
estudada quanto a ontogenia, evolução e função ecológica até o momento, é provavelmente o
canto das aves (Marler & Slabbekoorn 2004). Sinais acústicos são especialmente importantes
para a comunicação no ambiente aquático e animais tais como pinípedes e cetáceos possuem
amplo repertório vocal (Payne & McVay 1971; Moore 1974; Thomas & Kuechle 1982; Au
1993).
1.2 Cetáceos e os desafios sensoriais no ambiente aquático
Há aproximadamente 10 milhões de anos atrás, o ancestral terrestre dos atuais cetáceos
adentrava um novo ambiente: a água. Este novo meio não direcionaria apenas a evolução da
morfologia destes seres mas também modificaria a funcionalidade dos sistemas sensoriais e
consequentemente de seus mecanismos de comunicação (Tyack 2000).
A água é um meio mais denso e mais viscoso do que o ar. Possui elevada capacidade
térmica e alta capacidade de dissolução. Nela compostos químicos como feromônios e outras
partículas olfativas viajam muito lentamente e por isso são ineficazes para a comunicação
rápida e de longo alcance (Thomas & Kastelein 1990; Tyack 2000). Apesar da propagação
eficiente de sinais elétricos na água, cetáceos em geral possuem discreta eletrossenbilidade. Em
botos-cinzas (Sotalia guianenis), criptas vibrissais foram recentemente descritas como órgãos
eletrossensíveis funcionais porém, sua eficiência e a extensão de sua utilidade sensorial ainda
são incógnitas (Czech-Damal et al. 2012). Em contrapartida, o contato físico entre os indivíduos
representa importante ferramenta de manutenção de relações afiliativas. Sugere-se por exemplo
que o contato sexual exerça um papel valioso nas relações sociais de diversas espécies de
cetáceos (Tyack 2000).
7
A maioria dos cetáceos possui função visual desenvolvida e adaptada para o ambiente
subaquático (Thomas & Kastelein 1990; Tyack 2000). Os olhos são capazes de suportar as
pressões de mergulhos profundos, grandes variações de temperatura e algumas espécies podem
enxergar fora d’água tão bem quanto dentro dela (Thomas & Kastelein 1990; Tyack 2000). Por
essa razão displays visuais são utilizados por algumas espécies, por exemplo golfinhos narizde-garrafa (Tursiops sp.) na comunicação de curto alcance, em interações sexuais ou agressivas
(Fig. 2). Bolhas, posturas, movimentos e diferentes pigmentações (Caro et al. 2011) são
exemplos de sinais que podem ser empregados na comunicação visual (Tyack 2000). Entretanto
a intensidade, distribuição e a disponibilidade dos componentes espectrais da luz tornam-se
cada vez menores conforme há o aumento da profundidade prejudicando a sensibilidade e a
definição da visão (Warrant & Locket 2004). A luz que se propaga no meio aquático é
severamente absorvida pelo meio entretanto o mesmo não é verdadeiro para ondas sonoras.
Fig. 2 - Coalisão de golfinhos pintados do Atlântico (Stenella frontallis) machos em resposta a presença de um
golfinho nariz de garrafa (Tursiops truncatus) macho. A união de cabeças, movimentos sincrônicos e a
apresentação
da
boca
aberta
são
parte
do
display
agressivo
da
espécie.
Fonte:
http://www.wilddolphinproject.org/dolphins-2/life-in-a-dolphin-pod-male-social-structure/
Acesso
em
15/04/2015.
A onda sonora é uma onda mecânica e portanto necessita de um meio para se propagar
(o ar ou a água, por exemplo). Na água, a propagação do som é mais veloz e mais eficiente do
que no ar e sua absorção é consideravelmente menor do que a absorção da luz. Nenhuma outra
forma de energia se propaga no meio aquático como a energia sonora e por isso, o emprego da
8
acústica para investigar diversos aspectos ecológicos e comportamentais dos quais depende a
sobrevivência de cetáceos é uma estratégia extremamente eficiente (Au & Hastings 2008).
1.3 Sons e os grandes cetáceos
Cetáceos dependem do som em inúmeros aspectos de sua ecologia comportamental tal
como a exploração do ambiente, localização de presas e comunicação (Tyack 2000).
Misticetos, ou baleias de barbatanas, em geral produzem sons de baixa frequência
capazes de se propagar por longas distâncias (Payne & Webb 1971). O repertório acústico das
baleias verdadeiras pode ser divido em sons vocais e não-vocais (Clark 1990). Sons não-vocais
incluem sopros – produzidos durante a expiração ou inspiração no momento da passagem do ar
pelos orifícios respiratórios; são sons de baixa intensidade, caóticos com energia distribuída em
largas bandas de frequência – “slaps”, - sons percussivos produzidos em geral como produto de
comportamentos aéreos; são sons intensos e de curta duração, com energia distribuída por
diversas frequências – e sons diversos – produzidos por exemplo, pela flatulência ou pelo atrito
da superfície do corpo do animal em um objeto. Tanto sopros quanto “slaps” podem ser
importantes para a comunicação (Clark 1990).
Sons vocais podem ser canções ou chamados. Canções são emissões vocais longas e de
estrutura complexa onde sequências de notas estereotipadas são reproduzidas repetidamente de
maneira padronizada em um intervalo de tempo (Payne & McVay 1971). Uma canção pode ser
subdividida em unidades hierárquicas conforme proposto por Payne & McVay (1971). Desta
maneira, uma canção é composta por conjuntos de temas. Temas são sequências de frases.
Frases são constituídas por unidades ou notas reproduzidas em série. Unidades podem ser
definidas como os sons contínuos de menor duração numa canção. Apesar de amplamente
utilizada, a divisão sistemática das canções de misticetos possui diversos aspectos subjetivos e
arbitrários que devem ser esclarecidos e padronizados (Cholewiak et al. 2012). É provável que
9
a canção mais estudada dentre os cetáceos seja a canção das baleias jubarte (Megaptera
noveangliae) (Payne & McVay 1971). Porém outras espécies também produzem canções, como
por exemplo baleias azuis (Balaenoptera muscuslus) (Cummings & Thompson 1971), fin
(Balaenoptera
physalus)(Croll
et
al.
2002),
baleias-da-Groenlândia
(Balaena
mysticetus)(Tervo et al. 2009) e baleias minke (Balaenoptera ocutorostraca) (Gedamke et al.
2001). As baleias francas (Eubalaena sp.) no entanto, produzem exclusivamente chamados
(Clark 1983).
A
B
Fig. 3 – Espectrogramas de canto de baleia jubarte (Megaptera novaeangliae) gravado no Brasil em 2005 e suas
subdivisões hierárquicas. A) Em detalhe, seleção de uma frase. Setas indicam os limites de subfrase enquanto que
letras indicam notas desta frase; B) Parte de uma gravação contínua onde retângulos numerados mostram as frases
que compõem temas. Adaptado de Sousa-Lima (2007).
10
Chamados são vocalizações discretas de curta duração (Fig.4). Clark (1990) divide os
chamados produzidos por misticetos em três categorias gerais: a) chamados simples, b)
chamados complexos e c) clicks, pulsos, estalos e grunhidos. Chamados simples possuem
energia concentrada em bandas estreitas de frequência, em geral abaixo de 1000Hz. Podem ser
modulados em frequência (FM) e conter alguma modulação de amplitude (AM) e harmônicos.
Auralmente se assemelham a lamúrias. Chamados complexos por sua vez são altamente
modulados em frequência e amplitude. Podem ser pulsados e ocupam faixas de frequência
entre 500 e 5000 Hz. São frequentemente chamados de rosnados ou gritos. Por fim, clicks,
pulsos, estalos e grunhidos são sons de duração menor que 0,1 segundo com nenhuma
modulação de frequência. Estes podem ocupar bandas estreitas ou largas de frequências altas
ou baixas e portanto são altamente variáveis entre as espécies em que ocorrem.
Fig.4 – Espectrograma (FFT=512, 50% de sobreposição) retratando sequência de chamados de baleia franca
austral. Cada retângulo destaca um chamado.
1.4 Produção e captação de sons em misticetos
Apesar de serem denominados vocais, os sons descritos a cima não são produzidos pela
vibração de cordas vocais (Reidenberg & Laitman 2007, 2010). Da mesma maneira que
11
mamíferos terrestres, as vocalizações de baleias são produzidas pela passagem do ar por meio
de membranas localizadas no lúmen da laringe, sendo a vibração produzida a origem da
perturbação no meio que gera o som. Todavia, misticetos não possuem pregas vocais e sim uma
estrutura homóloga denominada prega em U (U-fold) (Reidenberg & Laitman 2007; Adam et
al. 2013) disposta paralelamente ao fluxo de ar. O som produzido então se propaga através dos
tecidos moles da região da cabeça do animal e são transferidos para o ambiente com elevada
eficiência devido a semelhança de impedância e densidade destes tecidos e da água (Reidenberg
& Laitman 2010; Adam et al. 2013) (Fig. 5).
A
B
Fig. 5 - Produção de sons em misticetos. A) Visão dorsal da laringe de baleia franca do Atlântico Norte (Eubalaena
glacialis). Asteriscos brancos indicam a localização da prega em U; B) Exemplificação da hipótese de Reidenberg
& Laitman (2007) que explica o mecanismo de propagação e transferência do som para o meio. Em vermelho:
trato respiratório; em azul: trato digestivo; em rosa: lúmen da laringe; em branco: tecido cartilaginoso; em amarelo:
prega em U; em contorno verde: saco vocal. A adução das pregas em U na direção dorsal restringe a passagem do
ar na traqueia (vermelho) direcionando-o para o saco vocal. O contorno da prega em U vibra conforme a passagem
do ar. A vibração se propaga por todo o saco vocal, pelos tecidos da garganta e finalmente é transferida para o
meio. Imagens adaptadas de Reidenberg & Laitman (2007).
Além de fundamental no processo de geração e emissão de sons, o saco vocal também
pode ser importante para a manutenção da pressão no sistema respiratório e na flutuabilidade
dos animais (Gandilhon et al. 2015).
A audição de cetáceos é adaptada para captar sons no meio aquático (Nummela 2008;
Mooney et al. 2012). A estrutura de seu sistema auditivo deriva da anatomia básica do ouvido
de mamíferos terrestres mas atualmente o sistema auditivo dos cetáceos é mais complexo e
12
diverso do que qualquer grupo de mamíferos não-aquáticos (Ketten 1994). Cetáceos não
possuem pavilhão auricular externo, o canal auditivo foi reduzido a uma passagem estreita e
vestigial e o ouvido médio e interno se fundiram em uma estrutura densa denominada complexo
timpânico-peritótico (Ketten 1994; Yamato et al. 2012).
Em odontocetos, acredita-se que o som é captado do meio e transmitido para o complexo
timpânico-periótico por meio de tecido adiposo especializado localizado nas mandíbulas e ao
redor da cavidade timpânica (Yamato et al. 2012). Misticetos por outro lado, possuem anatomia
craniana distinta dos odontocetos e seu mecanismo de audição é pouco esclarecido (Tubelli et
al. 2012; Yamato et al. 2012). Nos últimos anos porém, o uso de tecnologias como a ressonância
magnética, tomografias e a modelagem computacional, permitiram avanços importantes quanto
a elucidação do mecanismo de capitação de sons pelas grandes baleias (Tubelli et al. 2012;
Yamato et al. 2012; Cranford & Krysl 2015). Evidências recentes sugerem que o principal meio
de condução do som de baixa frequência (<5kHz) é a condução óssea: a interação entre as ondas
incidentes e a estrutura densa do crânio gera deformações na estrutura óssea que por sua vez,
induzem o movimento do complexo ósseo timpânico-periótico. Ao menos para balenopterídios,
tecido adioposo acústico também é importante para a condução do som até o complexo
timpânico-periótico (Yamato et al. 2012; Cranford & Krysl 2015). Ainda assim, a
funcionalidade do canal auditivo permanece desconhecida, assim como a função do dedo-deluva, uma estrutura evertida, extensa e espessa derivada da membrana timpânica, presente
apenas na subordem Mysticeti (Tubelli et al. 2012; Yamato et al. 2012).
Tratando-se ainda de misticetos, audiogramas baseados em dados empíricos são raros
devido principalmente a impossibilidade da manutenção destes animais em cativeiro e
limitações tecnológicas para realização de experimentos em animais de vida livre (Ketten 1994;
Nummela 2008). As estimativas da capacidade auditiva desses animais são baseadas nas
frequências de suas vocalizações ou na descrição anatômica da orelha das espécies (Ketten
13
1994; Parks et al. 2007). Por exemplo, a partir de análises morfométricas do crânio de animais
encalhados, Parks e colaboradores (2007) criaram um modelo funcional do sistema auditivo de
baleias francas do Atlântico Norte (Eubalaena glacialis) e estimaram a capacidade auditiva da
espécie entre 10 Hz e 22kHz.
O estudo dos mecanismos envolvidos na captação e processamento de sons em cetáceos
são fundamentais para avaliação de impactos de ruídos antropogênicos no sistema de
comunicação, na fisiologia e na sobrevivência das populações.
1.5 A baleia franca
As baleias francas (Eubalaena sp.) pertencem a ordem Cetartiodactyla, e juntamente
com as baleias-da-Groenlândia (Balaena misticetus), compõe a família Balaenidae da subordem
Mysticeti (Shirihai & Jarrett 2006; Kenney 2008). O gênero Eubalaena possui características
marcantes que facilitam identificação de suas espécies. Dentre elas: ausência de pregas ventrais;
orifícios respiratórios bem demarcados e separados originando borrifo em formato de “V”;
ausência de nadadeira dorsal e calosidades epidérmicas infestadas por ciamídeos (Cyamidae)
na região da cabeça, boca e orifício respiratório (Payne 1983; Payne et al. 1983; Payne and
Dorsey 1983) (Fig. 6). A distribuição das calosidades é assimétrica em um mesmo indivíduo e
varia de indivíduo para indivíduo permitindo que estas marcam sejam utilizadas para atribuição
de identidade individual aos membros de uma população (Payne et al. 1983).
A coloração destes animais varia entre o acinzentado e o preto e eventualmente podem
apresentar manchas brancas ou acinzentadas (Payne et al. 1983) (Shirihai & Jarrett 2006;
Kenney 2008). Os filhotes nascem com aproximadamente 6m de comprimento enquanto os
adultos podem medir até 18m, sendo as fêmeas adultas em geral, maiores do que os machos
(Payne et al. 1983; Shirihai & Jarrett 2006; Kenney 2008). A região da cabeça se estende por
14
1/3 do comprimento total do corpo (Payne et al. 1983). As nadadeiras peitorais possuem a
distinta forma de um trapézio (Shirihai & Jarrett 2006; Kenney 2008).
B
A
C
D
Fig. 6 – Características do gênero Eubalaena. A) Visão superior do rostro de baleia franca austral (E. australis).
Note as calosidades epidérmicas incrustadas por crustáceos ciamídeos e o orifício respiratório bipartido; B) Par
mãe-filhote de E. australis. Note a ausência de nadadeira dorsal em ambos os indivíduos; C e D) Baleias francas
saltando. Observe a ausência de pregas ventrais. Imagens: Paulo A. C. Flores.
Em média, fêmeas produzem um filhote a cada 3 anos e atingem a maturidade sexual
aos 6 anos. Porém, a primeira gestação ocorre apenas aos 9. O período de gestão varia entre 11
e 12 meses e o desmame acontece após o primeiro ano de vida do filhote (Hamilton et al. 1998).
Uma fêmea pode viver até 65 anos e é reprodutivamente ativa por aproximadamente 30 anos
(Best 1994).
As baleias francas, assim como outras espécies de misticetos, passam o verão nos polos
e nos meses de inverno migram para águas tropicais e subtropicais para reproduzirem-se, darem
a luz seus filhotes e os amamentarem (IWC 2007; Kenney 2008). Atualmente são reconhecidas
três espécies do gênero Eubalaena (Rosenbaum et al. 2000): E. janoponica (Lacèpéde 1818) de ocorrência limitada à regiões do Pacífico Norte e população estimada em 35 indivíduos
15
(Wade et al. 2011); E. glacialis (Müller 1776) - a baleia franca do Atlântico Norte de população
estimada em 509 indivíduos (Pettis 2012) e E. australis (Desmoulins 1822) – que habita apenas
as águas do Hemisfério Sul e cuja população é estimada em 12.000 indivíduos (IWC 2012).
Baseando-se nas diferentes áreas reprodutivas, foram estabelecidos quatro estoques
reprodutivos primários para a baleia franca austral: Austrália, África do Sul, região subantártica
da Nova Zelândia e América do Sul (IWC 2007; 2012). Na Argentina a região da Península
Valdés abriga o maior número de baleias durante a temporada de inverno (IWC 2007; 2012) na
América do Sul. No Brasil, a ocorrência de baleias francas está concentrada principalmente na
região sul do país (Groch et al. 2005a; IWC 2007).
1.6 Baleias francas no Brasil
Baleias francas (E. australis) podem ser observadas no Brasil entre Julho e Novembro,
sendo o mês de agosto o período de maior abundância de indivíduos (Groch et al. 2005a; IWC
2007). A maior concentração destes animais acontece no Estado de Santa Catarina entre o Cabo
de Santa Marta, Laguna (28º36’ S, 48º49’ W) e Florianópolis (27º25’ S, 48º30’ W) (Groch et
al. 2005a; Groch et al. 2005b; Groch & Flores 2011).
A população de baleias francas no Brasil foi severamente reduzida pela a caça comercial
(neste caso o termo “população” refere-se ao grupo de animais que visita o Brasil durante a
temporada). Porém, não existem registros oficiais quantificando o número de animais abatidos
no país (Tormosov et al. 1998). Sabe-se que a área de ocorrência original da espécie estendiase desde a divisa com o Uruguai até a Bahia (Greig et al. 2001; Santos et al. 2001). Durante a
década de 70, os registros da espécie restringiram-se a animais encalhados e somente nos anos
80 os animais foram reavistados na costa de Santa Catarina (Tormosov et al. 1998). Estudos
revelam que a população brasileira vem se recuperando (Groch et al. 2005b; Groch & Flores
16
2011), no entanto, E. australis ainda consta na Lista de Espécies Ameaçadas como "em perigo"
(Ott et al. 2008) (Fig. 7).
A
B
Fig.7 - As principais ameaças a sobrevivência de baleias francas austrais são colisões com embarcações, os
emalhes em redes de pesca, a expansão do turismo de observação e a degradação do ambiente marinho (Ott et al.
2008; Reilly et al. 2013). A) fêmea de baleia franca austral na praia da Ribanceira, Santa Catarina, 2013; B) detalhe
apontado pela seta em vermelho: rede de pesca artesanal emalhada ao redor da boca do animal. Imagem: Carolina
Bezamat.
1.7 Bioacústica e conservação da baleia franca
A produção de sons por baleias francas foi inicialmente investigada por Cummings e
colaboradores (1972). Neste trabalho, o repertório acústico das baleias foi descrito em quatro
categorias: sons similares a eructações (belch-like sounds); lamúrias (moans); pulsos (pulses) e
sons diversos (miscellaneous).
Na década seguinte, Clark realizou estudos sistemáticos do repertório e do
comportamento de baleias francas austrais. Seu experimento de playback corroborou com a
hipótese de que os sons produzidos pelos animais teriam função de comunicação (Clark & Clark
1982). Clark (1983) também relacionou os sons ao nível de atividade e as características de
17
grupos de baleias e descreveu os parâmetros acústicos para 6 categorias de sons vocais (upcall,
downcall, pulsive call, hybrid call, high call, constant call) e 2 categorias de sons não vocais
(slaps e blows). Estas categorias são empregadas até hoje como bases para a classificação do
repertório das espécies do gênero Eubalaena. Parks e colaboradores (2005) investigaram a
produção de sons em grupos ativos de superfícies e complementaram algumas das inferências
feitas por Clark sobre a contextualização comportamental dos diferentes tipos de chamados
produzidos pela baleia franca. No entanto, o conhecimento acerca do significado funcional dos
chamados de baleias francas ainda é escasso e outros estudos são necessários para que a função
de cada tipo de som seja melhor entendida, especialmente em áreas de reprodução.
A importância da bioacústica e dos estudos de comportamento para a conservação vem
crescendo (Caro 2007; Laiolo 2010). No que diz respeito a conservação de cetáceos, técnicas
fundamentadas em princípios bioacústicos vem sendo empregadas em diversas regiões do
planeta para obtenção de parâmetros ecológicos populacionais de diferentes espécies (Clark et
al. 1996; Van Parijs et al. 2009; Marques et al. 2013). Sistemas de detecção de presença
baseados em sinais acústicos mostraram-se bem sucedidos na prevenção de colisões entre
baleias e embarcações (Hatch et al. 2012) particularmente no caso da baleia franca do Atlântico
Norte.
Contudo, as aplicações da bioacústica para conservação e pesquisa dependem da
detenção do conhecimento básico em relação a ecologia comportamental e acústica das espécies
incluindo taxas de emissão de chamados em relação ao comportamento dos animais, existência
de variação temporal na emissão vocal, parâmetros acústicos do repertório, entre outros
(Mellinger et al. 2006; Van Parijs et al. 2009; Marques et al. 2013; Sousa-Lima et al. 2013).
Tratando-se da baleia franca em suas áreas de ocorrência no Brasil, estes estudos são escassos
e como consequência, esta ciência não é aplicada em todo seu potencial para investigação do
comportamento e para proteção desta espécie ameaçada.
18
2. Objetivos e estrutura da dissertação
Considerando o diminuto número de trabalhos sobre a ecologia acústica da baleia franca
no Brasil; e a necessidade da expansão do conhecimento científico acerca do sistema de
comunicação e do comportamento da espécie, o objetivo desta dissertação é investigar a
ecologia acústica da baleia franca austral (Eubalaena australis) tendo como área de estudo
águas costeiras do estado de Santa Catarina, Brasil. Favorecidos por sua predominante presença
na região, de maneira inovadora, esta dissertação aborda principalmente sons e comportamentos
de grupos compostos pela fêmea e seu respectivo filhote: os pares mãe-filhote ou ainda pares
fêmea-filhote (Fig. 8). Durante a estruturação e execução deste projeto, a motivação de
conservação da espécie sempre esteve presente. A composição de informações geradas por este
trabalho constitui as bases do conhecimento acerca da bioacústica da baleia franca no Brasil e
serão fundamentais para a implementação de ferramentas de monitoramento e preservação
baseadas em princípios acústicos.
Este estudo foi divido três capítulos. Cada capítulo corresponde a um manuscrito a ser
submetido a revistas científicas de relevância internacional e por essa razão, foram elaborados
em inglês. O primeiro capítulo corresponde ao artigo: “Vocalizations produced by Southern
right whale (Eubalaena australis) mother-calf pairs in a calving area off Brazil” e traz a
descrição dos parâmetros acústicos dos chamados de pares mãe –filhote gravados no Santa
Catarina e testa a categorização dos chamados incluídos em seu repertório por meio de uma
metodologia estatística baseada em clusters. O segundo manuscrito é intitulado “Eubalaena
australis mother-calf pairs’ upcall production is independent of diel period in Brazil” e
investiga a variação nictemeral da atividade vocal dos pares. O terceiro capítulo, corresponde
ao artigo: “Behavioural context of southern right whale (Eubalaena australis) mother-calf
vocalizations” que descreve a produção de sons por pares mãe-filhote em diferentes estados
19
comportamentais; testa a associação entre o uso de chamados e o estado comportamental dos
pares e determina taxas de vocalização de acordo com seu comportamento.
A
B
Fig. 8 – A) Par fêmea-filhote e B) Filhote de baleia franca austral na Praia da Ribanceira, SC, 2013. Imagens:
Paulo A. C. Flores e Julia Dombroski.
20
ARTIGO 1
Vocalizações de pares mãe-filhote de baleia franca austral (Eubalaena australis) em uma área
de invernagem no Brasil.
Autores:
1. Julia R. G. Dombroski; Laboratório de Bioacústica, Universidade Federal do Rio Grande
do Norte.
2. Susan E. Parks, Universidade de Syracuse.
3. Karina R. Groch, Projeto Baleia Franca.
4. Paulo A. C. Flores, Centro Nacional de Pesquisa e Conservação de Mamíferos Aquáticos,
ICMBio.
5. Renata S. Sousa-Lima, Laboratório de Bioacústica, Universidade Federal do Rio Grande do
Norte e Programa de Pesquisa em Bioacústica, Universidade de Cornell.
Artigo a ser submetido ao Journal of the Acoustical Society of America (QUALIS: A2)
21
Resumo
Com o objetivo de reunir informações sobre as vocalizações de pares mãe-filhote de baleia
franca austral (Eubalaena australis), gravadores autônomos foram instalados em uma
importante área de invernagem para a espécies, no estado de Santa Catarina, Brasil. As
gravações foram realizadas de outubro a novembro de 2012. A inspeção manual dos
espectrogramas revelou sete tipos de chamados: upcall, downcall, down-upcall, tonal variável,
tonal constante, híbrido e pulsado. Valores médios de frequência inicial, final, máxima e
mínima, pico de frequência, largura de banda de frequência e duração foram calculados para
cada classe de chamado. Gunshots e warbles, chamados previamente descritos para outros
populações de baleia franca, não foram detectados. Esta descrição do repertório contrubirá para
a intensificação do uso do Monitoramento acústico passivo como uma ferramenta de pesquisa
e conservação de baleias-francas austrais no Atlântico Sul.
22
Vocalizations produced by Southern right whale (Eubalaena australis) mother-calf pairs in
wintering area off Brazil.
Julia R. G. Dombroski, Graduation Program in Psychobiology, Laboratory of Bioacoustics,
Department of Physiology, Federal University of Rio Grande do Norte, University Campus,
Natal, RN 59078-970, Brazil.
Susan E. Parks, Department of Biology, Syracuse University, 107 College Place, Syracuse,
New York 13244, United States.
Karina R. Groch, Projeto Baleia Franca, P. O Box 201, Imbituba, SC 88780-000, Brazil.
Paulo A. C. Flores, CMA- Centro Nacional de Pesquisa e Conservacão de Mamíferos
Aquáticos, ICMBio, MMA, Jurerê Florianopolis, SC, 88053-700, Brazil.
Renata S. Sousa-Lima, Laboratory of Bioacoustics, Department of Physiology, Federal
University of Rio Grande do Norte, P. O Box 1511, University Campus, Natal, RN 59078970, Brazil and Bioacoustics Research Program, Cornell Laboratory of Ornithology, 159
Sapsucker Woods Road, Ithaca, New York 14850, United States.
Running title: Southern right whales´ calls off Brazil.
23
ABSTRACT
Aiming to gather information concerning Southern right whale (Eubalaena australis) mothercalf pairs’ vocalizations, archival acoustic recorders were deployed off the state of Santa
Catarina, Brazil. Manual inspection of spectrograms, revealed seven call classes: upcall,
downcall, down-upcall, tonal variable, tonal constant, hybrid and pulsive calls. Gunshots and
warbles, vocalizations previously described for other right whale populations were not detected.
Mean values of start, end, maximum, minimum and peak frequencies, frequency bandwidth and
duration were calculated for each call class. Upcalls recorded off Brazil had lowest and shortest
star, end frequency and duration in relation to other right whale populations from the Southwest
Atlantic, North Atlantic and North Pacific right whales. However, only mean duration of upcalls
from Brazil was statistically different from the other populations. Our repertoire
characterization will contribute to magnify the use of passive acoustic monitoring as a
conservation and research tool for Southern Right whales in the Southwest Atlantic.
24
I. INTRODUCTION
Owing to the major role that acoustic communication plays in cetacean ecology (Au,
1993; Tyack, 2000), investigating acoustic repertoires is fundamental to better understand the
life history of cetacean species and to design effective acoustic-based research and management
tools (Bradbury and Vehrencamp, 1998; Van Parijs et al., 2009). Passive acoustic monitoring
(PAM) of dolphins and whales is based on the vital importance of sound for their livelihoods:
navigation, prey location and social interactions (Au, 1993; Tyack, 2000). The development of
PAM has increased the capacity of data acquisition over different temporal and spatial scales
and therefore has improved the applicability of bioacoustics scientific assessment into
management and mitigation measures (Clark et al., 2009; Van Parijs et al., 2009). Among
advantages of PAM over conventional observing methods is cost-effective long-term sampling
that can be continue through adverse weather conditions and during the night (Mellinger et al.,
2007; Van Parijs et al., 2009). Bioacoustic data is especially useful when combined with other
monitoring methodologies, such as visual surveys (Mellinger et al., 2007). Several distinct
sound monitoring devices are now available, fulfilling needs and aims of a great diversity of
applications, study areas and target species (Sousa-Lima et al., 2013). Remote acoustic sensing
has been used to investigate several aspects of cetacean ecology and behaviour as occurrence,
density (Marques et al., 2013), and impacts of anthropogenic sounds on communication
systems (Parks et al., 2007; Clark et al., 2009). Nonetheless, the efficiency of PAM methods
depends on the ability of researchers to detect and interpret acoustic signals and therefore, it
relies on baseline information about natural features of the target species’ vocal behaviour and
vocalizations (Mellinger et al., 2007; Van Parijs et al., 2009).
Right whales (Eubalaena sp.) are known to produce mostly low frequency calls
(<1000Hz) for communication (Clark, 1983; Parks and Tyack, 2005). The species vocal
repertoire may be described as a collection of sounds that encompasses stereotyped and variable
25
calls, from tonal sweeps to broadband pulsive sounds (Clark, 1982; 1983; Parks and Tyack,
2005). Over the past decade, extended effort is being made in order to understand the vocal
behaviour of the North Atlantic highly endangered species Eubalaena glacialis – NARW
(Parks and Tyack, 2005; Parks et al. 2005; Parks et al. 2011; Mussoline et al. 2012; Matthews
et al. 2014; Bort et al. 2015). In the other hand, recent studies on southern right whales´
(Eubalena australis - SRW) sounds and sound production behaviour in the Southern Atlantic
are not so common (Hofmeyr-Juritz and Best, 2011; Tellechea and Norbis, 2012, Parks et al.
in prep).
In the Southwest Atlantic, a SRW wintering ground is found off Brazil (IWC, 2012).
Even though occasional sightings range up to the northeast (Lodi et al., 1996) right whales
concentrate off the state of Santa Catarina (SC), southern Brazil (Groch et al., 2005; IWC 2012).
Sightings in SC are mainly of mother-calf pairs (m/c), (Groch et al. 2005). Pairs usually
aggregate in areas where the shelf break is closer to shore and water depth is less than 30m,
particularly between Imbituba (28°12’S, 48°49’W) and Santa Marta Cape (28°33’S, 48°47’W)
(Espírito Santo et al., 2013; Sayboth et al. 2015). According to latest estimates, from 2002 to
2013 an average of 107 whales/year visited SC area. The Brazilian population (here
“population” is used in reference to whales that visit a particular area during the winter) is
increasing at rate of 12% per year – IC 8.5% - 14.2%, and total abundance is estimated in 1266
individuals (IWC 2012). In order to protect the whale´s concentration areas off SC, the Brazilian
government created an Environment Protected Area (EPA) named Right Whale EPA (Brasil,
2000). Yet, E. australis is listed as “endangered” in the List of the Brazilian Threatened Fauna
(Machado et al., 2005) as it is noticiably threated by antropogenic activities and habitat
degradation (Ott et al., 2008; Rocha-Campos & Camara 2011).
In SC, artisanal fishery is an important income source for local traditional communities.
As a consequence of the use of gillnets close to shore (up to 1000m from coast), entanglements
26
are reported every season (Pontalti and Danielski, 2011; Antunes Zappes et al., 2013). Within
the Right Whale EPA, there is a commercial harbour from which shipping traffic potentially
exposes whales to loss of communication space (Clark et al., 2009), stress (Rolland et al., 2012)
and strikes (Mullen et al., 2013). Moreover, the local whale-watching industry is growing and
very little is known about how such touristic actions may or may not be affecting whales (Ott
et al., 2008; Rocha-Campos & Camara 2011).
Enhanced protection measures and perennial monitoring methods are required to ensure
the long-term health of Brazilian right whales. PAM is a suitable assessment tool that would
help expand scientific knowledge regarding SRW’s behaviour and communication system. It
could provide information regarding noise levels in the whales’ environment, and be applied to
investigate several aspects of the population´s ecology, contributing to the species management
(Sousa-Lima and Clark, 2009; Van Parijs et al., 2009). Nevertheless, no study aiming to
describe the vocal repertoire of SRW in Brazil was ever held, possibly preventing the further
development of PAM as monitoring tool for SRW. Therefore, the objective of our study was to
gather baseline information on southern Right whales´ vocalizations at the state of Santa
Catarina. The repertoire characterization will support the maximization of the use of PAM for
scientific and management purposes at an important wintering area for SRW in the Southwest
Atlantic.
II. MATERIAL AND METHODS
A. Acoustic recordings
Archival acoustic recorders DSG-Ocean (Loggerhead Instruments) were deployed in
two locations off the state of Santa Catarina within the Right Whale EPA: Gamboa (27º57'S,
48º37'W) from October 14 to 28, 2011 and Ribanceira (28º11'S, 48º37'W) from October 15 to
22 and from November 10 to 18, 2011 (Fig.1). Water depth at deployment sites ranged from 8
27
m to 11 meters including tide variations and devices were moored 1.5m above the sea floor.
Recorders were set to continuously sample at a rate of 8 kHz and 16-bit resolution. Low-pass
filter was applied to recordings at 3.3 kHz yielding an analysis bandwidth of 20 Hz to 3.3 kHz.
Frequency response of the recording system covered the fundamental frequency of previously
described right whale calls (Clark, 1983; Parks and Tyack, 2005, Parks et al. 2005).
FIG 1. Map of the study area. Archival acoustic recorders DSG Ocean (Loggerhead
Instruments) were deployed within the Right Whale Environment Protected Area – Right Whale
EPA – off Gamboa and Ribanceira between October and November 2011.
B. Acoustical Analysis
Acoustical analyses were done using the Raven Pro Software 1.4 (Charif et al. 2010).
Manual inspection of spectrograms followed a call-accumulation curve: one-hour files were
randomly examined until no new call type or call type variation was identified in the recordings.
28
Background noise samples were taken (1s duration, frequency range from 50Hz to 600Hz)
allowing comparisons between background noise and right whale calls. Calls with SNR<10 dB
or overlapping with noise and/or other sounds were withdrawn from dataset.
Values of the following acoustic parameters were extracted from the fundamental
harmonic of SRW calls: maximum frequency, minimum frequency, start frequency, end
frequency, frequency bandwidth, peak frequency and total duration (Fig. 2). Measurements of
frequency and temporal features were done in smoothed spectrograms (Hamming window, with
50% overlap) FFT size 1024 and 512, respectively. Start and end frequency of calls with unclear
harmonic structure were calculated by extracting the peak frequency in the initial and final
segments that concentrated the first and last 5% energy of the sound (Trygonis et al., 2013).
Listed parameters were chosen to be comparable to other right whale repertoire descriptions. In
order to compare values of features obtained from upcalls recorded off Brazil to other right
whale populations (cite), two-sided t-tests for independent samples were performed. Statistical
calculations were done using SPSS 21 (IBM Corp).
29
FIG 2. Spectrographic representation of an upcall with illustrated diagram of acoustic features
measured from SRW vocalizations with clear harmonic structure (Hamming window, FFT
1024, overlap 50%).
III. RESULTS
Mother-calf pairs represents 100% of identified whale groups off SC according to aerial
survey census conducted in October and November from 2002 to 2008 (Groch, unpublished
data). All identified groups from land based monitoring off Ribanceira from mid-October to
November 2011 were too m/c pairs (Groch, unpublished data). Therefore, we assume that at
least the massive majority of vocalizations described in our study belongs to m/c pairs.
In total, 162 hours of recordings from both combined deployment locations were
manually analysed. Overall, we detected 3898 SRW calls from which 1427 were used for
repertoire characterization. Calls were categorized in 7 call classes: upcall, downcall, downupcall, tonal constant, tonal variable, hybrid and pulsive calls. Spectrographic representation of
all call classes are shown in Fig. 3.
30
A
B
C
D
E
F
31
G
FIG 2. Spectrogram of call classes: (A) upcall, (B) downcall, (C) tonal variable, (D) constant, (E)
pulsive, (F) hybrid and (G) sequence of down-upcalls. Arrows in F shows pulsive components in hybrid
call. Spectrograms calculated with 1024 (A-D and G) and 512 (E and F) FFT points in Hamming
window, overlap 50%. Note differences in frequency and time scales between representations.
Upcalls, stereotyped tonal sweeps with ascending contour (Fig. 3 - A), were the most
frequent vocalization representing 56 % of calls. Other 13% of calls were classified as
downcalls (Fig. 3 – B), stereotyped tonal sweeps with descending contour. The down-upcall
category, which embraced tonal v-shaped calls (Fig. 3 – G), represented 12% of vocalizations.
Upcalls, downcalls and down-upcalls were frequently found in bouts.
Tonal calls with very little frequency modulation were categorized as tonal constant and
represented 10% of calls (Fig.3 - D). Hybrid (Fig. 3 -F), calls with both pulsive and tonal
components, and tonal variable calls (Fig.3 - C), tonal sounds with variable contour and
frequency modulation, were almost 2% and 7% of calls. Pulsive vocalizations (noisy, growllike sounds) were the rarest accounting for less than 1% of calls (Fig. 3 – E). Pulsive and hybrid
calls were found concentrated among other call types in periods of higher vocal activity.
Gunshots and warbles – a vocalization previously described by Parks and Tyack (2005) for
NARW - were not detected.
32
Summarized descriptive statistics (mean±standard deviation, range and median) of
acoustic features by call class are show in Table I. Values of parameters reported for other right
whale populations and repertoire comparison results are shown in Table II.
IV.DISCUSSION
Studies have been investigating the vocal behaviour of right whales’ surface-active
groups (SAG) but less is known about the repertoire of mother-calf pairs (Kraus and Hatch,
2001; Parks and Tyack, 2005; Trygonis et al., 2013). When comparing vocal activity of m/c
pairs and SAGs, some variance in the relative proportion of recorded calls is expected due to
differences in groups´ behaviour and in the ecological significance of certain call types. Upcalls
were the most frequent call type detected in SRW wintering grounds off Brazil as well as
NARW wintering areas (Soldevilla et al., 2014) but not in SAG focal studies (Parks and Tyack,
2005; Trygonis et al., 2013). The upcall may be used to announce presence of one individual
to others and for contact maintenance (Clark, 1983; Parks and Tyack, 2005). During SAG
activities, upcalls are produced by males approaching the group or when the focal female is
diving or leaving (Parks and Tyack, 2005). The use of upcalls by mother-calf pairs may serve
for intra and/or inter-pair communication as a signal of contact maintenance/avoidance.
Gunshots and moans were the most common calls detected in SAG focal studies (Parks
and Tyack, 2005; Trygonis et al., 2013). Gunshots are intense, brief, broadband sounds that
most likely function as sexual advertisement and/or agonistic signals (Parks et al., 2005; Parks
and Tyack, 2005). Gunshots were most frequently recorded in the presence of males however,
sex bias in gunshot production is not yet clear (Clark, 1983; Parks et al., 2005). No gunshots
were detected on the manually scrutinized recordings from Santa Catarina indicating that such
signal may have little importance in mother-calf pair communication. Consequently, our results
favour the hypothesis that gunshots are male sexual advertisement signals. Nevertheless, Clark
33
(1983) observed the production of a gunshot when an adult male approached a female with calf.
Gerstein et al. (2014) also provided evidence for gunshot production by a female right whale
with a calf. Thus, the hypothesis that females may produce gunshots as agonistic signals cannot
be discarded.
Down-upcalls were previously described as part of North Pacific Right whale
(Eubalaena glacialis) repertoire and may have been put together under “upcall” in NARW
studies (McDonald and Moore, 2002). This may also be case for SRW down-upcalls, as no
previous record of such call type was found in repertoire descriptions of populations from the
Southwest Atlantic. Despite differences in categories set to classify calls, all vocalizations
described for SRW in Brazil are similar to sounds described by Clark, 1983.
Upcalls from Brazil presented the lowest mean start, end frequencies, narrower mean
bandwidth and shorter mean duration next to other Southwest (from Argentina and Uruguay)
and Northern populations, However, only upcall duration differed significantly among
comparisons. Start frequency of upcalls from Brazil was also statistically different from North
Atlantic Right whales reported by Trygonis et al. 2013. Median values of start and end
frequency and duration of upcalls from SRW from Brazil are lower and shorter than upcalls
from North Pacific Right whale (Eubalaena japonica). Such differences in acoustics features
of upcalls from different right whale populations may be related to environmental features as
noise and sound propagation proprieties, or differences in group composition, behaviour, and
species (Clark, 1983; Parks and Tyack, 2005, Parks et al. 2007, Soldevilla et al. 2014).
V. CONCLUSION
Although PAM is a suitable method to monitor and investigate right whales, it is hardly
used off Brazil. One of the factors contributing to the under use of PAM may be the lack of
baseline information on the sound production behaviour of SRW. This study is the first aiming
34
to describe sounds produced by E. australis in the state of Santa Catarina, filling an important
gap on the knowledge about right whales off Brazil. Calls were classified in 7 classes: upcall,
downcall, down-upcall, tonal constant, tonal variable, pulsive and hybrid. Mean values of
acoustic features were reported. Start and end frequency, frequency bandwidth and duration
from upcalls recored off Brazil were shown to be lower, narrower and shorter than those from
other right whale populations, but only duration was significantly shorter. This repertoire
characterization will contribute to magnify the use of passive acoustic monitoring as a
conservation and research tool for SRW at an important wintering ground in the Southwest
Atlantic.
35
VI. ACKOWLEDGMENTS
Funding for fieldwork was provided by the Office of Naval Research to SEP (grant number:
N00014-08-1-0967). Licence for data collection at Right Whale EPA was granted to KG. through
SISBIO number 29774-1. CNPq provided a Scientific Expedition authorization to S.P. and a
Masters scholarship to JD. We acknowledge all people that collaborated with us in order to make
this research possible. Thanks to Marcos Brito for assistance with data processing and Renan
Lopes Paitach for confection of the study area map. We are also grateful for Chris Clark, Artur
Andriolo and Maria Luisa´s comments on early drafts of our manuscript.
36
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42
TABLE I. Call classes, number of calls per class and descriptive statistics (mean±SD, range and median) of acoustic parameters measured from fundamental frequency of SRW
vocalizations
Call Class
(n)
Descriptive
Statistics
Maximum
Frequency (Hz)
Minimum
Frequency (Hz)
Start
Frequency (Hz)
End
Frequency (Hz)
Peak
Frequency (Hz)
Frequency
Bandwidth (Hz)
Duration (s)
Upcall
(n=796)
Mean±SD
Range
Median
144±38
80-443
138
65±22
22-295
58
65±22
22-295
58
144±38
81-444
138
101±97
47-313
116
78±35
26-393
71
0.6±0.2
0.2-2
0.6
Downcall
(n=184)
Mean±SD
Range
Median
163±66
81-648
150
100±57
23-558
92
163±66
81-648
150
100±57
24-558
92
128±61
63-633
117
63±25
17-190
58
0.6±0.2
0.2-2
0.6
Down-upcall
(n=176)
Mean±SD
Range
Median
155±40
79-295
154
87±22
35-203
85
125±33
44-248
133
127±36
35-267
130
119±25
63-273
117
67±22
33-179
65
0.7±0.2
0.2-1
0.8
Tonal Constant
(n=144)
Mean±SD
Range
Median
116±28
68-279
107
84±23
37-172
66
89±28
42-193
84
90±31
42-188
85
96±24
55-188
85
41±15
14-186
39
1.5±1.0
0.3-6
1
Tonal Variable
(n=95)
Mean±SD
Range
Median
163±73
83-483
149
84±32
39-296
76
117±49
49-312
110
117±49
12-345
115
101±25
47-313
97
78±65
34-417
63
1.5±1.2
0.4-6
1
Hybrid
(n=23)
Mean±SD
Range
Median
238±72
106-413
232
61±30
43-141
80
179±57
63-280
187
194±55
78-284
203
127±32
70-219
125
158±66
52-331
141
1.8±1.9
0.7-8
1
Pulsive
(n=9)
Mean±SD
Range
Median
230±69
165-367
196
61±22
36-117
56
115±44
70-200
104
132±83
78-328
93
105±28
78-141
85
168±77
48-295
149
0.9±0.4
0.4-2
0.8
43
TABLE II. Mean±SD
extracted from upcalls of SRW from Brazil (our study), Argentina,
Uruguay, North Atlantic Right whales and North Pacific Right whales (previous studies).
Reported p values correspond to t test performed to compare acoustic variables values from
Brazil to other populations: italic, bold numbers means that averages (Brazil x other) are
statistically different.
Start
End
Frequency
Frequency
frequency
Bandwidth
(Hz)
(Hz)
(Hz)
78±15
156±29
86±23
0.82±0.23
p=0.565
p=0.756
p=0.842
p=0.027
Tellechea and
70±9*
173±8*
not reported
1.4±0.27*
Norbis, 2012
p=0.863
p=0.450
Parks et al. 2007
101±22
195±38
100±37
1.49±0.42
p=0.109
p=0.184
p=0.551
p=0.027
Trygonis et al.
120±22
214±44
not reported
1.49±0.42
2013
p=0.014
p=0,068
North Pacific***
McDonald and
89±34.7
153±26.7
(n=436)
Moore, 2002
-
-
Brazil (n=796)
Our study
65±22
144±38
Location/population
Argentina**(n=78)
Uruguay (n=11)
North Atlantic (n=929)
North Atlantic (n=49)
Reference
Parks et al. 2007
Duration (s)
p=0.028
p=0.029
not reported
0.7±0.27
-
78±35
0.6±0.2
*calculated based on data available on Tellechea and Norbis, 2012.
**data from 2000-2004 for NARW and from 2000 for SRW.
*** Median values.
44
ARTIGO 2
Emissão de upcalls por pares mãe-filhote Eubalaena australis no Brazil é independente do
período de incidência luminosa.
Autores:
do Norte.
ICMBio.
Nota a ser submetida a Marine Mammal Science (QUALIS: B1)
45
Eubalaena australis mother-calf pairs’ upcall production is independent of diel period in
Brazil
JULIA R. G. DOMBROSKI1, Graduation Program in Psychobiology, Laboratory of
Bioacoustics, Department of Physiology, Federal University of Rio Grande do Norte, Natal
59078-970 RN, C.P.1511, Brazil; SUSAN E. PARKS, Department of Biology, Syracuse
University, 114 Life Sciences Complex, Syracuse NY 13244, U.S.A; KARINA R. GROCH,
Projeto Baleia Franca, Av. Atlântica, Imbituba 88780-000 SC, C.P.201, Brazil; PAULO A. C.
FLORES, Centro Mamíferos Aquáticos, Instituto Chico Mendes para Conservação da
Biodiversidade, Rod. Maurício Sirosky Sobrinho, km 02, Florianópolis 88.053-700 SC, Brazil;
RENATA S. SOUSA-LIMA, Laboratory of Bioacoustics, Department of Physiology, Federal
University of Rio Grande do Norte, Natal 59078-970 RN, C.P.1511, Brazil and Bioacoustics
Research Program, Laboratory of Ornithology, Cornell University, 159 Sapsucker Woods
Road, Ithaca, New York 14850, U.S.A.
1
Corresponding author (email: [email protected])
46
Patterns in signal production may provide insight into vital aspects of a species’
behavior (Bradbury and Vehrencamp 1998). Temporal patterns in vocal behavior have been
reported for some baleen whale species; humpbacks (e.g. Au et al. 2000, Sousa-Lima and Clark
2008) minke (e.g. Risch et al. 2013); and right whales (e.g Matthews et al. 2014) and have
provided important clues to determine the factors influencing the evolution of communicative
behavior in different life stages. The objective of the present study was to investigate diel trends
in Southern right whale (Eubalaena australis) calling behavior off a wintering area in Brazil.
Right whales (Eubalaena sp.) are known for using low frequency vocalizations (usually
under 1000 Hz) for communication (Clark 1983, Parks and Tyack 2005). Their repertoire
consists of several call classes (Clark 1982). Among these call types, there is a stereotyped
upsweep, the upcall, used in different behavioral contexts for contact maintenance between
individuals (Clark 1983, Parks and Tyack 2005). Therefore, the upcall is also referred as the
contact call (Clark 1983) and is frequently used as a detection target in passive acoustic
monitoring situations (Van Parijs et al. 2009).
To date, three right whale species were recognized (Rosenbaum et al. 2000): Eubalaena
japonica, the North Pacific right whale (NPRW); Eubalaena glacialis, the North Atlantic right
whale (NARW) and Eubalaena australis, the Southern right whale (SRW). Right whales, as
observed in other baleen whale species, migrate to lower latitude regions in the colder months
of the year searching for better conditions to reproduce and calve (Lockyer and Brown 1981).
During spring and summer months, they migrate back to higher latitude areas for feeding
(Lockyer and Brown 1981). SRW wintering areas are distributed along coastal regions in the
Indian, South Pacific and South Atlantic Oceans (IWC 2012). In the Southwest Atlantic, an
important wintering area for SRW is found off Brazil (IWC 2012).
From July to November, one population of SRW concentrates in the southern part of
Brazil, mainly off the state of Santa Catarina (Groch et al. 2005). Key aggregation sites –
47
between Imbituba (28°12’S, 48°49’W) and Santa Marta Cape (28°33’S, 48°47’W) – are
characterized by a large number of bays and shallow waters (depth < 30m) where the shelf
break is closer to shore (Groch et al. 2005, Espírito Santo et al. 2013). Due to the importance
of the area for the species, the Brazilian government created the Right Whale Environment
Protection Area (Right Whale EPA), a federal conservation unit where exploitation and use of
the coastal environment is regulated in order to protect wintering whales (Brasil 2000).
Nevertheless, local right whales are still exposed to commercial shipping traffic, risk of
entanglement in gillnets and potential disturbances caused by whale-watching activities (Ott et
al. 2008, Rocha-Campos & Camara 2011). Thus, despite the IUCN status of “least concern”
species (Reilly et al. 2013), SWR is listed as “endangered” in the List of Brazilian Threatened
Fauna (Machado et al. 2005).
Survivorship of young is crucial for populations’ long-term viability (Whitehead and
Mann 2000). Female right whales provide all parental care, from conception to weaning. Hence,
investigating mother-calf behavioral dynamics is fundamental to understanding the biology and
behavior of right whales (Whitehead and Mann 2000). Crucial information obtained in
wintering areas around the globe may be applied to have better risk assessment and to aid in
the protection mother-calf pairs of any right whale population. The wintering area off Brazil
provides exceptional conditions for the study of mother-calf pair´s behavior and
communication. Based upon aerial surveys conducted between the central part of the state of
Santa Catarina and Rio Grande do Sul since 2002, from mid-October to November, 100% of
whale group sightings are identified as mother-calf pairs (Groch et al. unpublished data). Such
unique conditions allow dedicated studies of mother-calf pairs´ biology and behavior to be
conducted with minimal influence of juveniles, or other adult whales.
Aiming to investigate the vocal behavior of SRW mother-calf pairs, fixed archival
autonomous recording units were deployed in October 15 of 2011 at Gamboa beach (27º57'S,
48
48º37'W) for 14 days (Fig.1). The DSG Ocean devices (Loggerhead Instruments) were set to
continuously sample in a rate of 8 kHz and 16-bit resolution. Each DSG unit was equipped with
HTI-96 MIN hydrophones with sensitivity = -240 dB re 1V μPa-1 between 2 Hz and 30 kHz.
The frequency response of the recording system (+/- 1 dB 20 Hz – 3.3 kHz) covered the
fundamental frequency of all known right whale calls. Recordings were subjected to an
automated detection tool developed for detection of NARW vocalizations (Urazghildiiev and
Clark 2006, Urazghildiiev et al. 2009). In this study, trends in production of the upcall was used
as a proxy for overall vocal activity. Therefore, only upcalls were considered for our analysis.
False positives were manually withdrawn from the dataset. In order to improve detection
efficiency (Rocha et al. 2015; Dombroski et al. 2015), one-minute segments before and after
each detection event were hand browsed for missed upcalls using XBAT (Figueroa 2007).
Days of uninterrupted sampling were divided in 4 diel periods according to the sun
altitude angle in relation to the horizon: Dawn, Day, Dusk and Night (Munger et al. 2008).
Dawn was defined by sun altitude between -12° and 0°, which corresponds to the beginning of
nautical twilight until sunrise. Day was the period between sunrise and sunset when sun altitude
was >0°. Dusk was defined by the period where sun altitude was between -12° and 0° followed
by sunset. Night periods were defined as hours of darkness in which sun altitude was <-12° to
the horizon. Hourly altitude angle of the sun for Gamboa (27º57'S, 48º37'W) was obtained at
the United States Naval Observatory website (http://aa.usno.navy.mil/data).
Calling rates (upcalls/hr) were calculated within diel periods by dividing the total
number of detected calls in a given period by the period duration (Munger et al. 2008). To
correct for variation in the number of detected calls in each day, mean-adjusted calling rates
were computed by subtracting the daily calling rate from the calling rate of each diel period of
that same day (Munger et al. 2008). As data was divided in heteroscedastic groups (Levene’s
test=11.6; df1=3; df2=40; P<0.001), the Kruskal-Wallis test was used to verify the null
49
hypothesis that the mean ranks of adjusted calling rates across periods were the same. Statistical
tests were done using SPSS software (IBM Statistics).
Overall, 3,712 right whale upcalls were detected in 264 hours of continuous recordings.
Statistical results indicates no significant diel pattern in the detection of contact calls (KruskalWallis test chi-square=5.8, df=3, P=0.1). Mean rank of adjusted calling rates for Dawn, Day,
Dusk and Night were 14.5, 23.9, 26.5 and 25.0 respectively. Median and mean values for
adjusted calling rates in each diel period are shown in Table 1. Distribution of calling rate
throughout a 24 hour period is shown in Figure 2. Hourly distribution of the median calling rate
is shown in Figure 3.
Previous studies reported significant trends in upcalling behavior of right whales in
foraging grounds in the North Atlantic: Morano et al. (2012) and Matthews et al. (2014)
reported higher calling rates during the night while Mellinger et al. (2007) and Mussoline et al.
(2012) reported greater calling activity during the day and during twilight, respectively. For
North Pacific right whales, Munger et al. (2008) reported a significant diel trend with increased
calling rates at night. Similarly, on the wintering grounds, higher calling activity during the
night were reported in NARW (Soldevilla et al. 2014, Bort et al. 2015) and in Southern right
whales off Argentina (Clark 1983).
As main group composition and behavior varies between feeding and wintering areas,
differences in temporal patterns in calling behavior may be expected. In feeding areas, calling
patterns may be explained by the negative correlation between foraging behavior and vocal
activity (Parks et al. 2011, Morano et al. 2012, Matthews et al. 2014). In wintering areas,
foraging behavior is infrequent; consequently, it is unfeasible to link vocal and feeding
behavior. A more reasonable explanation for increased calling rates during dark periods would
be the greater use of acoustic communicative signals over less effective alternative cues when
light is absent (Soldevilla et al. 2014, Bort et al. 2015). As visual monitoring of whale groups
50
in periods of darkness is hardly possible, increased calling rates at night could also mean
increased number of vocal active whales under the hydrophones’ detection range in both
wintering and feeding areas (Mellinger et al. 2007, Munger et al. 2008).
Temporal patterns in calling behavior may be related to site-specific characteristics
(Mellinger et al. 2007) and, according to our study, it may be linked to the predominant
behavioral state of whale groups. During calf development, distinct mother-calf behavioral
patterns may be observed in wintering grounds (Taber and Thomas 1982, Thomas and Taber
1984, Cartwright and Sullivan 2009). Right after the calf’s birth, the pair is more likely to spend
most of its time slowly traveling in close proximity. As the calf grows older, its activity level
increases and it spends more time playing around its resting mother. By the end of season, prior
to the pair´s desertion to migration, the behavior is generally characterized by low activity levels
and by female and calf spending great amounts of time in close proximity, within ¼-whale
length from each other. The calf spends much less time playing and the pair spends more time
traveling, likely in preparation for migration (Taber and Thomas 1982, Thomas and Taber
1984).
Individual calves actively maintain physical closeness to their mothers as they near the
departure date from the wintering grounds (Thomas and Taber 1984).
Traveling in close
proximity is the predominant behavior state of mother-calf pairs throughout a 24-hour period
near the end of the winter season (Thomas and Taber 1984) invariable calling activity within
pairs is expected if calls are necessary to remain in contact. Our results support this hypothesis
that there is selective pressure for frequent acoustic signaling between mother and calf to ensure
maintenance of close proximity during the period of this study that coincides with the final
weeks of the wintering season. Given the short duration of our recorder deployment, our study
is not able to provide evidence about variations in the temporal pattern of calling behavior
during early and mid-season when different predominant behavioral states are expected, and
51
future recordings are necessary to further test the hypothesis that increased acoustic activity
occurs shortly before departure from the wintering grounds.
The vocal pattern detected in our study may reflect the calling pattern throughout the
entire season. In this scenario, constant need of contact maintenance between mother-calf could
be related to bounds of parental care and calf dependence of lactation to feeding during the
complete wintering season (Whitehead and Mann 2000). Increased calling rates of mother-calf
pairs are observed during interaction events with other whales in the environment, in reunion
events of female and calf or encounters with other groups. Punctual variations in median
adjusted calling rates (call/hr) may indicate occurrence of such events or other situations that
may favour greater vocal activity. Increased upcall detection may indicate increment on the
number of vocally active animals under the detection range of our recording system (Mellinger
et al. 2007, Munger et al. 2008). Nevertheless, visual monitoring of whale groups were not
possible and therefore any conclusion about whale´s density would be unrealistic.
Our results suggest that the vocal activity of southern right whale mother-calf pairs do
not vary significantly accordingly to diel periods and that predominant behavioral state may be
related to vocal temporal patterns in wintering grounds. Other features that were not
investigated in this study may reveal temporal patterns in vocal behavior of right whales. Tide
variations, moon phase and boat traffic and noise are among factors that may influence vocal
activity of whales (Sousa Lima and Clark 2007) and may potentially to be related to temporal
patterns of calling behavior. To confirm our findings and to further investigate time-based
patterns of vocal behavior, long-term acoustic monitoring of the right whale wintering area off
Brazil is required. Future studies of vocal patterns should also consider variation in behavioral
patterns all through the whale´s stay in a given area, especially when focusing on mother-calf
pair dynamics. The investigation of behavior and communication of this sub-group of
52
individuals with specific protocols and approaches is critical to propose effective protection
measures and therefore, to the conservation of all right whale populations.
53
Acknowledgements
We are grateful for the valuable comments of Artur Andriolo and Maria Luisa da Silva that
helped us to improve this manuscript. We also would like to acknowledge Ildar R.
Urazghildiiev for assistance with the detection tool, Fúlvio A. M. Freire for suggestions on
statistical methods and Renan Paitach for confection of map. Scientific Expedition
authorization was provided by Conselho Nacional de Desenvolvimento Cientifico e
Tecnológico (CNPq) to SEP. We also would like to thank CNPq and the Graduation Program
in Psychobiology for JD´s masters scholarship. The Office of Naval Research provided funding
for fieldwork (grant n: N00014-08-1-0967). License for data collection at Right Whale EPA
was granted to Karina R. Groch through SISBIO number 29774-1.
54
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59
Figures
Figure 1. Map of the study area. The Right Whale Environment Protected Area (EPA) extends from the
south of Florianópolis Island to Rincão. Main SRW aggregation areas are between Imbituba and Santa
Marta Cape. Adjacent to the whale´s key aggregation area, the Imbituba harbor concentrates commercial
shipping traffic in the area. The archival recording device was deployed at Gamboa beach.
60
Figure 2. Adjusted calling rate (upcall/hr) was not statistically different throughout diel periods. Color
bar corresponds to light regime within each diel period: Dawn and Dusk (gray), Day (white) and Night
(black).
61
Figure 3. Hourly distribution of median calling rates (upcall/hr). The inner circle shows hours of the
day. The black dotted line links the median calling rates in each hour. Outer circle shows light regime
in each diel period: Night (black), Dawn and Dusk (gray) and Day (white). Statistical tests revealed no
significant variation of calling rates throughout diel periods.
62
Table
Table 1.Mean (xˉ ±SD) and median of adjusted calling rates (upcall/hs) for each diel period.
Diel Period
Mean
Median
Dawn
(n=11)
7.4±12.6
-7.8
Day
(n=11)
0.6±4.5
-1.3
Dusk
(n=11)
16.0±31.2
9.9
Night
(n=11)
0.02±6.5
1.4
63
ARTIGO 3
Contexto comportamental das vocalizações de pares mãe-filhote de baleia franca austral
(Eubalaena asutralis)
Autores:
do Norte.
ICMBio.
Artigo a ser submetido a Bioacoustics (QUALIS: A2)
64
RESUMO
Por meio de gravações acústicas e observações comportamentais sincrônicas, conduzimos um
estudo dedicado exclusivamente a pares mãe-filhote, com o objetivo de: discutir o uso de
diferentes tipos de chamados de acordo com o contexto comportamental; e obter taxas de
produção de som de acordo com o estado comportamental. O comportamento dos pares foi
continuamente amostrado seguindo metodologia de grupo-focal. Gravações acústicas foram
realizadas usando um arranjo linear de hidrofones. Ângulos correspondentes a fonte sonora
foram estimados por meio da função “beamforming” do software Raven Pro. Upcalls e
chamados v foram atribuídos a pares em descanso e em deslocamento. Chamados tonais
constantes foram detectados quando um par se deslocou em direção a embarcação de pesquisa.
Chamados pulsados foram emitidos por um par em deslocamento na presença de golfinhos
nariz-de-garrafa. Pares mãe-filhote passaram 20% do tempo total de observação interagindo
com outros pares e a maior diversidade de chamados foi captada durante estas interações.
Chamados pulsados (12%) e híbridos (13% - gravados exclusivamente durantes os eventos de
interação entre pares) são característicos de relações agonísticas entre baleias. Quando mãe e
filhote estavam interagindo entre si, apenas upcalls foram captados. Nenhum chamado foi
atribuído a pares em mergulho ou amamentando. A taxa de emissão de chamados
(chamados/minuto) está associada ao nível de atividade do par, sendo maior durante interações
entre os pares e entre mãe e filhote, e menor enquanto os animais estavam em descanso ou em
deslocamento. Quando comparadas a grupos ativos de superfície, as taxas de vocalização de
pares mãe-filhote são baixas o que sugere o uso de outras modalidades de sinal para a
comunicação de curto-alcance. As baixas taxas de vocalização podem também estar associadas
a estratégias relacionadas a prevenção de detecção por predadores e/ou por outros grupos de
baleias.
65
Behavioural context of southern right whale (Eubalaena australis) mother-calf vocalizations.
Julia R. G. Dombroski1, Paulo A. C. Flores2, Karina R. Groch3, Susan E. Parks4 and Renata S.
Sousa-Lima 1,5.
1
Graduation Program in Psychobiology, Laboratory of Bioacoustics, Department of
Physiology, Federal University of Rio Grande do Norte, University Campus, Natal, RN
59078-970, Brazil. E-mail [email protected];
2
Centro Nacional de Pesquisa e Conservacão de Mamíferos Aquáticos, ICMBio, MMA,
Jurerê, Florianopolis, SC, 88053-700, Brazil;
3
Projeto Baleia Franca (Right Whale Project), P. O Box 201, Imbituba, SC 88780-000,
Brazil;
4
Parks Lab, Department of Biology, Syracuse University, 107 College Place, Syracuse, New
York 13244, United States;
5
Bioacoustics Research Program, Cornell Laboratory of Ornithology, 159 Sapsucker Woods
Road, Ithaca, New York 14850, United States.
Running title: Vocalizations and behaviour of right whales.
66
ABSTRACT: Using synched surface-behavioral observations and acoustic recordings, we
conducted a dedicated study of mother-calf pairs (mo/ca) to discuss the association between the
use of call classes and the pair’s behavioral state, and to obtain sound production rates in
different behavioral contexts. Behavior was continuously sampled through group-focal
observations. Acoustic recordings were done using a two-element linear array. Sound files were
hand browsed for right whale calls. Bearing angles of sound sources were estimated using the
Beamforming function in Raven Pro Software. Upcalls and v-shapped calls were attributed to
resting and traveling pairs. Tonal constant calls were detected when a pair was swimming
toward the research boat and pulsive calls were detected in the presence of dolphins in close
proximity to the focal group. Mother-calf pairs spend 20% of the sampling time interacting with
other pairs and the greatest diversity of calls was recorded during such events. Pulsive (12%)
and hybrid calls (13% - exclusively recorded during mo/ca interactions) are characteristics of
agonistic behavior between whales. When bonding, mother and/or calves produced exclusively
upcalls. No calls were attributed to diving or nursing pairs. Calling rate (call/min) was
associated with the activity level of mo/ca pairs, greater in interactions and bonding and lower
during travelling and resting. When compared to surface active groups, the calling rate of mo/ca
pairs was lower suggesting the use of other signal modalities for close range communication.
Low calling rates may also be related to avoidance of detection by predators and/or other whale
groups.
KEYWORDS: acoustic ecology; female-calf pair, right whale, sound production, calling
behavior.
67
INTRODUCTION
The use of sounds for communication is long recognised in cetaceans (Tyack 2000).
Species produce a wide collection of acoustic signals: from tonal to pulsive, with simple to
complex frequency and/or amplitude modulation, narrow to broadband, brief to long (Tyack
2000). Baleen whales are known to produce a variety of discrete low frequency calls of variable
nature and/or songs (Payne & Webb, 1971, Payne & McVay 1971). As a consequence of such
miscellany of sounds, studies describing physical features of species’ acoustic repertoires were
performed throughout the years at least for the most accessible ones (Cummings & Thompson,
1971, Payne & McVay 1971, Payne & Payne 1971, Cummings et al. 1972). Descriptive work
is essential for the characterization and categorization purposes and constitutes the foundation
for investigating acoustic communication systems. However, what those kinds of studies alone
reveal about biological significance and informational content of acoustics signals is limited
(Bradbury & Vehrencamp, 1998). To infer the nature of the message being transmitted, it is
crucial to analyse acoustic signals within behavioural contexts in which sounds are originally
produced (Clark 1980, 1983).
Remote passive acoustic sensing is increasingly being used as a management,
conservation and research tool of marine mammal species (Van Parijs et al. 2009).
Nevertheless, its efficiency and success are highly dependable of understanding the natural
variations in sound production behaviour of the target species (Mellinger et al. 2007, Van Parijs
et al. 2009, Sousa-Lima et al. 2013). As vocal behaviour may be affected by group composition
and behavioural state, assessing site and species-specific calling rates and behavioural contexts
of sound production is crucial to correctly interpreter PAM data (Mellinger et al. 2007, Van
Parijs et al. 2009). Together with signal function data, this kind of information is obtained from
synchronic behavioural observations and acoustic recordings.
68
Detailed behavioural observations of cetaceans are challenging even for the largest
species (Mann 2000). Observations of underwater behaviour are hardly achievable - for an
exception see Miles & Herzing (2003). Consequently, only the animal’s surface behaviour is
taken into consideration (Mann 2000). To relate vocalizations with behaviour is even more
puzzling since sound production is more likely to occur underwater making it difficult to
identify the sound source (Clark 1982, Parks & Tyack 2005). Still, by implementing
troubleshooting approaches, vocalizations and its related behaviour were examined for some
free-ranging delphinids as orcas (Miller & Tyack 1998), bottlenose dolphins (Herzing 1996)
and pilot whales (Weilgart & Whitehead 1990) and baleen whale as fin (Croll et al. 2002), mink
(Gedamke et al. 2001), blue (Oleson et al. 2007), humpback (Zoidis et al. 2008) and right
whales (Clark 1983, Parks & Tyack 2005).
The right whale vocal repertoire is a graded assortment of low frequency tonal calls and
broader-band sounds (Clark 1983, Parks & Tyack 2005). By performing playback experiments,
Clark (1982) has proven that right whales are able to distinguish the species vocalizations from
other whale species’ calls reinforcing the importance of acoustic signals to intra-specific
communication. Studies of synchronic behavioural observations and acoustic recordings
already allowed researchers to deduce the biological significance of some right whale calls. For
instance: the upcall is the right whale contact call, a signal for contact maintenance (Clark
1983); in surface-active groups (SAGs), scream calls - general call category incorporating high,
hybrid and pulsive calls – are most likely produced by females (Parks & Tyack, 2005); gunshots
are stereotyped sounds which ecological function in SAGs is related to agonistic interactions
and/or sexual advertisement (Parks et al. 2005a, Parks et al. 2005b).
In right whales, as in other misticeti, females are responsible for all parental investment
in the offspring - e.g protection, nourishment, nurturing social skills (Whitehead & Mann 2000).
Every calf represents a great part of the reproductive success of the female: motherhood is
69
extremely costly as maternal investment is enormous and the species reproductive rate is low
(Kraus et al. 2001, Kraus & Hatch 2001). Before weaning, calves are highly attached and
dependent of their mothers (Whitehead & Mann 2000). Communicative mechanisms by which
the relationship between a female and its calf is mediated and the vocalization dynamics of
mother-calf pairs are unknown in detail. Nevertheless, due to the importance of this subgroup
to the population survivorship, such knowledge is vital in order to better understand the
communication system and protect all right whale species (Soldevilla et al. 2014). Therefore,
this study seeks to determine the sound production rate and discuss the use of different call
types by southern right whales mother-calf pairs in accordingly to behavioural contexts.
MATERIALS AND METHODS
Study population and area
During the austral winter, part of the right whale (Eubalaena australis) population of
the Southwest Atlantic migrates from feeding grounds to southern Brazil and from July to
November and aggregates off Santa Catarina, particularly between Imbituba (28°12’S,
48°49’W) and Santa Marta Cape (28°33’S, 48°47’W) (Groch et al. 2005, IWC 2007). Whale
groups, especially mother-calf pairs are usually distributed in clusters along the shallow-water
sandy-bottom bays that characterizes the area (Espírito Santo et al. 2013). Females show
elevated site fidelity and return to the area in average, every 3 years (Groch &Flores 2011).
After almost being hunted to extinction, latest reports have shown that the Brazilian
population is recovering (Groch et al. 2005). However, right whales are threatened by
increasing commercial ship traffic, entanglement in fishing gear, whale-watching activities and
deterioration of the marine environment (CMA, 2009). In 2000, the Brazilian government
created the Right Whale Protected Area (Right Whale APA), a federal conservation unit that
covers 130km of coast, from Santa Catarina Island to Rincão, with 156 thousand hectares
70
(Brasil 2000) (Figure 1). The APA embraces sites of highest whale sights and is aimed to
regulate activities that are potentially deleterious to whales and their environment. Data
collection was undertaken at the Right Whale APA in late wintering season. Surveys were
conducted in 5 days of October (17, 18, 19, 25 and 29) and 3 days of November (05, 13 and
14) 2013. Licence for data acquisition was granted to J.D. (SISBIO number 41162-1).
Behaviour observations and acoustic recordings
Synchronous behavioural observation and acoustics recordings of southern right whale
mother-calf pairs were performed from a fast-boat, wooden diving trawler or zodiac. The type
of vessel used in surveys varied according to daily availability from collaborators. Whale pairs
were
carefully
approached
and
observations/recordings
started
immediately
after
environmental condition assessment and after the engine turned off. Maximum distance to start
observations/recordings was 400 meters. If there was more than one pair that could potentially
be recorded within sight, we selected the one to be approached located as far as possible from
other whale group(s) and from the wave break zone. In some occasions, land-based team
provided information about the whales’ position. Whenever a group got too close to the vessel
or if the boat drifted away from the group, behavioural and sound recordings were interrupted
and, whenever possible, the boat was relocated.
Behavioural methodology
Mother-calf pairs’ behaviour was continuously sampled through group-focal
observations (Martin & Bateson 2007). Group composition was determined by visual
observations of individual body sizes. Mother-calf pairs were groups composed by two
individuals, always in pairs: one clearly adult and the other calf with about ½ or less body length
of the adult. The adult individual was assumed a female. Behavioural states were addressed to
71
the group and were divided in travelling, resting, bonding, socializing, nursing and diving
(Clark 1983, Thomas & Taber 1984, Thomas 1986, Cassini & Vila 1990).

Travelling: directional forward movement that resulted in significant change of
location.

Resting: motionless state with no evidence of physical extortion unless minor
movements for breathing or drifting.

Bonding: mother and/or calf exhibiting movements and actions toward each
other as turns, contacts and semi-immersions.

Interacting: mother-calf pairs exhibiting movements and actions toward and in
close proximity with other pairs.

Nursing: nursing was assumed when the calf was parallel to its motionless
mother, diving at about ¾ of the adults’ body with

Diving: complete immersion of both individuals.
During interaction events, all pairs involved in the activity were considered the focal
group.
Acoustic methodology
Recordings were done using a linear array composed by two High Tech Inc. 96MIN
hydrophones (sensitivity -201dB re: 1V/μPa; frequency response 2Hz-30kHz) spaced by 5m,
plugged into a ZOOM H6 portable digital recorder (flat frequency response 2Hz-20kHz –
sampling at 44.1 kHz, 16bit-resolution). The array structure was made of PVC pipes covered
with thermal insulation and diving weights for ballast. The device was sustained on the water
column at 3-5m deep by a buoy set. Distance (m) between the group from the array central
point and bearing (degree) in relation to the array azimuth were taken using a laser range finder
72
and a waterproof compass, respectively. Every ten minutes or whenever the boat or whales
moved too much, angles and distance were taken.
Behaviour-acoustical analyses
Recordings were hand scrutinized for right whale calls using Raven Software version
1.4 (512 points FFT in Hamming Window respectively; 50% overlap). Calls were classified
according to Dombroski et al., (Article 1).
Aiming to find the sound source and thus to correctly relate behavioural observations
with the recorded calls, bearing angles were estimated using the Beamforming function in
Raven Pro Software version 1.4 (Charif et al. 2010). Bearing angle is established by time of
arrival differences of the target sounds between the array’s hydrophone units. Correspondence
between calls’ bearing angles and groups’ angles assessed during fieldwork indicated that the
observed group was the sound source (Clark 1980, Parks et al. 2005). If we find no match
between call and the focal group angle (admitting deviance of ±20°), it was assumed that those
data were not from the focal group and disregarded. Speed of sound was calculated based on
salinity and water temperature 1m below the surface for each day and water depth in each data
collection point. Each vocalization was saved in a different file and a low pass filter was applied
before beamforming (-60dB attenuation between 500 Hz and 22000Hz). Channels were
normalized due to possible gain imbalance between units. Reference bearing was set to 0
degrees as the array was always positioned perpendicularly to the focal group.
The use of each call class is discussed within behavioural states. Total count of each call
type was sorted by behavioural state to determine if call type usage can be associated to the
observed behavioural state by Pearson’s chi-square (bootstrapping - 2000 combinations) and
Fisher´s exact test. Calling rate (Call per minute - CPM) was calculated by dividing the total
73
number of calls produced in each behavioural state by the total time spent by all groups in that
state. All statistical tests were done using SPSS version 21 (IBM Statistics).
RESULTS
One hundred and two right whale calls were recorded during 542 minutes of behavioral
observations of 20 female-calf pairs (including resightings). Calls were classified into 6 classes
accordingly to visual and aural characteristics: upcall, downcall, vcall, constant, pulsive and
hybrid (Fig. 1). The most common calls were upcalls (59%) followed by downcalls (10%).
Most frequent behavioral states were travelling, resting and interacting representing
respectively 41%, 22% and 20% of the total sampling time as shown in table 1. Vocalizations
coming from groups travelling, resting, bonding and interacting were detected. However, no
calls were attributed to groups nursing or diving. Detected call classes and their proportions in
relation to the overall vocalizations in each behavioral state are shown in Table 2. Chi-square
test showed no association between call types and behavioral states (x2=19.06; df=15; p=0.37)
as well as Fisher´s exact test (14.82; p=0.21). CPM (call per minute) for each behavioral state
in which vocalizations were detected is presented in table 3.
DISCUSSION
Traveling
Distinct behavioral patterns during calf development in wintering areas present one
predominant behavioral state (Taber & Thomas 1982, Thomas & Taber 1984). Travelling is
frequent in the first days of life of the newborn, likely due to the lack of buoyancy of the calf,
and on the last days of the pairs’ stay in the wintering area, as a preparation for migration.
Travelling was the most frequent behavior observed during our study that coincided with the
final days of the pairs’ stay in Santa Catarina. The calf usually swims right next to the female,
74
which is attributed to hydrodynamic benefits of such position (Krasnova et al. 2006). During
this period when close proximity maintenance is crutial to the survival of the calf, it is expected
that whales frequently communicate using contact calls. Our results corroborate this hypothesis.
Alternatively, the upcall may serve as inter-pair communication, announcing a pair’s presence
and location to others while traveling.
Downcalls may have a similar adaptive function to upcalls, being also used as a contact
signal (Clark 1983). Our results showed that the downcall was the second most frequent call
class during travelling and its emission pattern was in bouts similar to upcalls.
All pulsive calls detected during travelling behavior were recorded in October 25 at
Ribanceira beach. Initially the focal pair was resting and no calls were attributed to them.
However, upcalls were heard in recordings, possibly coming from a group approximately 800m
away (angle difference between them >40). The presence of bottlenose dolphins (Tursiops
truncatus) in the area was acoustically detected and visually confirmed. The focal group started
travelling as the group in the vicinity started to swim in the same direction. Dolphins were seen
around the focal group (~100m from the pair) and followed them as they swan away. Several
pulsive calls were detected (13) in a series, but only 3 were attributed to the focal group by
sound source beam calculation. Pulsive calls are considered aggressive signals (Clark, 1983).
Thus, the focal group may have produced this calls due to the disturbing presence of dolphins
or/and the approach of the other whale group.
Constant calls were detected among upcalls and attributed to the focal group during a
single event when the calf swam towards the research zodiac followed by its mother on October
17 at Ribanceira beach. Despite recent evidence of females producing gunshots during
interactions with anthropogenic elements in the environment (Gerstein et al. 2014), such sound
was not detected in our recordings.
75
Resting
Towards the end of the wintering season, pairs are expected to save energy by assuming
low energy demanding behaviors (Taber & Thomas 1982, Thomas & Taber 1984). In our study,
the second most frequent behavioral state was resting which is coincides with the expectation
from the sampling period. While resting, right whales are most likely to produce discrete calls
as upcalls. During our observations of resting whales, upcalls and vcalls were used in the same
proportion indicating that perhaps the vcall has the same adaptative function as the upcall.
Nursing and Diving
No calls were attributed to diving and nursing pairs suggesting the use of alternative
cues for communication. During the observed nursing event, the mother was initially resting
while the calf was diving by its side. The calf positioned itself at about ¾ on the lower part of
the mother body and only the calf´s tailstock and fluke were visible from the surface.
Eventually, the calf was seen coming at the surface to breathe and quickly re-assumed his
underwater position. When another group was sighted about 200m away for our focal pair, the
mother dove, probably to interrupt the calf’s meal. No vocalizations were recorded from any of
the pairs. The secondary pair stopped their movement about 100 meters from the focal pair.
The focal pair silently moved away 400m from the secondary pair and rested. Observations and
recordings were then interrupted.
Bonding
Interactions between mothers and their calves may involve maternal behavior by the
female and/or begging by calves as well as playful behaviors (Sakai et al. 2013). During the
first stay of a right whale calf in the wintering area, the adult female is responsible for
maintaining its proximity to the calf, thus being responsible for the majority of approach
76
behaviors and therefore it is likely that she is also the responsible for the emission of contact
calls toward its calf (Taber & Thomas 1982, Thomas & Taber 1984). Alternatively, the calf
may be responsible for calling until the mother joins him (Sousa-Lima per comm 2015). Only
upcalls were attributed to the focal pair during interactions between a mother and its calf.
However, due to technical limitations of our array, identification of the vocalizing individual
was not possible. Future studies should focus on discriminating who is calling to better
understand the communication dynamics between mother and calves.
Interacting
Mother-calf pairs are frequently described as having a tendency to avoid other mothercalf pairs (Clark 1983, Whitehead & Mann 2000, Kraus & Hatch 2001, Hamilton & Cooper
2010). Interestingly, in 20% of the total sampling time of this study, whales were involved in
inter-pair interactions with up to three pairs displaying different kinds of active behavior
towards each other. Reasons for pairs to engage in such social events are not clear. However,
they may represent one aspect of the maternal care where the adult female is responsible for
nurturing social skills that will be necessary to the calf´s survivorship and reproductive success
(Whitehead & Mann 2000). In the case of right whales, such social interactions may be
important to the calf in learning how to behave when part of a SAG (Kraus & Hatch 2001).
Kidnapping behavior is not uncommon in odontocetes. In bottlenose dolphins, mothers
that failed in their reproductive attempts try to steal newborns from their biological mothers
(Mann & Smuts 1998). Therefore, mothers with newborn calves up to one-week old are known
to avoid other females until the calf is about two-weeks old, when it is expected to have learned
how to recognize its mother apart from other females (Mann & Smuts 1998). However,
kidnapping a calf may have high costs as the enormous energy investment and the agonistic
interactions with the calf´s biological mother (Mann & Smuts 1998). For a right whale female,
77
who already is a mother, having another o calf to nurse would have a gigantic energy cost which
would likely affect her and her calf’s chances of survivorship (Kraus et al. 2001, Kraus & Hatch
2001).
During pair-pair interactions, a resting pair is approached by other group. The approach
is not silent and upcalls are frequently heard. When groups join, females and calves are
observed exposing pectoral fins and heads. Fluke exposure, rolling and belly-up are also
behaviours displayed by females during such interactions, but not by calves. During
observations in November 13, a calf was observed opening its mouth 8 times in 21 minutes.
Perhaps this behaviour is related to the great level of activity observed what could have
increased the calf´s body temperature. Opening its mouth would allow water to come in helping
it decrease its internal temperature (Heyning 2001).
The greatest diversity of calls were recorded during these pair-pair interaction events.
Hybrid calls were exclusively recorded during such interactions and, along with pulsive calls,
are related to aggressiveness and disturbance, indicating that the interactions between pairs have
characteristics of agonistic behaviour (Clark 1983). Upcalls were detected throughout the
observations, presumably as means to maintain contact between mothers and their calves during
these potentially confusing situations. Neither visual nor acoustic identification of the original
groups (mothers and its respective calf) or individuals producing the calls were not possible
from the surface raising the question of how calves its mothers would mutually recognise each
other underwater.
As a species with such low reproductive rate, extended parental care and in which longrange communication takes place mainly through acoustic signals, vocal recognition between
right whale mother-calf pairs are expected to be an important mechanism to reunite the
individuals after accidental separations, specially in the wintering grounds, due to the clustered
distribution of pairs, and during the journey toward the feeding grounds (Sousa-Lima et al.
78
2002, Frasier et al. 2010). It is believed that the upcall may contain distinguishable individual
features. This call type is adapted to propagate through long ranges; it is produced by all whales
(males, females and from all age classes) and is known to vary in order to avoid overlap with
noise (Clark 1983, Parks et al. 2007, Parks et al. 2009, Van Parijs et al. 2009).
As described in bottlenose dolphins, the calf may go through a sensible period when the
mother upcall would be imprinted (Mann & Smuts 1998). In right whales, this period may
coincide with the close proximity and constant travelling behaviour displayed by the pair right
after the calf birth (Taber & Thomas 1982). It is also expected the calling rate during this period
to be high. Due to the sampling time of our study, it was not possible to record the pair´s vocal
ontogeny. Assuming there is a strong selective pressure to evolve vocal recognition, by the end
of season the vocal recognition system should already be established between the calf and its
mother and therefore, during interactions between pairs, individuals should be able distinguish
each other by their individual upcall features.
Call per minute (CPM)
Despite the fact that the number of individuals involved in pair-pair interactions may have
affected our results, greater CPM was observed in interacting groups. The CPM varied
according to the level of activity in each behavioural state, being greater in higher active
behaviours (interacting and bonding) and lower in less energetic states (travelling and resting).
When compared to the calling rate of SAGs (Kraus et al. 2001, Parks & Tyack 2005) CPM of
mother calf pairs is low, suggesting that perhaps other signal modalities are also used by
mothers and calves especially for close range communication, most likely visual and/or tactile.
Alternatively, low calling rates may be related to avoidance of detection by predators and/or
other whale groups and adult males that could hurt the calf when trying to engage in sexual
contact with the female (Kraus et al. 2001).
79
CONCLUSION
Acoustical signals are important for communication in mother-calf pairs. All call types used by
this subgroup appear to have the same functional significance as previously described in other
studies and overall calling rate is low. The use of more precise sound source calculations, real
time localization as well as the use of acoustic tags in future studies will reveal important
features of right whale mother-calf pairs’ communication dynamics and will provide further
fundamental information to the application of PAM in conservation efforts for the species.
80
ACKNOWLEDGEMENTS
Thank you to the many people that made this study possible, especially to Camila Morais and
all Right Whale Project volunteers of 2013. For logistical support we thank Juçara Wanderlinde,
Luiz Rodrigo Maçaneiro and Gustavo Stahelin from Fundação Pro-Tamar; APA Baleia Franca,
APA Anhatomirim, Rebio Arvoredo, Esec Carijós, ICMBio, Murilo Ternes from Base Cangulo
and Laguna´s Environmental Patrol. Cetacean Society International, Rufford Fundation (grant
14080-1) and the Federal university of Rio Grande do Norte funded this work.
81
FIGURES
A
B
C
D
E
F
Fig. 1. Spectrograms (Hamming window, FFT 512; overlap: 70%) of the six call classes identified in
the recordings: A- upcall; B- donwcall; C- vcall; D- constant call; E – hybrid call; F – pulsive call. Note
differences in frequency and time scales for each call type.
82
TABLES
Table 1. Activity budget of right whale mother-calf pairs.
Behavioural
state
Travelling
Resting
Interacting
Diving
Bonding
Nursing
Time (%)
41
22
20
7
5
5
Table 2. Behavioural states of mother-calf pairs observed in Santa Catarina, its related vocalizations and
proportion of call types.
Behavioura
l state
Interacting
Travelling
Bonding
Resting
Diving
Nursing
Total
Calls
(n)
67
27
6
2
0
0
Upcall
(%)
Downcall
(%)
Vcall
(%)
Constant
(%)
Pulsive
(%)
Hybrid
(%)
52
64
100
50
-
9
16
0
0
-
7
0
0
50
-
7
8
0
0
-
12
12
0
0
-
13
0
0
0
-
Table 3. CPM (call per minute) in each behavioural state in which vocalizations were recorded.
Behavioural state CPM
Interacting
3.35
Bonding
0.21
Travelling
0.12
Resting
0.02
83
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89
3. Discussão geral e conclusões
O conteúdo dessa dissertação constitui a base do conhecimento acerca da bioacústica
da baleia franca austral em águas brasileiras. Contribuições importantes foram dadas quanto ao
comportamento vocal e a ecologia comportamental de pares mãe-filhote. Estas informações
serão cruciais para futuras iniciativas que empregarão o monitoramento acústico passivo com
fins de investigação e/ou conservação especialmente na área de invernagem das baleias na costa
brasileira.
A comparação entre a proporção de tipos de chamados emitidos em áreas de invernagem
por pares mãe-filhote e em áreas de alimentação e/ou por grupos ativos de superfície (GAS),
relevou importantes diferenças que suportam hipóteses quanto ao significado adaptativo de
certos tipos de chamados e fornecem pistas sobre o uso das diferentes classes de sons por pares
mãe-filhote (Artigos 1 e 3).
O upcall, ou chamado de contato, foi o chamado mais frequentemente emitido na área
invernagem de Santa Catarina, e o único emitido durante interações entre mãe e filhote. Além
disso foi frequentemente ouvido durante a aproximação dos pares em interações par-par.
Chamados híbridos e pulsados, sons que apresentaram os maiores valores de parâmetros
relacionados a desordem acústica, foram encontrados concentrados em alguns minutos de
gravação sugerindo o uso destes em situações específicas (Artigo 1). De acordo com os
resultados da análise comportamental, o chamado down-upcall é empregado na mesma
proporção que downcalls enquanto o par está em descanso, o que pode indicar que o significado
adaptativo destes dois sons é semelhante (Artigo 3).
Gunshots não foram captados durante o processamento dos dados desta dissertação,
indicando que este som não é empregado com frequência na comunicação de pares mãe-filhote
e sua importância para este grupo é pequena (Artigos 1 e 3). Estes resultados porém, contrariam
90
evidências recentes do uso deste som por uma fêmea acompanhada por filhote, durante
interação com um elemento antropogênico do ambiente.
De acordo com os resultados deste estudo, a emissão de chamados de contato por pares
mãe-filhote não sofre variação nictemeral significativa (Artigo 2). É provável que este padrão
comportamental esteja associado ao estado comportamental predominante do par ao longo de
seu período de estadia nas áreas de invernagem. Desta maneira, recomenda-se que futuros
estudos abordando o comportamento vocal de baleias francas, especialmente de pares mãefilhote, leve em consideração variações no comportamento dos animais durante sua estadia em
determinadas áreas, sejam elas áreas de alimentação ou invernagem.
Supreendentemente durante a coleta de dados acústicos/comportamentais de 2013
(Artigo 3) eventos de interação entre pares representaram 20% do tempo total de
observação/gravação. Este cenário contraria descrições prévias do comportamento dos pares
que retratam a tendência a evitar outros grupos. Eventos de interação entre os pares com até 3
pares foram observados. A razão destas interações não é clara, porém acredita-se que estas
possam estar relacionadas ao desenvolvimento de habilidades sociais pelos filhotes. A maior
diversidade de tipos de chamados foi captada durante estas interações. A taxa de emissão de
chamados dos pares varia de acordo com o nível de atividade dos pares, sendo maior em estados
de maior agitação e movimentação, como em interações par-par e interações entre mãe e filhote,
e menor enquanto os animais estão em deslocamento e descanso. A baixa taxa de vocalização
dos pares e o fato de nenhum chamado ter sido detectado por pares enquanto mergulhados e em
eventos de amamentação, sugerem que outras modalidades de sinais podem ser empregadas
pelos pares para comunicação de curto alcance.
Deste projeto extraem-se também importantes recomendações para futuras iniciativas
de investigação:
91

O comportamento vocal de pares mãe-filhote pode ser afetado pela ontogenia
comportamental do grupo durante a permanência em uma determinada área.
Assim, os próximos estudos devem levar em consideração a influência do(s)
possível(eis) padrão(ões) de comportamento ao longo da estadia do par numa
determinada área.

Importantes avanços serão obtidos com o emprego de sistemas de localização
da fonte sonora que atuem em tempo real e com alta precisão, e também tags
acústicos. O uso destas tecnologias poderá elucidar questões importantes quanto
a produção individual de sons, sobre a ontogenia do aprendizado vocal e acerca
da identidade individual possivelmente contida nos chamados.
92
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