DEBORAH PINTO FERNANDES SPATIAL DISTRIBUTION of HUMPBACK WHALE SINGERS in the ABROLHOS BANK, BA, BRAZIL Dissertação Apresentad

DEBORAH PINTO FERNANDES

SPATIAL DISTRIBUTION OF HUMPBACK WHALE SINGERS IN THE ABROLHOS

BANK, BA, BRAZIL

Dissertação apresentada à Universidade

Federal do Rio Grande do Norte, para

obtenção do título de Mestre em Psicobiologia.

Natal

2014 DEBORAH PINTO FERNANDES

SPATIAL DISTRIBUTION OF HUMPBACK WHALE SINGERS IN THE ABROLHOS

BANK, BA, BRAZIL

Dissertação apresentada à Universidade

Federal do Rio Grande do Norte, para

obtenção do título de Mestre em Psicobiologia.

Orientador: Renata S. Sousa-Lima Mobley

Co-Orientador: Cristiane C. A. Martins

Natal

2014

Titulo: Spatial Distribution of Humpback Whale Singers in the Abrolhos Bank, BA, Brazil

Autor: Deborah Pinto Fernandes

Data da Defesa: 31/03/2014

Banca Examinadora:

______

Prof. Paulo André de Carvalho Flores, ICMBio

______

Prof. Eduardo Martins Venticinque, UFRN

______

Profa. Renata Santoro de Sousa Lima Mobley, UFRN

AGRADECIMENTOS

São poucas as pessoas que têm o privilegio de fazer o que sempre sonhavam. Sempre fui interessada por cetáceos mas nunca tinha imaginado que eu teria a chance de um dia estudá-los. Foi na graduação que descobri a oportunidade de chegar mais perto de alcançar esse sonho. Em Pipa que eu tive minha primeira chance de trabalhar com cetáceos, mais especificamente, golfinhos. Senti um prazer enorme como jamais tinha sentido em qualquer outro trabalho que fiz. Foi daí que percebi: quero ser pesquisadora e trabalhar com golfinhos.

Mas a vida sempre dá voltas. Eu imaginava que estudar baleias seria uma coisa ainda mais inatingível do que com golfinhos. Eis que surgiu uma oportunidade de pegar um barco saindo da Praia de Pirangi à procura de baleias. Podem anotar a data. Dia sete de agosto de

2010, minha vida mudou! Vi baleias jubartes pela primeira vez na minha vida! Que emoção que senti, que adrenalina, que animais magníficos! E foi ali, naquele dia, vendo aquelas três baleias saltando, batendo nadadeiras e borrifando que eu me apaixonei de vez. Decidi correr atrás desse sonho e ingressar num programa de mestrado, para estudar baleias, claro! E finalmente, em 2012 a minha oportunidade chegou! Passei na seleção para o programa de

Psicobiologia. Estudar comportamento animal, olha só que maravilha!

Serei sempre grata pela oportunidade que me foi dada. Professora Renata Sousa-

Lima, minha orientadora que em mais de uma ocasião foi também minha psicóloga, colega, amiga e conselheira. Acima de tudo uma pessoa que eu respeito e admiro muito. Renata, muito obrigada por acreditar em mim, por me aceitar em seu laboratório e em sua casa. Me sinto honrada em ser sua primeira aluna de mestrado da UFRN e espero muito ter feito um trabalho do qual você se orgulhe. Encontramos muitas dificuldades no caminho, mas com força e determinação, finalmente chegamos lá. Levarei sempre no meu coração os choros, as risadas, os conselhos, as piadas, os ensinamentos e as experiências que tivemos juntas (especialmente o karaokê!). Jamais conseguirei colocar em palavras o quanto sou grata por tudo que você fez por mim! Minha caminhada na estrada profissional está apenas começando e você esteve lá no primeiro passo me dando força pra seguir em frente.

Tivemos algumas dificuldades que só eu e Renata não conseguiríamos superar sozinhas. Foi aí que entrou em cena a mais que querida Cristiane Martins. Cris, acho que nunca troquei tanto e-mail com alguém como fiz com você! Mas valeram muito a pena. Eu só imagino o quanto poderia ter aprendido com você se nossos contatos fossem "ao vivo". Muito obrigada por todo o apoio, por todas as conversas em skype, todos os conselhos e incentivos e por acreditar que eu conseguiria. Aprendi a usar um programa que até me fazia medo e tudo foi com a sua ajuda! Sofri um bocado, tive até vontade de desistir, mas você nunca deixou.

Estava sempre dando uma força, mesmo que longe. E eu agradeço de coração por tudo que você fez por mim! Não há farofa no mundo que pague o seu apoio!!

Agradeço também ao Wall por todo o conhecimento passado. É incrível como tenho um bloqueio com estatística, mas sem dúvidas suas maravilhosas aulas me ajudaram a superar pelo menos um pouco o medo. Muito obrigada pela contribuição nos textos e estatísticas do terceiro capítulo da minha dissertação.

Aos professores do Programa de Pós-Graduação em Psicobiologia por todos os ensinamentos e conhecimentos passados. Foram aulas marcantes, que levarei pra sempre comigo durante minha formação. À equipe do Laboratório de Bioacústica! Marcos, Geraldo,

Bruna, Luciana, Jeniffer, pelas boas companhias no LaB e nas reuniões.

À CAPES pelo apoio financeiro.

Também a Isa e Ju por todas as risadas, pelo apoio e incentivo e pela amizade. Nos tempos de desespero, suas palavras confortantes me ajudaram muito. Tudo acontece em seu tempo e o tempo da nossa amizade foi logo no finalzinho do meu mestrado. Mas tenho certeza que muitas outras experiências (profissionais também) estão por vir. Jamais esquecerei Olinda e as praias e as comidinhas e tudo mais. O futuro que nos aguarde!

Não podia deixar de fora a minha grande parceira, Paulinha. Também nos aproximamos há pouco tempo, mas já foi tempo suficiente pra ver que essa amizade veio pra ficar. Muito obrigada pelos dias de surf, pela sua amizade querida e por todo o apoio e incentivo que você sempre me deu. Principalmente na reta final, você me ajudou a fazer análises na hora do desespero. Jamais esquecerei tudo que você fez e serei eternamente grata!

A todos os meus amigos e amigas da biologia. Minha caminhada talvez não teria vindo tão longe se não fosse pela existência de vocês na minha vida. Em especial a Matheus por toda a força que me deu com o ArcGIS! Camila, Julu, Lala, Keké, Julinha, Honara, Jack,

Lucas, e todo mundo que fez parte dessa jornada, estarão sempre em meu coração!

À minha família, minha fortaleza, minha base de apoio. Aos meus pais Fábio e Magda, palavras e acho que nem gestos serão representativos do quanto sou grata por vocês. Sempre me apoiando, me incentivando e até gritando (né Mainha?) pra fazer a coisa andar. Obrigada por me fazer ter força e inspiração para seguir em frente. Espero algum dia conseguir ser uma pessoa tão boa como vocês são. Amo e admiro muito vocês!

À minha one and only big sister Larissa. Brigada por todas as conversas, por sempre me incentivar, por seu amor e por seu lindo e maravilhoso filho! Noah, meu amor! Mesmo sem saber, você trouxe à sua titia muita felicidade e amor quando mais precisava.

A todas as pessoas que de forma direta ou indireta fizeram parte dessa jornada e contribuíram para a realização e conclusão do meu projeto. Foram dois anos cheios de emoção e que o resultado finalmente está aqui!

A todos, obrigada de coração!

"It is a curious thing that the sea, from which life first arose, should now be threatened by the activities of one form of that life. But the sea, though changed in a sinister way, will continue to exist: the threat is rather to life itself." Rachel Carson RESUMO

Mamíferos marinhos formam um grupo bastante diversificado, incluindo cetáceos, sirênios, pinípedes e carnívoros, como lontras e ursos polares. Estudos sobre a distribuição e abundância de mamíferos marinhos são de grande importância para fins de conservação e manejo. Esses são animais que passam toda ou a maior parte da vida no ambiente aquático e dependem de diversos fatores, como distribuição de recursos alimentares, batimetria, distribuição de parceiros, entre outros para sobreviver. Dentre todos os mamíferos marinhos, a baleia jubarte é uma das espécies mais estudadas. A jubarte é conhecida por produzir longas sequências padronizadas de sons conhecidas como "canto", sendo a acústica uma das principais formas de comunicação no meio aquático. Este trabalho tem como objetivo (1) fornecer uma revisão da literatura disponível sobre o estudo da distribuição de mamíferos marinhos utilizando métodos acústicos e/ou visuais nos últimos onze anos para identificar quais métodos e técnicas têm sido mais utilizados; (2) prever a distribuição de grupos de baleia jubarte vocalmente ativos em relação a variáveis ambientais e sociais no entorno do

Arquipélago dos Abrolhos; e, (3) verificar a existência de sobreposições entre a rota utilizada pelos barcos de turismo e machos cantores no entorno do Arquipélago dos Abrolhos, áreas onde possa haver potenciais interações espaciais e acústicas. Através da revisão de literatura no capítulo1, encontramos que, apesar do uso de monitoramento acústico passivo estar se tornando mais econômico e acessível nos últimos anos, os métodos mais usados para estudar distribuição de mamíferos marinhos são visuais. Ao responder um questionário sobre o método utilizado, a maioria dos pesquisadores tendeu a escolher o método visual por estarem inseridos em projetos maiores com outros focos. No segundo capítulo, foi feita uma regressão logística utilizando profundidade, distância a um buffer ao redor do Arquipélago dos

Abrolhos (0,92 km), distância a corais, tamanho de grupo e presença de filhote para prever atividade vocal. O modelo que melhor previu que grupos de baleias jubartes estariam vocalmente ativos quando não houver filhote presente no grupo (B = 1,234, Wald = 16,016, p

< ,01), estiverem distantes de corais (B = ,403, Wald = 4,263, p < ,05) e em áreas mais profundas (B = ,079, Wald = 3,460, p > ,05). Finalmente, no terceiro capítulo, realizamos análises espaciais que resultaram em mapas de densidade de grupos vocalmente ativos de baleias jubarte e de embarcações de turismo. Encontramos que as áreas de maior densidade de cantores coincide com áreas de maior densidade de embarcações. Tais áreas foram classificadas como alto risco para a comunicação da espécie na área amostrada. Investigar as preferências de habitat das baleias jubarte para atividade vocal com base em características ambientais e composição de grupo é essencial para o estabelecimento de áreas de manejo espaço-temporal com o objetivo de garantir uma comunicação acústica adequada, tão importante em áreas de reprodução. Nós também fornecemos resultados que enfatizam a necessidade de pôr em prática planos de manejo adaptativo que levem em consideração fatores que possam ser importantes para a conservação e manejo espaço-temporal da baleia jubarte.

Palavras-chave: Mamíferos marinhos, baleia jubarte, distribuição espacial, atividade vocal,

Abrolhos.

ABSTRACT

Marine mammals are a very diverse group, including cetaceans, sirenians, pinnipeds and carnivores such as otters and polar bears. Studies on marine mammal distribution and abundance are of great importance for conservation and management purposes. These are animals that spend most or all of their lives in the aquatic environment and depend on many factor, including acoustic communication to survive. Among all marine mammals, the humpback whale is one of the most studied species. This study aims to (1) provide a review of the available literature in research on marine mammal distribution using acoustic and/or visual methods over the past ten years to identify which methods and techniques have been used more often in the field; (2) predict the distribution of vocally active humpback whale groups in relation to environmental and social variables around the Abrolhos Archipelago; and (3) describe in a qualitative manner, the spatial interactions of humpback whales and tourism and research boats in the Abrolhos Archipelago. Through the literature review in chapter 1, we found that even though passive acoustic monitoring has become cheaper and more available in recent years, the most used methods to study marine mammals distribution consisted of visual surveys. In the second chapter, we performed a logistic regression using depth, distance to a buffer around the Abrolhos Archipelago (0.92 km), distance to reefs, group size and calf presence to predict vocal activity. The model that best predicted humpback whale singing activity included calf presence (B = 1.234, Wald = 16.016, p < .01), distance to reefs (B = .403, Wald = 4.263, p < .05) and depth (B = .079, Wald = 3.460, p >

.05). Finally, in the third chapter, we performed spatial analyses that resulted in density maps of humpback whales and boats and found that the areas of higher density of humpback whales coincide with areas of higher density of boats. These areas were classified as higher risk for the conservation of the species in the surveyed area. Investigating humpback whale habitat preferences for singing activity based on environmental characteristics and group composition is important in discussing spatio-temporal restriction areas aiming to ensure proper acoustic communication so important in nursing sites and the overall conservation of the populations along the Brazilian coast. We also provided spatial data that emphasize the need to put in practice adaptive management plans based on the results of experiments taking into consideration factors that may be important for conservation and management.

Keywords: Marine mammals, humpback whale, spatial distribution, vocal activity, Abrolhos.

SUMÁRIO

INTRODUÇÃO ...... 1

OBJETIVOS ...... 5

CAPÍTULO I - The use of acoustic and visual methods to study marine mammal distribution: an overview of the past eleven years...... 7

RESUMO ...... 9

ABSTRACT ...... 11

INTRODUCTION ...... 13

METHODS ...... 17

Literature review ...... 17

Questionnaire Analyses ...... 19

RESULTS ...... 21

Literature review ...... 21

Questionnaire Responses...... 24

DISCUSSION ...... 27

ACKNOWLEDGEMENTS ...... 30

REFERENCES ...... 30

CAPÍTULO II - Spatial distribution of singing humpback whale groups in the Abrolhos Bank,

Bahia, Brazil...... 40 RESUMO ...... 42

ABSTRACT ...... 43

INTRODUCTION ...... 44

METHODS ...... 50

Study site ...... 50

Data acquisition on humpback whale singers ...... 51

Data analyses ...... 52

RESULTS ...... 54

DISCUSSION ...... 58

ACKNOWLEDGEMENTS ...... 62

LITERATURE CITED ...... 63

CAPÍTULO III - Spatial overlap in distributions of vessel traffic and humpback whale singers in the navigation corridor to the Abrolhos National Marine Park ...... 74

RESUMO ...... 76

ABSTRACT ...... 78

INTRODUCTION ...... 80

METHODS ...... 85

Study site ...... 85

Humpback whale data ...... 86 Vessel traffic spatial data ...... 88

Co-occurrence qualitative analysis...... 89

Classification of co-occurrence areas ...... 89

Vessels sound data ...... 90

RESULTS ...... 92

Humpback whale data ...... 92

Vessel traffic spatial data ...... 93

Co-occurrence analysis ...... 95

Vessels sound data ...... 96

DISCUSSION ...... 97

CONCLUSIONS ...... 104

REFERENCES ...... 105

DISCUSSÃO & CONCLUSÃO ...... 120

REFERÊNCIAS BIBLIOGRÁFICAS ...... 124

APPENDIX A - SURVEY ...... 139 1

INTRODUÇÃO

Mamíferos marinhos têm sido amplamente estudados ao longo dos anos. A intenção de muitos pesquisadores é espécie a fim de medir seus padrões de distribuição e implicações para fins de conservação e manejo (Redfern et al. 2006). Os mamíferos marinhos têm sido explorados por humanos de forma consistente e a proteção desses animais pode garantir também a proteção de espécies chave no ecossistema marinho (Folkens et al. 2002, Bailey &

Thompson 2009). A conservação dos mamíferos marinhos necessita de informações a respeito de sua biologia, ecologia e também de características ambientais e geográficas que influenciam sua ocorrência e distribuição (Kaschner et al. 2006).

Diversos métodos de pesquisa são utilizados para estudar padrões espaciais de mamíferos marinhos, como pesquisas de ponto fixo e sobrevoôs (Higdon et al. 2012,

Langtimm et al. 2011), monitoramento acústico passivo (Mellinger et al. 2007, Van Parijs et al. 2009, Newhall et al. 2012), marcação por satélite (Ward et al. 2008), registros de encalhes

(Santos et al. 2010, Frantzis et al. 2011), dados históricos de caça (Ivaschenko & Clapham

2010, Weir 2010), entre outros.

Mamíferos marinhos dependem do som para comunicação e tais vocalizações estão relacionadas a comportamentos como comunicação intra-específica, atração de parceiros, agressão, alimentação, entre outros (Payne & McVay 1971, Thompson et al. 1979, Thompson et al. 1986). Mysticetos, ou grandes baleias, produzem sons de baixa frequência para se comunicar a longas distâncias e através disso, manter a comunicação mesmo quando há baixo 2

contato visual (Wursig 1988). A baleia jubarte, Megaptera novaeangliae (Borowski, 1781), é uma das espécies de grandes baleias mais estudadas (Norris et al. 1999) e dentre of mamíferos marinhos, é a mais conhecida por seus sons (Payne & McVay 1971, Tyack & Whitehead

1983, Clapham et al. 1992).

Baleias jubarte são conhecidas por seus complexos comportamentos aéreos (Clapham

& Meade 1999, Clapham 2000) e pelo canto produzido pelos machos (Payne & McVay 1971,

Darling 1983, Cholewiak et al. 2012). A estrutura e os padrões apresentados nos cantos das baleias jubartes podem depender de características ambientais que afetam a propagação do som (Mercado & Frazer 1999, Cerchio et al. 2001, Darling & Sousa-Lima 2005, Darling et al.

2006, Sousa-Lima et al. 2010).

A baleia jubarte tem fidelidade a áreas de alimentação e reprodução tradicionais e muitas vezes são encontradas em áreas costeiras (normalmente próximo à costa ou águas de plataformas continentais) (Dawbin 1966, Whitehead & Moore 1982, Clapham & Meade

1999). As jubartes são migratórias e distribuídas em hábitats de alta latitude durante o verão para se alimentar e em águas tropicais ou subtropicais no inverno para fins de reprodução

(Clapham 2000, Rasmussen et al. 2007).

No Brasil, a população de baleia jubarte está distribuída durante o inverno e primavera austrais ao longo de águas costeiras desde 5º a 24ºS, aproximadamente (Zerbini et al. 2004,

Zerbini et al. 2011, Martins et al. 2013). A população que utiliza a costa Brasileira como zona 3

de reprodução, pertence ao grupo "A" como definido pela International Whaling Commission

(IWC). A área mais importante para reprodução para as baleias jubartes da costa Brasileira é o

Banco de Abrolhos (16º40' - 19º30'S), localizado no sul do estado da Bahia e no norte do

Espírito Santo (Engel 1996, Siciliano 1997, Martins et al. 2001).

A escolha de hábitat em áreas de reprodução é uma função entre comportamento, necessidades biológicas e condições ambientais (Robbins et al. 2001) e pode ter influência de fatores sociais. Alguns estudos mostram que em áreas de reprodução, a distribuição de diferentes grupos de baleias jubartes pode estar relacionada a proximidade à costa e profundidade (Clapham 2000, Martins et al. 2001, Ersts & Rosenbaum 2003).

Devido a sua ampla distribuição em áreas com alta densidade de atividades antrópicas, a baleia jubarte se encontra vulnerável a poluição química, ruídos antropogênicos e interações com redes de pesca. O crescimento do tráfego marítimo, as velocidades de embarcações e o crescente número de colisões com baleias também geram preocupação (Reeves et al. 2003,

Jensen & Silber 2004, Félix & Waerebeek 2005). Atividades de turismo de observação de cetáceos também têm crescido muito e, apesar de ser uma alternativa à caça, pode trazer reações indesejadas a cetáceos como a baleia jubarte (Hoyt 2001, Parsons et al. 2003).

Há um acúmulo de evidências mostrando que a aproximação de embarcações turísticas pode alterar o comportamento de cetáceos (Williams et al. 2002, Scheidat et al. 2004, Corbelli

2006), levando a impactos que podem ser de longo prazo (Lusseau 2005, Bejder et al. 2006). 4

Tais distúrbios podem levar a efeitos negativos em comportamentos de superfície (Coscarella et al. 2003, Lusseau 2006, Noren et al. 2009, Stamation et al. 2010), tamanho e composição de grupo (Mattson et al. 2005, do Valle and Cunha Melo 2006), velocidade e direcionalidade de natação (Williams et al. 2002, Scheidat et al. 2004, Timmel et al. 2008, Williams et al.

2009), alimentação (Stamation et al. 2007, Carrera et al. 2008, Dans et al. 2008, Lusseau et al.

2009), descanso (Williams et al. 2006, Stockin et al. 2008, Visser et al. 2011) e comunicação acústica (Scarpaci et al. 2000, Buckstaff 2004, Foote et al. 2004, Sousa-Lima and Clark

2008), dentre outros (Bryant et al. 1984, Lusseau 2005, Bejder et al. 2006, Carrera et al.

2008).

OBJETIVOS

1. Capítulo 1:

Resumir tendências históricas recentes na utilização de métodos para avaliar padrões espaciais de populações de mamíferos marinhos;

Identificar possíveis fatores que influenciam as tendências encontradas no uso de métodos acústicos e/ou visuais.

2. Capítulo 2:

Identificar a distribuição espacial de machos cantores de baleias jubartes durante duas temporadas reprodutivas;

Prever a distribuição espacial de machos cantores baseado em variáveis ambientais e sociais.

3. Capítulo 3:

Identificar áreas de densidade de baleias jubarte no Banco de Abrolhos;

Identificar áreas de densidade de embarcações turísticas e de pesquisa no Banco de

Abrolhos; 6

Identificar áreas de sobreposição de densidade de baleias e embarcações a fim de verificar a existência de áreas de risco.

CAPÍTULO I - The use of acoustic and visual methods to study marine mammal distribution: an overview of the past eleven years.

Deborah P. Fernandes1, Renata S. Sousa-Lima1,2, Cristiane C. A. Martins3, Wallisen Tadashi

Hattori1

1Universidade Federal do Rio Grande do Norte

2Cornell Lab of Ornithology

3Université de Montreal

MAMMAL REVIEW (Qualis: A2, Impact factor: 3.425)

A ser submetido.

The use of acoustic and visual techniques to study marine mammal distribution:

an overview of the past eleven years

Deborah P. Fernandes

Bioacoustics Laboratory, Federal University of Rio Grande do Norte, Natal, RN, 59078-970, Brazil

Renata S. Sousa-Lima

Bioacoustics Laboratory, Federal University of Rio Grande do Norte, Natal, RN, 59078-970, Brazil

Cristiane C. A. Martins

Geography Department, University of Montreal, 520 Chemin de la Côte de Saint Catherine, Outremont, H2V

2B8, Canada

Wallisen Tadashi Hattori

Laboratory of the Evolution of Human Behavior, Graduate Program in Psychobiology, Federal University of Rio

Grande do Norte, Natal, RN, 59078-970, Brazil

Correspondence: D. P. Fernandes. E-mail: [email protected]

RESUMO

1. Mamíferos marinhos formam um grupo bastante diversificado incluindo cetáceos, sirênios, pinípedes e carnívoros como lontras e ursos polares. Estudos sobre distribuição espacial e abundância são de extrema importância para fins de conservação e manejo. Tornam-se ainda mais relevantes devido à expansão de atividades antropogênicas no ambiente marinho. Estas atividades podem ter efeitos negativos em mamíferos marinhos de diferentes formas e apesar de não ser provável que todas as consequências possam ser e serão medidas, monitoramento adequado pode ajudar a detectar possíveis tendências. Diferentes métodos e técnicas são utilizados para abordar tais questões: visuais, aéreos, monitoramento acústico passivo (MAP), marcação por satélite, registros de encalhes, dados históricos sobre caça, etc.

2. Nós fornecemos uma revisão da literatura disponível de pesquisas sobre distribuição de mamíferos marinhos usando métodos acústicos e/ou visuais nos últimos onze anos para identificar quais métodos e técnicas têm sido mais utilizados em campo ao longo dos anos e verificar quais dificuldades têm sido enfrentadas por pesquisadores na escolha do método utilizado.

3. Foi realizada uma busca de artigos científicos de 2003 a 2013 através da Web of Science e outras bibliotecas virtuais utilizando 539 combinações de palavras-chave relativas ao método, grupo animal e foco do estudo. Informações foram coletadas sobre qual método foi utilizado, seja ele visual, acústico ou ambos. Além disso, um questionário foi enviado a pesquisadores de mamíferos marinhos através de e-mails pessoais e pela Marine Mammal Research and

Conservation Discussion (MARMAM) a fim de complementar os dados com informações pessoais dos pesquisadores. 10

4. Pesquisas visuais foram as mais desenvolvidas ao longo dos anos. Também foi evidente que o uso de esforços combinados usando métodos acústicos e visuais estão aumentando.

Palavras-chave: mamíferos marinhos, distribuição, métodos acústicos, métodos visuais, pesquisas

ABSTRACT

1. Marine mammals are a very diverse group, including cetaceans, sirenians, pinnipeds, and carnivores such as otters and polar bears. Studies on marine mammal distribution and abundance are of great importance for conservation and management purposes. They are even more relevant due to the expansion of anthropogenic activities in the marine environment.

These activities can have negative impacts on marine mammals in many different ways, and although it is not likely that all the consequences can and will be measured, adequate monitoring can be used to detect possible trends. Different methods and techniques are used to address these issues: visual surveys, aerial surveys, passive acoustic monitoring (PAM), satellite tagging, stranding records, historical data on whaling, etc.

2. We provide a review of the available literature in research on marine mammal distribution using acoustic and/or visual methods over the past eleven years to identify which methods and techniques have been used more often in the field over the years and to verify the difficulties faced by researchers when choosing the method used.

3. Scientific papers from 2003 to 2013 were searched through the Web of Science and other virtual libraries using 539 combinations of keywords regarding the method, animal group and focus of the study. Information was collected about which method was employed, whether it was visual surveys, acoustic monitoring or both. Additionally, a questionnaire was sent to marine mammal researchers through personal e-mail and Marine Mammals Research and

Conservation Discussion (MARMAM), in order to complement with personal information from researchers. 12

4. Visual surveys were the most used method even in the most recent years. It was also evident that the use of combined efforts using acoustic and visual methods is increasing over the past years.

Keywords: marine mammals, distribution, acoustic methods, visual methods, surveys

INTRODUCTION

Marine mammals are a very diverse non-taxonomic group, including about 100 living species. They are spread out among four different mammalian groups: pinnipeds (seals, sea lions and walruses), cetaceans (whales, dolphins and porpoises), sirenians (manatees and dugongs), carnivores (otters and polar bears). These animals are well adapted for life in the water, including physiological and structural specializations for the aquatic environment, such as the development of blubber to increase insulation, countercurrent heat exchange systems, helping cope with low temperatures, and other modifications of eyes, noses, ears and limbs.

All marine mammals depend on some level on the aquatic environment in order to survive, whether if it is spending their wholes lives in the water, as it is for cetaceans and sirenians, or coming ashore for reproduction, to molt or rest (Jefferson et al. 1993, Berta et al. 2006).

Marine mammals form one of many groups that have been consistently exploited by humans. They have been hunted for fur, meat, oil and are still being hunted, causing the reduction or even extinction of some species (Folkens et al. 2002). Marine mammals can be potential indicators of ecosystem processes and their protection could also ensure protection of other key species of the marine ecosystem (Bailey & Thompson 2009). Protecting these animals through effective conservation measures requires detailed information not only on biological processes of each species but also on environmental and geographical characteristics (Kaschner et al. 2006) that influence their occurrence and distribution.

Occupying many habitats, from major rivers and coastal areas to deep portions of the ocean, marine mammals are a very widespread group (Folkens et al. 2002, Bastida et al.

2007). These animals are not restricted to one specific geographical area and can be found from polar to tropical waters (Bastida et al. 2007). Species may select their habitats based on prey availability, climatic variations or other characteristics, which may also inflict seasonal or temporal variations in habitat choices (Gambaiani et al. 2008, Davies et al. 2014). Seeing that these animals spend most or all of their lives in the water and occupy numerous habitats, they can become hard to study (Jefferson et al. 1993, Gambaiani et al. 2009).

Studies that focus on the animals' distribution and habitat use can be important in assessing impacts of human activities on species and to properly manage areas of high concentration of marine mammals (Dalla Rosa et al. 2012, Matkin et al. 2012). It has been known for a very long time that some species of marine mammals are found exclusively or primarily in waters with determined depth, temperature variation and oceanographic characteristics, and not in areas without at least one or let alone all of these features (Martins et al. 2001, Ersts & Rosenbaum 2003, Forney et al. 2012). However, the characteristics that dictate the range of certain species distribution are not fully known (Jefferson et al. 1993).

Many factors influence distribution patterns of marine mammals, for instance, major ocean surface currents and subsurface movements of major water masses (Smith et al. 1986, Hooker et al. 1999, Gregr & Tristes 2001, Félix & Botero-Acosta 2011). Such movements may regulate nutrient distribution, making it likely that some species will take advantage of the richness present in certain areas (Jefferson et al. 1993, Davis et al. 2014).

Marine mammals are constantly exposed to anthropogenic activities, such as maritime traffic and hydrocarbon exploration (Martins et al. 2013). These activities may have negative effects on these animals, due to the increasing disturbance, injury or even death from ship strikes. Commercial whaling also had great impact on the population size and structures of many marine mammals. For example, it is believed that as much as 95% of the existing population of humpback whales prior to whaling was eliminated (Clapham 2000). Aside from this, marine mammals are great dependants on sound as a primary form of communication, which is highly affected by human activities, especially commercial shipping and seismic surveys (Clark et al. 2009). Through analysis of spatial data on marine mammals it is possible to assess how anthropogenic activities such as the mentioned above and even global phenomena like global warming may be affecting these animals’ behavior and spatial patterns

(Gambaiani et al. 2008).

The main focus on research about marine mammals' spatial patterns has been distribution (Langtimm et al. 2011, Dalla Rosa et al. 2012, Matkin et al. 2012). To study distribution, many methods can be used, which can be categorized as visual, acoustic or others

(Mellinger et al. 2007, Van Parijs et al. 2009, Manna et al. 2010, Langtimm et al. 2011,

Higdon et al. 2012, Newhall et al. 2012). Among visual methods, there are land-based, ship- based and aerial surveys (Bazzalo et al. 2008, Manna et al. 2010, Langtimm et al. 2011,

Higdon et al. 2012). Acoustic methods can be fixed (archival or real time), towed (single or multi sensors) and others such as drifting sensors, unmanned vehicles and acoustic tags

(Mellinger et al. 2007, Van Parijs et al. 2009, Kimura et al. 2012, Newhall et al. 2012).

Acoustic methods allow for large spatial and time scale studies with the species of interest 16

(McDonald et al. 1995, Santos et al. 2010, Higdon et al. 2012, Jewel et al. 2012, Sousa-Lima et al. 2013). Along with the advancements in passive acoustics technology, it has become possible not only to study behavior and distribution of marine mammals, but also to detect and track animals through sound (Payne & McVay 1971, Watkins 1986, Clark et al. 1996,

Thode et al. 2000, Wahlberg 2002, Sousa-Lima 2007). Other methods include satellite tagging, stranding records and historical data on whaling (Ward et al. 2008, Ivaschenko &

Clapham 2010, Santos et al. 2010, Weir 2010, Frantzis et al. 2011).

The study of a species' distribution, occurrence and abundance is of extreme importance for wildlife and conservation purposes, and to understand their role in a region's ecosystem (Williams & Thomas 2007, Gedamke & Robinson 2010). An overview on how research on marine mammals’ spatial distribution has developed throughout the years can help us assess if the development of acoustic sensors has impacted trends related to methods used, species group studied and even geographic location of the studies. Thus, the purpose of this study was to assess the use of acoustic and/or visual methods to study marine mammal distribution through a review of the available literature and through a questionnaire analyzing the difficulties faced by researchers. We do not intend to discuss effectiveness of each method, but in fact show what tendencies can be seen in the use of each method and technique.

METHODS

Literature review

A broad review of available literature on marine mammal distribution has been conducted. The search focused on peer-reviewed publications, scientific books, theses and dissertations on marine mammal distribution using acoustic, visual or combined acoustic and visual methods (Figure 1). We compiled literature published between 2003 and 2013.

Figure 0-1 - Conceptual map of the acoustic, visual and combined acoustic and visual methods.

The search was done mainly in the Web of Science virtual library with the intention of reaching the highest number possible of publications. Also, the virtual libraries 'Periódicos 18

CAPES', available through the Coordination of Improvement of Higher Education Personnel

Brazilian agency (CAPES), the Cornell University Library, which provides access to various databases, as well as Google Scholar were used in the search. Available literature was searched using 539 combinations of keywords regarding the method, animal group and focus of the study (Table 1).

Table 1 - Keywords used in the literature search.

Method Group Objective

- Marine Mammal, Dolphin, Whale, Porpoise, Manatee, Seal

- Cetacea

- Odontoceti (Pontoporia, Sotalia, Stenella, Delphinus, Platanista, Inia, Lipotas, Lissodelphis, Steno, Sousa, Tursiops, Cephalorhynchus, Phocoena, Neophocoena, - Acoustic Lagenorhynchus, Phocenoides, Lagenodelphis, Kogia, Orcaella, Peponocephala, Feresa, Grampus, - Acoustic Mesoplodon, Ziphius, Tasmacetus, Hyperoodon, monitoring Berardius, Delphinapterus, Monodon, Pseudorca, Globicaphala, Orcinus, Physeter, Indopacetus) - Passive acoustic monitoring - Mysticeti (Caperea, Balaena, Eubalaena, - Distribution Balaenoptera, Megaptera, Eschrichtius) - Monitoring - Abundance - Pinnipedia - Aerial - Occurrence - Phocidae (Hydrurga, Leptonychotes, Lobodon, - Ship based Ommatophoca, Mirounga, Monachus, Erignathus, Cystophora, Pagophilus, Phoca, Halichoerus) - Land based - Odobenidae (Odobenus)

- Otariidae (Zalophus, Eumetopias, Neophoca, Phocarctos, Arctocephalus, Otaria, Callorhinus)

- Sirenia

- Trichechidae (Trichechus)

- Dugongidae (Dugong)

Records were reviewed and all information relevant to this study was extracted, such as: method employed; animal group studied; location of study; publishing year; and focus on distribution, abundance and/or occurrence. All records included in this review were of research conducted with species located in the aquatic environment, excluding studies that registered animals located on land. For the purpose of this study, only peer-reviewed publications were taken into consideration.

Questionnaire Analyses

In order to complement the review in an exploratory manner, a questionnaire was created (Appendix A). This research instrument consisted of three groups of questions. The first question contained nine items to evaluate on a 7-point Likert scale (1 being least important and 7 being most important) the importance of each item in influencing the method used by the researcher. In the second question, they were asked to describe more specifically how the items that they classified on the previous question influenced the choice of technique or method used. Finally, the third question was an open space for researchers to describe any advantages and/or disadvantages they considered during their research. The questionnaire was created with the SurveyMonkey website and sent to the main authors of the papers that resulted from the literature review and also to MARMAM, an e-mail list that connects researchers working with marine mammals worldwide.

The questionnaire responses were analyzed in the program SPSS. In order to investigate the participant's answers for the first question, we performed a factorial analysis 20

with the principal component extraction method and Varimax rotation. To identify if the correlation matrix was in fact factorable, we used the global Kaiser-Meyer-Olkin (KMO) diagnostic indicators and the Bartlett sphericity test. We considered the eigenvalue limit higher or equal to one to determine the total explained variance of the sample by interdependence of the answer, which determined the number of factors to be considered. In order to compose the factors, we considered only the items with a value of |0.30| or higher and with the sampling adequacy measure of each question with a value of 0.5 or higher in the anti- image matrix. For comparison between the extracted factors, we saved each factors’ regression coefficients.

We also performed a cluster analysis with the hierarchic methods with the connection between groups (interval measure of the square Euclidian distance) to determine the number of participant groups, which is most likely based on the answer patterns. After we determined the number of groups, we performed a cluster analysis with the k-means method in order to identify which participant belonged to each cluster.

Finally, we conducted a Multivariate Generalized Linear Model (GLM) to identify the effect of the extracted clusters on each factors regression coefficient. For all analysis, we considered the significance level of 5%.

RESULTS

Literature review

The literature survey resulted in a total of 154 publications from 2003 to 2013. In general, visual surveys have been the most used method in the publications that resulted from this survey. Visual surveys (N = 98) represented 64% of the papers found, while acoustic surveys (N = 29) represented 19% and the combination of both visual and acoustic methods

(N = 27) resulted in 17% of the publications.

The use of combined visual and acoustic methods has fluctuated over time (Figure 2).

Visual methods are always the most used throughout the years, except in the year of 2013 (N

= 1). The number of publications that used acoustic methods also fluctuated over the years, but in general, the highest percentages were seen in the years of 2008, 2010 and 2012 and were approximately the same.

Figure 0-2 - Use of each research method to study marine mammal distribution by publication year.

Acoustic methods were mostly used for baleen whales and toothed whales (Figure 3).

There were no publications that used only acoustic methods to study spatial patterns of sirenians (dugongs and manatees), but there were publications that used visual and acoustic methods combined. Mysticetes and odontocetes were the most studied animal groups using visual methods alone and acoustic and visual methods combined.

Figure 0-3 - Use of research method to study marine mammal distribution by animal group.

The analysis by oceans shows that the North Atlantic, North Pacific and Others were the ones with the greatest percentage of publications (Figure 4). It is possible to see that acoustic methods were most used in the North Pacific and North Atlantic but also very used in others (Indian Ocean, river basins, combination of more than one locations or worldwide).

Visual methods were most used in the North Atlantic. The combination of acoustic and visual methods was most used in the North Pacific. 24

Figure 0-4 - Use of each research method to study marine mammal distribution by ocean basin.

Questionnaire Responses

The global diagnosis indicators showed that the correlation matrix is factorable (KMO

= 0.70, χ² = 128.60, DF = 36, p < 0.001). We also observed the sampling adequacy of all items. The analysis indicated two factors that explained 53.75% of the total sample variance.

We can see that the factor 1 was composed of the questions 3, 4, 5, 8 and 9, which represent difficulties with smaller means. Factor 1 consisted of the difficulties related to financing.

Factor 2 was composed of the questions 1, 2, 6 and 7, which together represent difficulties with higher values. Factor 2 consisted of the difficulties related to logistics. Table 2 shows the values of this analysis.

Table 2 - Description of each items' values and the extracted factors.

Factors Sampling Adequacy Items Mean Standard deviation Measure Commonality 1 2

I3 2.70 1.87 0.69 0.70 0.84

I4 3.19 2.01 0.69 0.70 0.83

I5 3.23 1.93 0.85 0.39 0.49

I8 2.62 2.07 0.73 0.53 0.68

I9 3.09 1.81 0.69 0.59 0.72

I1 4.38 2.05 0.85 0.31 0.39

I2 4.70 2.20 0.58 0.44 0.56

I6 4.53 2.03 0.67 0.57 0.73

I7 4.74 1.93 0.60 0.61 0.78

The hierarchical cluster analysis showed that two groups of respondents is the formation that best represents the answers pattern. The variance analysis of each item showed that, with exception of item 2, all items contributed to the formation of the two participant clusters (Table 3).

Table 3 - Variance analysis of the contribution of each

item in the formation of clusters.

Items F DF p

I1 8.90 1, 51 0.004

I2 0.32 1, 51 0.575

I3 40.03 1, 51 0.000

I4 25.53 1, 51 0.000

I5 10.74 1, 51 0.002

I6 8.42 1, 51 0.005

I7 4.15 1, 51 0.047

I8 71.10 1, 51 0.000

I9 9.76 1, 51 0.003

The linear model constructed indicated a difference in the regression coefficients among clusters (F = 47.58, DF = 2, 50, p < 0.001). For factor 1 (F = 54.43, DF = 1, 51, p <

0.001), we observed that cluster 2 (M = 1.08) showed a higher score than cluster 1 (M = -

0.47). Cluster 2 represents the groups that presented difficulties related to financial issues, those that composed factor 1. For factor 2 (F = 7.24, DF = 1, 51, p = 0.006), we observed that cluster 1 (M = 0.24) presented higher scores than cluster 2 (M = -0.56). Cluster 1 represents the groups with difficulties related to logistical issues, that is, difficulties that composed factor

2. Means and 95% confidence intervals for the regression are found in Figure 5.

Figure 0-5 - Means and 95% confidence intervals of the regression factors for clusters 1 (●) and 2 (○).

DISCUSSION

Through the database created from the literature review, we were able to identify trends related to the use of acoustic and visual methods. Of the 154 publications that made up the database, the most used methods over the period of eleven years consisted of visual surveys. According to the researchers answers to our questionnaire, visual methods were most used in studies that focused not only on habitat use and animal distribution, but also on animal behavior (e.g. Manna et al. 2010, Félix & Botero-Acosta 2011, Scheidat et al. 2011,

Anderwald et al. 2012, Higdon et al. 2012) and population size estimates (e.g. Sumich &

Show 2011, Matkin et al. 2012).

The individuals that formed cluster 1 had difficulties included in factor 2 regarding logistics issues. Many of the responders were part of surveys that depended on the use of methods already determined by a larger, umbrella project, or on other specific research questions that could only be answered by using visual methods. Visual surveys are highly dependent on environmental conditions, access to the surveyed area and the total range of the study area (local, regional or worldwide) and many authors described in the questionnaire that combining the use of visual and acoustic methods could be a solution to this problem (Pirotta et al. 2011, Rako et al. 2013).

Even though the use of passive acoustic monitoring has become cheaper and more available for research over the years (Sousa-Lima et al. 2013), visual methods continue to dominate the research on marine mammal spatial patterns. This is surprising given that these animals rely on sound to communicate and are so visually elusive. Perhaps the use of combined visual and acoustic methods is sure to address these pitfalls due to the complimentary methods of detection of underwater creatures (Barlow & Taylor 2005,

Williams et al. 2011). Researchers acknowledge that acoustic equipments can have high initial costs, but can be used for many years. Depending on the size of the survey area, visual surveys would have higher costs, due to fuel, time needed to properly survey the entire area and environmental conditions.

Acoustic methods were most used in surveys performed in northern oceans (Verfuß et al. 2007, Akamatsu et al. 2010, Kerosky et al. 2012), a trend that could be associated with the 29

availability of equipment and lack of financial constraints in that region. From the questionnaires' answers, it seems that the size and availability of research staff is not an issue for researchers working with acoustic methods as has been previously seen by Sousa-Lima et al. (2013).

Even after the development of new tools for acoustic detection of marine mammals, visual methods are still the most commonly used in verifying where and how animals are distributed. It maybe a result of the lack of information on individual sound production rates

(but see Parks et al. 2010) that would increase the accuracy of acoustic surveys for animal abundance estimates. Nonetheless, some advances in developing fields are being made to address this caveat (Marques et al. 2013). Field surveys on marine mammals have shown to present many logistical and analytical challenges (Connor et al. 2000). Overcoming these issues is necessary in order to properly study marine mammal spatial patterns and obtain the best data that can be collected in the most reliable and efficient way to inform management and conservation efforts. The use of acoustic methods has been proven to be effective for monitoring marine mammals and determining spatial patterns (Stafford et al. 1999, Mellinger et al. 2004, Širović et al. 2009, Sousa-Lima & Clark 2009) and equipment continues to become more accessible and cost-effective (Sousa-Lima et al. 2013), an increase in the use of acoustic methods in studying marine mammals' spatial patterns is likely to occur.

ACKNOWLEDGEMENTS

This work was supported by the Coordination of Improvement of Higher Education

Personnel (CAPES).

REFERENCES

Akamatsu T, Nakamura K, Kawabe R, Furukawa S, Murata H, Kawakubo A, Komaba M

(2010) Seasonal and diurnal presences of finless porpoises at a corridor to the ocean from their habitat. Marine Biology 157:1879-1887.

Anderwald P, Evans PGH, Dyer R, Dale A, Wright PJ, Hoelzel AR (2012) Spatial scale and environmental determinants in minke whale habitat use and foraging. Marine Ecology

Progress Series 450:259-274.

Bailey H, Thompson PM (2009) Using marine mammal habitat modelling to identify priority conservation zones within a marine protected area. Marine Ecology Progress Series 378:279-

287.

Barlow J, Taylor B (2005) Estimates of sperm whale abundance in the Northeastern

Temperate Pacific from a combined acoustic and visual survey. Marine Mammal Science

21:429-445.

Bastida R, Rodríguez D, Secchi E, Silva V (eds; 2007) Mamíferos Acuaticos de Sudamerica y

Antartida. Vazquez Mazzini Editores, Buenos Aires, Argentina. 31

Bazzalo M, Flores PAC, Pereira MG (2008) Uso de hábitat y principales comportamientos del delfín gris (Sotalia guianensis, Van Bénéden, 1864) en la Bahía Norte, Estado de Santa

Catarina, Brasil. Mastozoologia Neotropical 15:9-22.

Berta A, Sumich JL, Kovacs KM (eds; 2006) Marine Mammals Evolutionary Biology.

Elsevier, Burlington, USA.

Clark CW, Charif R, Mitchell S, Colby J (1996) Distribution and behavior of the Bowhead whale, Balaena mysticetus, based on analysis of acoustic data collected during the 1993 spring migration off Point Barrow, Alaska. Reports of the International Whaling Commission

46:541-552.

Clark CW, Ellison WT, Southall BL, Hatch L, Van Parijs SM, Frankel A, Ponirakis D (2009)

Acoustic masking in marine ecosystems: intuitions, analysis and implication. Marine Ecology

Progress Series 395:201-222.

Clapham PJ (2000) The humpback whale: seasonal feeding and breeding in a baleen whale.

In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean Societies - field study of dolphins and whales, 173-196. University of Chicago Press, Chicago, USA.

Connor RC, Mann J, Tyack PJ, Whitehead H (2000) Introduction: the social lives of whales and dolphins. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean Societies - field study of dolphins and whales, 1-6. University of Chicago Press, Chicago, USA.

Dalla Rosa L, Ford JKB, Trites AW (2012) Distribution and relative abundance of humpback whales in relation to environmental variables in coastal British Columbia and adjacent waters.

Continental Shelf Research 36:89-104. 32

Davies KTA, Taggart CT, Smedbol RK (2014) Water mass structure defines the diapausing copepod distribution in a right whale habitat on the Scotian Shelf. Marine Ecology Progress

Series 497:69-85.

Ersts PJ, Rosenbaum HC (2003) Habitat preference reflects social organization of humpback whales (Megaptera novaeangliae) in a wintering ground. Journal of Zoology 260:337-345.

Félix F, Botero-Acosta N (2011) Distribution and behaviour of humpback whale mother-calf pairs during the breeding season off Ecuador. Marine Ecology Progress Series 426:277-287.

Folkens PA, Reeves RR, Stewart BS, Clapham PJ, Powell JA (eds; 2002) Guide to Marine

Mammals of the World. National Audubon Society, New York, USA.

Forney KA, Ferguson MC, Becker EA, Fiedler PC, Redfern JV, Barlow J, Vilchis IL,

Ballance LT (2012) Habitat-based spatial models of cetacean density in the eastern Pacific

Ocean. Endangered Species Research 16:113-133.

Frantzis A, Airoldi S, Notarbartolo-di-Sciara G, Johnson C, Mazzariol S (2011) Inter-basin movements of Mediterranean sperm whales provide insight into their population structure and conservation. Deep-Sea Research I 58:454-459.

Gambaiani DD, Mayol P, Isaac SJ, Simmonds MP (2008) Potential impacts of climate change and greenhouse gas emissions on Mediterannean marine ecosystems and cetaceans. Journal of the Marine Biological Association of the United Kingdom 89:179-201.

Gedamke J, Robinson MS (2010) Acoustic survey for marine mammal occurrence and distribution off East Antarctica (30-80ºE) in January-February 2006. Deep-Sea Research II

57:968-981. 33

Gregr EJ, Trites AW (2001) Predictions of critical habitat for five whale species in the waters of coastal British Columbia. Canadian Journal of Fisheries and Aquatic Science 58:1265-

1285.

Higdon JW, Hauser DDW, Ferguson SH (2012) Killer whales (Orcinus orca) in the Canadian

Arctic: Distribution, prey items, group sizes, and seasonality. Marine Mammal Science

28:E93-E109.

Hooker SK, Whitehead H, Gowans S (1999) Marine protected area design and the spatial and temporal distribution of cetaceans in a submarine canyon. Conservation Biology 13:592-602.

Ivashchenko Y, Clapham P (2010) Bowhead whales Balaena mysticetus in the Okhtsk Sea.

Mammal Review 40:65-89.

Jefferson TA, Leatherwood S, Webber MA (eds; 1993) Food and Agriculture Organization of the United Nations Species Identification Guide: Marine mammals of the world. United

Nations Environment Programme, Rome, Italy.

Jewel R, Thomas L, Harris CM, Kaschner K, Wiff R, Hammond PS, Quick NJ (2012) Global analysis of cetacean line-transect surveys: detecting trends in cetacean density. Marine

Ecology Progress Series 453:227-240.

Kaschner K, Watson R, Trites AW, Pauly D (2006) Mapping world-wide distributions of marine mammal species using a relative environmental suitability (RES) model. Marine

Ecology Progress Series 316:285-210. 34

Kerosky SM, Širović A, Roche LK, Baumann-Pickering S, Wiggins SM, Hildebrand JA

(2012) Bryde's whale seasonal range expansion and increasing presence in the Southern

California Bight from 2000 to 2010. Deep-Sea Research I 65:125-132.

Kimura S, Akamatsu T, Li S, Dong L, Wang K, Wang D, Arai N (2012) Seasonal changes in the local distribution of Yangtzee finless porpoises related to fish presence. Marine Mammal

Science 28:308-324.

Langtimm CA, Dorazio RM, Stith BM, Doyle TJ (2011) New aerial survey and hierarchical model to estimate manatee abundance. Journal of Wildlife Management 75:399-412.

Manna GL, Clò S, Papale E, Sarà G (2010) Boat traffic in Lampedusa waters (Strait of Sicily,

Mediterranean Sea) and its relation to the coastal distribution of common bottlenose dolphin

(Tursiops truncatus). Ciencias Marinas 36:71-81.

Marques TA, Thomas L, Martin SW, Mellinger DK, Ward JA, Moretti DJ, Harris D, Tyack

PL (2013) Estimating animal population density using passive acoustics. Biological Reviews of the Cambridge Philosophical Society 88:287-309

Martins CCA, Morete ME, Engel MH, Freitas AC, Secchi ER, Kinas PG (2001) Aspects of habitat use patterns of humpback whales in the Abrolhos Bank, Brazil, breeding ground.

Memoirs of the Queensland Museum 47:563-570.

Martins CCA, Andriolo A, Engel MH, Kinas PG, Saito CH (2013) Identifying priority areas for humpback whale conservation at Eastern Brazilian Coast. Ocean & Coastal Management

75:63-71. 35

Matkin CO, Durban JW, Saulitis EL, Andrews RD, Straley JM, Matkin DR, Ellis GM (2012)

Contrasting abundance and residency patterns of two sympatric populations of transient killer whales (Orcinus orca) in the northern Gulf of Alaska. Fishery Bulletin 110:143-155.

McDonald MA, Hildebrand JA, Webb SC (1995) Blue and fin whales observed on a seafloor array in the Northeast Pacific. Journal of the Acoustical Society of America 98:712-721.

Mellinger DK, Stafford KM, Fox CG (2004) Seasonal occurrence of sperm whale (Physeter macrocephalus) sounds in the Gulf of Alaska, 1999-2001. Marine Mammal Science 20:48-62.

Mellinger DK, Stafford KM, Moore SE, Dziak RP, Matsumoto H (2007) An overview of fixed passive acoustic observation methods for cetaceans. Oceanography 20:36-45.

Moore SE, Stafford KM, Melling H, Berchok C, Wiig O, Kovacs KM, Lydersen C, Richter-

Menge J (2012) Comparing marine mammal acoustic habitats in Atlantic and Pacific sectors of the High Arctic: year-long records from Fram Strait and the Chukchi Plateau. Polar

Biology 35:475-480.

Muanke PB, Niezrecki C (2007) Manatee position estimation by passive acoustic localization.

Journal of the Acoustical Society of America 121:2049-2059.

Newhall AE, Lin Y-T, Lynch JF, Baumgartner MF, Gawarkiewicz GG (2012) Long distance passive localization of vocalizing sei whales using an acoustic normal mode approach.

Journal of the Acoustical Society of America 131:1814-1825.

Parks SE, Johnson M, Nowacek D, Tyack PL (2010) Individual right whales call louder in increased environmental noise. Biology Letters doi:10.1098/rsbl.2010.0451.

Payne R, McVay S (1971) Songs of humpback whales. Science 173:585-597. 36

Pirotta E, Matthiopoulos J, MacKenzie M, Scott-Hayward L, Rendell L (2011) Modelling sperm whale habitat preference: a novel approach combining transect and follow data. Marine

Ecology Progress Series 436:257-272.

Rako N, Fortuna CM, Holcer D, Mackelworth P, Nimak-Wood M, Pleslic G, Sebastianutto L,

Vilibic I, Wiemann A, Picciulin M (2013) Leisure boating noise as a trigger for the displacement of the bottlenose dolphins of the Cres-Losinj archipelago (northern Adriatic Sea,

Croatia). Marine Pollution Bulletin 68:77-84.

Rayment W, Davidson A, Dawson S, Slooten E, Webster T (2012) Distribution of southern right whales on the Auckland Islands calving grounds. New Zealand Journal of Marine and

Freshwater Research 46:431-436.

Rodas-Trejo J, Romero-Berny EI, Estrada A (2008) Distribution and conservation of the West

Indian manatee (Trichechus manatus manatus) in the Catazajá wetlands of northeast Chiapas,

México. Tropical Conservation Science 1:321-333.

Santos MCO, Siciliano S, Vicente AFC, Alvarenga FS, Zampirolli É, Souza SP, Maranho A

(2010) Cetacean records along São Paulo state coast, southeastern Brazil. Brazilian Journal of

Oceanography 58:123-142.

Scheidat M, Friedlaender A, Kock K-H, Lehnert L, Boebel O, Roberts J, Williams R (2011)

Cetacean surveys in the Southern Ocean using icebreaker-supported helicopters. Polar

Biology 34:1513-1522.

Širović A, Hildebrand JA (2011) Using passive acoustics to model blue whale habitat off the

Western Antarctic Peninsula. Deep-Sea Research II 58:1719-1728. 37

Širović A, Hildebrand JA, Wiggins SM, Thiele D (2009) Blue and fin whale acoustic presence around Antarctica during 2003 and 2004. Marine Mammal Science 25:125-136.

Smith RC, Dustan P, Au D, Baker KS, Dunlap EA (1986) Distribution of cetaceans and sea- surface chlorophyll concentrations in the California Current. Marine Biology 91:385-402.

Sousa-Lima RS (2007) Acoustic ecology of humpback whales (Megaptera novaeangliae) in the Abrolhos National Marine Park, Brazil. PhD dissertation, Cornell University, Ithaca,

USA.

Sousa-Lima RS, Clark CW (2009) Whale sound recording technology as a tool for assessing the effects of boat noise in a Brazilian marine park. Park Science 26:59-63.

Sousa-Lima RS, Norris TF, Oswald JN, Fernandes DP (2013) A review and inventory of fixed autonomous recorders for passive acoustic monitoring of marine mammals. Aquatic

Mammals 39:23-53.

Stafford KM, Nieukirk SL, Fox CG (1999) Low frequency whale sounds recorded on hydrophones moored in the eastern tropical Pacific. Journal of the Acoustical Society of

America 106:3687-3698.

Sumich JL, Show IT (2011) Offshore migratory corridors and aerial photogrammetric body length comparisons of southbound Gray Whales, Eschrichtius robustus, in the Southern

California Bight, 1988-1990. Marine Fisheries Review 73:28-34.

Sveegaard S, Teilmann J, Berggren P, Mouritsen KM, Gillespie D, Tougaard J (2011)

Acoustic surveys confirm the high-density areas of harbour porpoises found by satellite tracking. ICES Journal of Marine Science 68:929-936. 38

Thode AM, D'Spain GL, Kuperman WA (2000) Matched-field processing, geoacoustic inversion, and source signature recovery of blue whale vocalizations. Journal of the

Acoustical Society of America 107:1286-1300.

Van Parijs SM, Clark CW, Sousa-Lima RS, Parks SE, Rankin S, Risch D, Van Opzeeland IC

(2009) Management and research applications of real-time and archival passive acoustic sensors over varying temporal and spatial scales. Marine Ecology Progress Series 395:21-36.

Verfuß UK, Honnef CG, Meding A, Dähne M, Mundry R, Benke H (2007) Geographical and seasonal variation of harbour porpoise (Phocoena phocoena) presence in the German Baltic

Sea revealed by passive acoustic monitoring. Journal of the Marine Biological Association of the United Kingdom 87:165-176.

Wahlberg M (2002) The acoustic behavior of diving sperm whales observed with a hydrophone array. Journal of Experimental Marine Biology and Ecology 281:53-62.

Watkins WA (1986) Whale reactions to human activities in Cape Cod waters. Marine

Mammal Science 2:251-262.

Ward J, Morrissey R, Moretti D, DiMarzio N, Jarvis S, Johnson M, Tyack P, White C (2008)

Passive acoustic detection and localization of Mesoplodon densirostris (Blainville’s Beaked

Whale) vocalizations using distributed bottom-mounted hydrophones in conjunction with a digital tag (DTAG) recording. Canadian Acoustics 36:60-66.

Weir CR (2010) A Review of cetacean occurrence in West African waters from the Gulf of

Guinea to Angola. Mammal Review 40:2-39. 39

Williams R, Thomas L (2007) Distribution and abundance of marine mammals in the coastal waters of British Columbia, Canada. Journal of Cetacean Research and Management 9:15-

28.

Williams R, Hedley SL, Branch TA, Bravington MV, Zerbini AN, Findlay KP (2011) Chilean blue whales as a case study to illustrate methods to estimate abundance and evaluate conservation status of rare species. Conservation Biology 25:526-535.

CAPÍTULO II - Spatial distribution of singing humpback whale groups in the Abrolhos Bank,

Bahia, Brazil.

Deborah P. Fernandes1, Renata S. Sousa-Lima1,2, Cristiane C. A. Martins3

1Universidade Federal do Rio Grande do Norte

2Cornell Lab of Ornithology

3Université de Montreal

MARINE MAMMAL SCIENCE (Qualis: B1, Impact factor: 2.128)

A ser submetido.

Spatial distribution of singing humpback whale groups in the Abrolhos Bank,

Bahia, Brazil

Deborah Pinto Fernandes

Bioacoustics Laboratory,

Federal University of Rio Grande do Norte,

Natal, RN, 59078-970, Brazil

Renata S. Sousa-Lima

Bioacoustics Laboratory,

Federal University of Rio Grande do Norte,

Natal, RN, 59078-970, Brazil

and

Bioacoustics Research Program,

Cornell Lab of Ornithology,

159 Sapsucker Woods Road, Ithaca, NY 14850, USA

Cristiane Cavalcante de Albuquerque Martins

Geography Department,

University of Montréal,

520 Chemin de la Côte de Saint Catherine, H2V 2B8, Montréal, Canada

RESUMO

A escolha de habitat é estabelecida a partir de interações entre fatores ambientais, a biologia da espécie e organização social dos indivíduos. Em baleias jubarte, tais interações são mediadas pelo som e por isso é importante investigar como grupos vocalmente ativos (VA) e vocalmente inativos (VI) estão espacialmente distribuídos. Uma pesquisa foi conduzida ao redor do arquipelago de Abrolhos durante as temporadas de 2004 e 2005. Monitoramento acústico em tempo real e observações diretas dos grupos de baleias foram conduzidos em embarcações de pesquisa. Localizações dos grupos foram gravadas com GPS e plotadas no

ArcGIS 9.3 para análises espaciais. Uma regressão logística utilizando profundidade, distância a uma área de entorno ao redor das ilhas (0.5 nm), distância a corais, tamanho de grupo e presença de filhote, foi executada para prever atividade vocal. Um total de 201 grupos foram monitorados acusticamente, resultando em 103 grupos VA e 98 grupos VI. O melhor modelo incluía presença de filhotes (B = .403, Wald = 4.263, p < .01), distância a corais (B =

.403, Wald = 4.263, p < .05) e profundidade (B = .079, Wald = 3.460, p > .05). Investigar as preferências de habitat para atividade vocal de baleias jubartes baseado em características ambientais e composição de grupo é importante para discutir áreas de restrição espaço- temporais com o objetivo de garantir a manutenção da comunicação acústica tão importante em áreas de reprodução e para a conservação das populaçõesao longo da costa brasileira.

Palavras-chave: baleia jubarte, Megaptera novaeangliae, distribuição, canto, atividade vocal, características ambientais, presença de filhote.

ABSTRACT

Habitat preferences are established by interactions among environmental factors, species biology and social organization. In humpback whales, such interactions can be mediated by sound, making it important to investigate how vocally active (VA) and inactive (VI) groups are spatially distributed. Real-time acoustic monitoring and direct observation of whale groups were conducted during vessel surveys around the Abrolhos Archipelago in the winters of 2004 and 2005. Group locations were recorded with GPS and plotted onto ArcGIS 9.3 for spatial analyses. A logistic regression using depth, distance to a buffer around the islands

(0.92 km), distance to reefs, group size and calf presence, was performed to predict vocal activity. A total of 201 groups were acoustically monitored, resulting in 103 VA groups and

98 VI groups. The best model included calf presence (B = .403, Wald = 4.263, p < .01), distance to reefs (B = .403, Wald = 4.263, p < .05) and depth (B = .079, Wald = 3.460, p >

.05). Investigating humpback whale habitat preferences for singing activity based on environmental characteristics and group composition is important in discussing spatio- temporal restriction areas aiming to ensure proper acoustic communication so important in nursing sites and the overall conservation of their populations along the Brazilian coast.

Key words: humpback whale, Megaptera novaeangliae, distribution, singing behavior, vocal activity, environmental characteristics, calf presence.

INTRODUCTION

The humpback whale, Megaptera novaeangliae (Borowski, 1781) is one of the most commonly studied species of baleen whales around the world (Norris et al. 1999). It is a cosmopolitan migratory species that has an affinity to traditional feeding grounds and nursing grounds that are close to shore habitats (usually close to coast lines or in continental shelf waters) (Dawbin 1966, Whitehead and Moore 1982, Clapham and Meade 1999). The humpback whale has a distinct temporal geographical distribution, performing great migrations that can exceed 8000 km one-way (Horton et al. 2011). This migrating behavior is thought to be organized based on factors such as social age or class (Chittleborough 1965,

Dawbin 1966, Dawbin 1997, Brown et al. 1995, Garrigue et al. 2000). Humpback whales are distributed in high-latitude habitats during the austral summer displaying mainly feeding behavior and during the winter they travel to tropical or subtropical waters known as breeding and calving grounds that present distinct geographical characteristics, such as bathymetry and sea surface temperature (Clapham 2000, Martins et al. 2001, Rasmussen et al. 2007, Lunardi et al. 2008, Martins et al. 2013).

The humpback whales' breeding stock "A", as defined by the International Whaling

Commission (IWC), occurs off the Brazilian coast during the austral winter (Zerbini et al.

2011a, Martins et al. 2013). The most important breeding and calving ground for the

Brazilian humpback whales population is the Abrolhos Bank (16º40' - 19º30'S), located off the coast of the state of Bahia, northeastern Brazil (Engel 1996, Martins et al. 2001).

When humpback whales are concentrated in breeding and calving areas, females have an unpredictable distribution (Clapham 1996) due to the lack of prey resources. Also, the lack of predation pressure in tropical habitats supports the tendency to find humpback whales mostly in pairs or alone, but they are also found in small unstable groups (Matilla and

Clapham 1989, Clapham 1992, Clapham and Meade 1999). In the Abrolhos Bank, the most frequently seen humpback whale group composition is that of dyads and mother-calf pairs

(Martins et al. 2001). Larger groups are generally considered competitive groups, where there can be one female, a principal escort and one or more secondary escorts (Tyack and

Whitehead 1983, Clapham 1996). Humpbacks are very well known for their complex behavioral patterns (Chlapham and Meade 1999, Clapham 2000). During the breeding and calving season, males are often displaying aggressive behaviors and also singing, which may be in order to gain access to and attract potential mates (Payne and McVay 1971, Tyack 1981,

Tyack and Whitehead 1983, Baker and Herman 1984, Clapham et al. 1992).

Not unlike other marine mammals, humpback whales rely on sound for communication. Even though females produce sounds (Simão and Moreira 2002), males are known for producing long, patterned sequences of sounds, commonly called "songs" (Payne and McVay 1971, Darling 1983, Cholewiak et al. 2012). Humpback whale songs have been recorded in several group compositions, such as competitive groups (Clapham et al. 1992), lone individuals (Darling 1983), pairs (Darling et al. 2006) and even in groups with calves

(Darling et al. 2006). Recent evidence found that mature and immature males sing, which can be a form of enhancing the acoustic signal, attracting a greater number of potential mates

(Herman et al. 2013). Although there have been records of humpback whale songs in feeding 46

grounds (Mattila et al. 1987, McSweeny et al. 1989, Clark and Clapham 2004) and along migration routes (Tyack and Whitehead 1983, Frankel et al. 1995, Norris et al. 1999, Noad et al. 2000), they are more commonly recorded in mating and calving areas (Norris et al. 1999,

Smith et al. 2008).

The song structure and patterns may be dependent on geographical, social and environmental characteristics which affect sound propagation (Mercado and Frazer 1999,

Cerchio et al. 2001, Darling and Sousa-Lima 2005, Darling et al. 2006, Sousa-Lima et al.

2010). It has been seen that males from a given population produce a particular song that may change collectively over time (Winn et al. 1981, Payne and Guinee 1983, Noad et al. 2000,

Cerchio et al. 2001, Darling et al. 2006, Garland 2011). Over the years, there have been several hypotheses trying to explain the purpose of the humpback whale song (Baker and

Herman, 1984, Clapham and Matilla 1990, Frankel et al. 1995, Frazer and Mercado 2000,

Darling and Bérubé 2001, Darling et al. 2006, Smith et al. 2008, Herman et al. 2013).

However, the most accepted hypothesis for the function of vocal displays is female attraction

(Winn and Winn 1978, Tyack 1981, Clapham 2000, Smith et al. 2008). There has also been evidence of females reacting to songs, supporting the intersexual function of songs in this species (Smith et al. 2008).

Although not many long-term studies have classified or described habitat use and distribution of humpbacks on wintering grounds, several studies show that humpback whales prefer warm, shallow and protected waters (Katona and Beard 1990, Ersts and Rosenbaum 47

2003). Habitat choice in breeding grounds is a function of behavior, biological needs and environmental conditions (Robbins et al. 2001), and it may also be due to social organization, where the distribution of different group types can be related to proximity to the coast and water depth (Clapham 2000, Martins et al. 2001, Ersts and Rosenbaum 2003).

Access to conspecifics may be a driving factor in habitat selection, influencing not only spatial distribution, but also behavior, reproductive success and gene flow (Ersts and

Rosenbaum 2003). Group characteristics such as age class, breeding states, presence or absence of calf in group can be important factors in how humpback whales are organized spatially (Félix and Haase 2005, Félix and Botero-Acosta 2011). In many areas such as the waters around Ecuador and Hawaii, groups of humpbacks are randomly distributed within depths of up to 200m (Craig and Herman 2000, Félix and Botero-Acosta 2011). Craig and

Herman (2000) found that, in Hawaii, female distribution is dependent on reproductive status.

They also found that groups with calves are most often found in shallow, protected waters, as has been seen in several other studies (Herman and Tavolga 1980, Craig and Herman 2000,

Martins et al. 2001, Félix and Botero-Acosta 2011).

According to Félix and Haase (2005), singleton subadults are also found in shallower waters, but groups of adults without calves are most likely found in deeper waters more distant from shore, a result also found by Betancourt et al. (2012). In breeding areas, males are expected to be distributed where females are most likely to be found, either in shallow areas (high concentration of females with calves) or in deeper waters where competitive 48

groups may aggregate in order to avoid collisions with the seabed and coral heads (Jones and

Swartz 1984, Martins et al. 2001).

Previous studies have taken into consideration many environmental variables, such as sea surface temperature, depth, slope, month, salinity, and others to use as predictors of cetacean habitat and distribution in feeding grounds (Smith et al. 1986, Hooker et al. 1999,

Gregr and Trites 2001). However, it was found that the predictive power of most variables was relatively weak.

Ersts and Rosenbaum (2003) developed a long-term study that took place in the

Antogil Bay, Madagascar, wintering ground and found that depth and distance from shore were the most relevant variables for predicting habitat and distribution of humpback whales.

Studies that took place in the Bering Sea and off northern Washington coast, found an association between humpback whales and bathymetry (Moore et al. 2002). Long term studies with North Atlantic and North Pacific humpback whale populations found that these animals prefer warm, shallow and protected areas on wintering grounds (Simmons and Marsh 1986,

Mattila et al. 1989).

Areas known as breeding grounds, where mating and calving take place, are usually composed of offshore reef systems, banks, continental shores, or are associated with islands.

In these areas, congregations of relatively high densities of whales can be observed in localized regions (Ersts and Rosenbaum 2003, Martins et al. 2013). 49

A lot of research has been done trying to describe habitat preferences and spatial distribution of humpback whales including different group compositions on both feeding and breeding grounds (Simmons and Marsh, 1986, Matilla et al. 1989, Frankel et al. 1995, Craig and Herman 2000, Martins et al. 2001, Moore et al. 2002, Ersts and Rosenbaum 2003, Félix and Botero-Acosta 2011, Rossi-Santos 2012). There are many aspects that can determine singing males’ spatial distribution. It is suggested that humpback whale males aggregate in a lek mating system, where the song may function as an intersexual signal (Herman and

Tavolga 1980, Clapham 1996, Cerchio 1999, Cerchio et al. 2001). Male singing behavior is also subject to the complex shallow water sound propagation in most breeding grounds, which can also be related to other physical characteristics of the ocean, such as temperature and depth profiles (Sousa-Lima 2007). Frankel et al. (1995) found that, in Hawaii, singing males are more likely concentrated in areas close to coast, even though they may be found in deeper waters. However, there has not yet been a study focusing on describing humpback whale male singers' distribution in relation to environmental characteristics as well as group composition, which is the main purpose of this study.

Environmental characteristics such as depth profile, distance to coast and presence of corals may affect the efficiency in sound propagation, therefore influencing where males would prefer to sing. Also, social differences in group sizes and composition, for example, presence of calves in a group, may also be an important factor in determining where or if there will be males singing in the group. The purpose of this study was to predict the distribution of vocally active humpback whale groups in relation to environmental and social variables around the Abrolhos Archipelago. 50

METHODS

Study site

The Abrolhos Bank is considered the most important breeding and calving site for humpback whales in the Southwestern Atlantic (Engel 1996, Martins et al. 2001), with the current population estimated between 6,000-10,000 individuals (Andriolo et al. 2010, Zerbini et al. 2011b). The Abrolhos Bank is located off the coast of Brazil between 16°40’-19°30’S, covering an area of approximately 30,000 km² (Figure 1). The ocean bottom of this area has a mean depth of 30 m and is made up of coral reefs, mud, sand and calcareous algae (Fainstein and Summerhayes 1982). The coral reefs in the Abrolhos Bank grow as large columns that can sometimes reach sea level (Leão et al. 2002). The Abrolhos Archipelago is located in the northern portion of the Abrolhos Bank, within the Abrolhos National Marine Park (ANMP ).

The bathymetry surface used for this study (Figure 1) is based on depth measurements from approximately 1,793 GPS points taken during research surveys using either a hand-held depth finder or the echo-sounder from the research boats as described in Sousa-Lima (2007).

The original depth measurement points were projected to UTM WGS 1984 Zone 24S. The surface was generated by Zev Ross who modeled the variogram in R using the GSTAT library (spherical model with a nugget of 0, range of 8,960.9 and sill of 128.51). These parameters were used in ArcGIS Geostatistical Analyst to create a surface using ordinary kriging and 40 lags of 750 m each. The kriged surface was exported to a grid of 50 m x 50 m resolution. The layer of the coral reefs was obtained as described in Moura et al. (2013) and shows the reefs exposed during the low tide as well as the submerged reefs, with a buffer area already represented area around them. 51

Figure 1 - Bathymetry map of the surveyed area.

Data acquisition on humpback whale singers

The humpback whale data was collected during the breeding and calving seasons of the years 2004 and 2005. Visual vessel based surveys were conducted around the Abrolhos

Archipelago area with the purpose of registering behavioral data on humpback whale groups.

At all times, two observers were aboard the vessels and registered group behavior, size and composition, GPS positions and acoustic activity (Sousa-Lima 2007). This data was further used in order to also describe humpback whale distribution.

Acoustic data was collected using a combination of one hydrophone (HTI-90 or HTI-

96 MIN) and one recorder (Sony DAT D8 or Marantz PMD670 Solid State, 20 kHz frequency response). When a group was first sighted, the hydrophone was deployed into the water and the observers began monitoring the sound to see if the whale group was vocally active or inactive. In order two know if the group being acoustically monitored was in fact the group being observed, two cues were used. First, if the sound level being recorded increased as the boat approached the group and second, if the sound attenuated when an individual in the group surfaced (the singer). If there was any ambiguity or uncertainty even with the cues, the data were not used for analyses. Several GPS positions were taken for each group during these surveys, however, only one position was used for each group and that was the closest position to the group.

Data analyses

Data on humpback whale group positions were plotted onto the program ArcMap from the ArcGIS® 9.3 package, in order to attribute environmental data to each group position

(Figure 2). The environmental variables used were depth (from the bathymetry layer described above), shortest distance of each group to a buffer of 0.92 km around the islands and distance to coral reefs (buffer area according to Moura et al. 2013), both obtained using the Buffer tool in the Spatial Analyst Extension of ArcGIS®. The buffer around the islands was used in order to consider the archipelago as a whole, instead of individual islands.

Figure 2 - Distribution of humpback whale groups around the Abrolhos Archipelago.

In addition, some group social characteristics were also taken into consideration, as: group size, presence of calf in group and vocal activity (active or inactive). The different types of groups compositions were defined sensu Martins et al. (2001): individual (referred to as SOL); pair (referred to as PA); competitive group (referred to as CG); mother and calf

(referred to as MoCa); competitive group with a mother-calf pair (MoCaCG); mother and calf with principal escort (referred to as MoCaPe). Once the environmental variables were attributed to each group location the data was statistically analyzed using the program PASW

18.0 (SPSS Inc. 2009). A logistic regression (backward stepwise method) was performed in 54

order to identify which variables (depth, distance to islands buffer, distance to coral reefs, group size and presence of calf in group) best predicted habitat use.

The logistic regression analysis is used to predict which of two categories (vocal active or inactive) a group is most likely to belong given the predicting variables. The backward stepwise logistic regression runs a full model with all the variables entered. At each step, the program removes the variable that is least significant to the model. The final step will be the one where removing variables will no longer have a significant difference in the model (p < 0.001) and therefore will be the model that best predicts the dependent variable

(Burns and Burns 2008, Field 2009).

RESULTS

A total of 201 humpback whale groups and 493 individuals were sighted during this survey. From the total, 103 were vocally active groups and 98 were vocally inactive (Figure

3). Of the vocally active groups (n = 103), 72% did not have calves present (n = 74) and 28% had calves present (n = 29). Of the remaining vocally inactive groups (n = 98), 43% did not have calves present (n = 42) and 57% had calves present (n = 56).

For each group category a different level of vocal activity can be observed, that is, they can have more or less vocal activity going on (Figure 3). Mother and calf (MoCa) groups were the ones who showed the smallest occurrence of vocal activity. However, in groups with calves and the presence of principal and secondary escorts, the percentage of vocal activity 55

was higher. Solitary individuals were the group composition with the highest percentage of vocal activity.

Figure 3 - Count of different group compositions' vocal activity (MoCaPe: mother and calf with principal escort; PA: pair: SOL: individual; CG: competitive group; MoCaCG: competitive group with a mother-calf pair; MoCa: mother and calf).

The average group size was 2.45 (SD = 1.38, n = 201) with the smallest group containing 1 individual and the largest, containing 11 individuals. The average distance of whale groups to the islands buffer was of 10.54 km (SD = 11.00 km, n = 201) with the 56

minimum distance of 0 km, that is, the group was located within the buffer and the maximum distance was 43.19 km away from the buffer. The average distance to reefs was of 0.41 km

(SD = 0.85 km, n = 201), with a minimum distance of 0 km and a maximum of 4.78 km. The average depth was of 19.82 m (SD = 3.76, n = 201) with a minimum depth of 8 m and a maximum of 33 m (Table 1).

Table 1 - Descriptive statistics

Distance to Distance to Vocal Islands Group Size Depth Calf Presence Reefs Activity Buffer

201 201 201 201 201 201 Valid n Missing 0 0 0 0 0 0

Mean 10.54 2.45 19.82 0.41 .42 .51

Standard Error of 0.77 0.09 0.26 0.06 .03 .03 Mean

Median 5.90 2.00 20.00 0.00 .00 1

Mode 0.00 2.00 19.00 0.00 0 1

Standard Deviation 11.00 1.38 3.76 0.85 .49 .49 (SD)

Minimum 0.00 1.00 8.00 0.00 0 0

Maximum 43.19 11.00 33.00 4.78 1 1

A logistic regression analysis was conducted to predict vocal activity of 201 humpback whale groups using depth, distance to shore, distance to reefs, presence of calf and group size as predictors (Table 2). Three models are presented, the dependent variable in each is whether the humpback whale group would be vocally active or inactive (VA = 1, VI = 0). 57

Each model includes different combinations of independent variables, always removing the variable with the smallest power of prediction from one model to the other.

In the first model (Table 2), the variable with the smallest power of prediction was

Distance to Islands (B = .014, Wald = .527, p > .05) and for this reason, it was the variable removed in order to obtain the second model. Group Size had a small predictive power in

Model 2 (B = .118, Wald = .924, p > .05) and therefore, it was removed in order to obtain

Model 3.

The most parsimonious model includes the variables that best predict vocal activity, which are: Calf Presence (B = 1.234, Wald = 16.016, p < .01), Distance to Reefs (B = .403,

Wald = 4.263, p < .05) and Depth (B = .079, Wald = 3.460, p > 0.05). In this model, the variable Depth does not have a high predictive power, however, removing this variable to obtain a fourth model did not create a significant difference (p > .05) and for this reason, the iterations stopped at Model 3.

Table 2 - Logistic regression analysis predicting vocal activity from (N = 201)

Model 1 Model 2 Model 3

Predictors B SE B Wald B SE B Wald B SE B Wald

(Constant) 2.670 .964 7.677 2.765 .958 8.330 2.399 .877 7.477

Calf Presence 1.325 .326 16.512 ** 1.323 .308 16.574 ** 1.234 .308 16.016 **

Distance to reefs .297 .247 1.437 .409 .196 4.358 * .403 .195 4.263 *

Depth .071 .045 2.515 .081 .043 3.551 .079 .043 3.460

Group Size .119 .124 .921 .118 .123 .924

Distance to islands .014 .019 .527

Nagelkerke R² .173 .170 .164

Chi-square (df) 27.856** 27.325** 26.322**

Note: * p < .05, ** p < .01

DISCUSSION

Habitat preference is mediated by a number of different variables, a combination of social and behavioral patterns all allied with the characteristics of the environment (Robbins et al. 2001). Large whales distribution may be a function of factors such as prey distribution, depth, temperature and physical characteristics of both feeding and breeding grounds (Davis et al. 2002). Defining these patterns is very complicated when studying large whales, seeing as they can be inconspicuous, very mobile and have dynamic social interactions (Ersts and

Rosenbaum 2003).

Humpback whales aggregate in the study area in order to mate, give birth and nurse.

Habitat use and social organization can be used for studying spatial patterns. During migration, it has been seen that humpback whales may organize themselves differently. There has been evidence of sex-segregated migration (Brown et al. 1995), but also a temporal segregation, where individuals of different age and reproductive statuses migrate separately

(Baker and Herman 1981). As has been seen in previous studies, social structures that are associated with breeding and calving behaviors are important variables in determining humpback whales spatial distribution (Baker and Herman 1981, Brown et al. 1995, Ersts and

Rosenbaum 2003).

Previous studies on humpback whale distribution aimed to describe locations where whales were found or to provide subjective information on habitat use (Ersts and Rosenbaum

2003). Aside from the variables used in this study, several other surveys also used sea surface temperature, wind speed, tide height, presence or absence of prey and data obtained from satellites (Moses and Finn 1997, Davis et al. 2002, Félix and Botero-Acosta 2011). In many studies, depth has been seen to be one of the most informative variables when trying to explain humpback whales spatial patterns (Hooker et al. 1999, Gregr and Trites 2001).

In this study, the model that best predicted vocally active groups around the Abrolhos

Archipelago included Calf Presence, Distance to Reefs and Depth. That is, in general, vocally active groups will less likely have calves, will be farther away from coral reefs and in shallower waters. 60

We have found that the presence or absence of a calf in a group is a highly predictive variable for vocal activity. What this tells us is that when there is a calf present in the group, it is most likely that there will not be an active singer present. Even though there has been a record of a mother and calf pair producing vocalizations, they have not yet been documented singing (Simão and Moreira 2005). Mother and calf pairs are most likely found in shallow waters (Martins et al. 2001, Félix and Botero-Acosta 2011) and this group composition might not only have an effect on singing, but also on distribution of humpback whales. Shallow waters may be ideal for mothers to be located with their calves, but the small water column is not adequate for courting males (Smultea 1994, Ersts and Rosenbaum 2003). Females might prefer shallow waters in order to avoid collisions with the seabed and possible harassment by males, disrupting nursing, injuring or separating calves from their mothers (Smultea 1994,

Elwen and Best 2004). Félix and Botero-Acosta (2011) suggest that different groups may show discrete reproductive strategies when responding to social and environmental conditions. Even though females mate post partum, they are not the ideal partner for courting males (Smultea 1994). Locations where mature females that are fit for mating are found may determine the main singing areas (Frankel et al. 1995).

Distribution of humpback whale singers may be affected not only by social conditions, but also by different environmental characteristics. Our results differ in some aspects (e.g. the use of the vocal component) to other similar studies where humpback whale distribution was highly associated with bathymetry (Gregr and Trites 2001, Dalla Rosa et al. 2012). In the

Abrolhos Archipelago, depth was not found to be a significant variable (p > .05) when predicting humpback whales singers distribution. This may be due to geographical variation 61

and specific environmental characteristics of the area. The bathymetry in Abrolhos is very constant, with an average depth of 19.82 m (SD = 3.76 m), and may be why this variable had a low predictive power in the model. However, the study area was composed of only a small area of the Abrolhos Bank, perhaps if we took into consideration the whole Bank, we could present a different result. For this reason, it is necessary to obtain data on other parts of

Abrolhos to have a more precise result.

Effective acoustic communication in the ocean is highly dependent on how sound propagates in the medium. The sound already suffers attenuation due to geometrical loss, medium absorption and scattering. Another factor that can influence effective sound propagation is the presence of physical barriers which can modify the structure of the sound

(Urick 1983, Richardson et al. 1995). Deeper waters with no presence of coral reefs or other physical barriers would be ideal for sound propagation (Frankel et al. 1995). We found that the distance of a group to a coral reef formation influenced whether or not that group would have an active singer present (B = .403, Wald = 4.263, p < .05). That is, the closer the group was to coral reefs, less likely it would be that there would be vocal activity going on. Coral reefs in the Abrolhos area are the largest and richest coral reefs in Brazil (Leão 2002). The large coral columns that can reach sea level occupy a large area around the Abrolhos Bank and can act as physical barriers that can alter characteristics of sounds emitted by humpbacks

(Richardson et al. 1995). It is possible that singers avoid these formations in order to maximize effective communication without further modifications of the sound structure, by singing in areas without the presence of coral reefs.

The present study focused on a small portion of the main breeding area for humpback whales off the Brazilian coast. It would be interesting to expand the study to be representative of the different portions of the Abrolhos bank and take into consideration other variables such as wind speed, salinity, temperature and others. Further investigations of habitat preferences for vocal activity of humpback whales based on environmental factors might guide the discussion of spatio-temporal restriction areas aiming to ensure the acoustic communication so important as a mechanism facilitating breeding success. Sound travels in water much more efficiently than in air, allowing for an even larger geographical scale of impact from anthropogenic noise (Agardy et al. 2007). Only mature males have real chances in mating and the interactions with females that can become potential mates are mediated by songs (Herman et al. 2013). The use of spatio-temporal restrictions has been seen to be one of the most effective ways to protect cetaceans (Barlow and Gisiner 2006, Weilgart 2006). However, these restrictions depend highly on the availability of data regarding the species of interest

(Agardy et al. 2007). Therefore, it is important to take into consideration, not only distribution of humpback whales on feeding and breeding grounds, but also acoustic behaviors in order to guarantee the conservation of the species along the Brazilian coast.

ACKNOWLEDGEMENTS

This work was supported by the Canon National Parks Scholars Program, Animal

Behavior Society, Society for Marine Mammalogy and the the Coordination of Improvement of Higher Education Personnel (CAPES). Many thanks to Wallisen Tadashi Hattori for the input on the statistical analysis.

LITERATURE CITED

Agardy, T., N. Aguilar, A. Cañadas, et al. 2007. A global scientific workshop on spatio- temporal management of noise. Report of the Scientific Workshop, 51+vii pp.

Andriolo, A., P. G. Kinas, M. H. Engel, C. C. A. Martins and A. M. Rufino. 2010. Humpback whales within the Brazilian breeding ground: distribution and population size estimate.

Endangered Species Research 11:233-243.

Baker, C. S. and L. M. Herman. 1984. Seasonal contrasts in the social behavior of the humpback whale. Cetus 5:14-16.

Barlow, J and R. Gisiner. 2006. Mitigating, monitoring and assessing the effects of anthropogenic sound on beaked whales. Journal of Cetacean Research and Management

7:239-251.

Betancourt, L., A. Herrera-Moreno and K. Beddal. 2012. Spatial distribution of humpback whales in Samaná Bay, Dominican Republic. Journal of Cetacean Research and Management

SC/64/O12.

Brown, M R., P. J. Corkeron, P. T. Hale, K. W. Schultz and M. M. Bryden. 1995. Evidence for a sex-segregated migration in the humpback whale (Megaptera novaeangliae).

Proceedings of the Royal Society of London B 259:229-234.

Burns, R. and R. Burns. 2008. Business research methods and statistics using SPSS. Sage

Publications Inc., London.

Cerchio, S. 1999. Do humpback whales lek? Thirteenth Biennial Conference on the Biology of Marine Mammals, Maui, Hawaii, USA. 64

Cerchio, S., J. K. Jacobsen and T. F. Norris. 2001. Temporal and geographical variation in songs of humpback whales, Megaptera novaeangliae: synchronous change in Hawaiian and

Mexican breeding assemblages. Animal Behaviour 62:313-329.

Chittleborough, R. G. 1965. Dynamics of two populations of the humpback whale, Megaptera novaeangliae (Borowski). Australian Journal Marine Freshwater Research 16:33-128.

Cholewiak, D. M., R. S. Sousa-Lima and S. Cerchio. 2012. Humpback whale song hierarchical structure: historical context and discussion of current classification issues. Marine

Mammal Science 29:E312-E332.

Clapham, P. J. 1992. The attainment of sexual maturity in humpback whales. Canadian

Journal of Zoology 70:1470-1472.

Clapham, P. J. 1996. The social and reproductive biology of humpback whales: An ecological perspective. Mammal Review 26:27-49.

Clapham, P. J. 2000. The humpback whale: seasonal feeding and breeding in a baleen whale.

Pages 173-196 in J. Mann, R. C. Connor, P. L. Tyack, H. Whitehead, eds. Cetacean Societies

- field study of dolphins and whales. University of Chicago Press, Chicago.

Clapham, P. J. and D. K. Mattila. 1990. Humpback whale songs as indicators of migration routes. Marine Mammal Science 6:155-160.

Clapham, P. J. and J. G. Mead. 1999. Megaptera novaeangliae. Mammalian Species 604:1-9.

Clapham, P. J., P. J. Palsbøll, D. K. Matilla and O. Vásquez. 1992. Composition and dynamics of humpback whale competitive groups in the West Indies. Behaviour 122:182-194. 65

Clark, C. W. and P. J. Clapham. 2004. Acoustic monitoring on a humpback whale

(Megaptera novaeangliae) feeding ground show continual singing into late Spring.

Proceedings of the Royal Society B 271:1051-1057.

Craig, A. S. and L. M. Herman. 2000. Habitat preferences of female humpback whales

Megaptera novaeangliae in the Hawaiian Islands are associated with reproductive status.

Marine Ecology Progress Series 193: 209-216.

Dalla Rosa, L., J. K. B. Ford and A. W. Trites. 2012. Distribution and relative abundance of humpback whales in relation to environmental variables in coastal British Columbia and adjacent waters. Continental Shelf Research 36:89-104.

Darling, J. D. 1983. Migrations, abundance and behaviour of Hawaiian humpback whales

(Megaptera novaeangliae). Ph.D. thesis, University of California, Santa Cruz.

Darling, J. D. and M. Bérubé. 2001. Interactions of singing humpback whales with other males. Marine Mammal Science 17:570-584.

Darling, J. D. and R. S. Sousa-Lima. 2005. Songs indicate interaction between humpback whale (Megaptera novaeangliae) populations in the Western and Eastern South Atlantic

Ocean. Marine Mammal Science 21:557-566.

Darling, J. D., M. E. Jones and C. P. Nicklin. 2006. Humpback whale songs: Do they organize males during the breeding season? Behaviour 143:1051-1101.

Davis, R. W., J. G. Ortega-Ortiz, C. A. Ribic, et al. 2002. Cetacean habitat in the northern oceanic Gulf of Mexico. Deep-Sea Research Part I Oceanographic Research Papers 49:121-

142. 66

Dawbin, W. H. 1966. The seasonal migratory cycle of humpback whales. Pages 145-170 in K.

S. Norris ed. Whales, dolphins and porpoises. University of California Press, Los Angeles.

Dawbin, W. H. 1997. Temporal segregation of humpback whales during migration in

Southern Hemisphere waters. Memoirs of the Queensland Museum 42:105-138.

Elwen, S. H. and P. B. Best. 2004. Female southern right whales Eubalaena australis: are there reproductive benefits associated with their coastal distribution off South Africa? Marine

Ecology Progress Series 269:289-295.

Engel, M. 1996. Comportamento reprodutivo da Baleia Jubarte (Megaptera novaeangliae) em

Abrolhos. Anais de Etologia 275-284.

Ersts, P. J. and H. C. Rosenbaum. 2003. Habitat preference reflects social organization of humpback whales (Megaptera novaeangliae) on a wintering ground. Journal of Zoology

260:337-345.

Fainstein, R. and C. P. Summerhayes. 1982. Structure and origin of marginal banks off eastern Brazil. Marine Geology 46:199-215.

Félix, F. and B. Haase. 2005. Distribution of humpback whales along the coast of Ecuador and management implications. Journal of Cetacean Research and Management 7:21-31.

Félix, F. and N. Botero-Acosta. 2011. Distribution and behaviour of humpback whale mother- calf pairs during the breeding season off Ecuador. Marine Ecology Progress Series 426:277-

287.

Field, A. 2009. Descobrindo a estatística usando o SPSS. Artmed, Porto Alegre. 67

Frankel, A. S., C. W. Clark, L. M. Herman and C. Gabriele. 1995. Spatial distribution, habitat utilization, and social interactions of humpback whales, Megaptera novaeangliae, off Hawai'i determined using acoustic and visual techniques. Canadian Journal of Zoology 73:1134-1146.

Frazer, L. N. and E. Mercado. 2000. A sonar model for the humpback whale song. Journal of

Oceanic Engineering 25:160-181.

Garland, E. C. 2011. Cultural transmission of humpback whale song and metapopulation structure in the South Pacific Ocean. PhD thesis, University of Queensland, Queensland,

Australia, 208 pp.

Garrigue, C., P. Forestell, J. Greaves, P. Gill, P. Naessig, N. M. Patenaud and C. S. Baker.

2000. Migratory movements of humpback whales (Megaptera novaeangliae) between New

Caledonia, East Australia and New Zealand. Journal of Cetacean Research and Management

2:111-115.

Gregr, E. J. and A. W. Trites. 2001. Predictions of critical habitat for five whale species in the waters of coastal British Columbia. Canadian Journal of Fisheries and Aquatic Science

58:1265-1285.

Herman, L. M. and W. N. Tavolga. 1980. The communication systems of cetaceans. Pages

149-209 in: L. M. Herman ed. Cetacean Behavior: Mechanisms and Functions. Krieger

Publishing Co., Malabar.

Herman, L. M., A. A. Pack, S. S. Spitz, E. Y. K. Herman, K. Rose, S. Hakala and M. H.

Deakos. 2013. Humpback whale song: who sings? Behavioral Ecology and Sociobiology

67:1653-1663. 68

Hooker, S. K., H. Whitehead and S. Gowans. 1999. Marine protected area design and the spatial and temporal distribution of cetaceans in a submarine canyon. Conservation Biology

13:592-602.

Horton, T. W., R. N. Holdaway, A. N. Zerbini, N. Hauser, C. Garrigue, A. Andriolo and P. J.

Clapham. 2011. Straight as an arrow: humpback whales swim constant course tracks during long-distance migration. Biology Letters doi: 10.1098/rsbl.2011.0279.

Jones, M. L. and S. L. Swartz. 1984. Demography and phenology of Gray whales and evaluation of whale-watching activities in Laguna San Ignacio, Baja California Sur, Mexico.

Pages 309-374 in Jones, M. L., S. L. Swartz and S. Leatherwood eds. The gray whale

Eschrichtius robustus. Academic Press Inc., Orlando.

Katona, S. K. and J. A. Beard. 1990. Population size, migrations and feeding aggregations of the humpback whale (Megaptera novaeangliae) in the Western North Atlantic Ocean. Reports of the International Whaling Commission Special Issue 12:295-305.

Leão, Z. M. A. N. 2002. Abrolhos, BA: O complexo recifal mais extenso do Atlântico Sul.

Pages 345-359 in Schobenhaus, C., D. A. Campos, E. T. Queiroz, M. Winge and M. Berbert-

Born eds. Sítios geológicos e paleontológicos do Brasil. DNPM/CPRM - Comissão Brasileira de Sítios Geológicos e Paleobiológicos (SIGEP), Brasília.

Lunardi, D. G., M. E. Engel and R. H. F. Macedo. 2008. Behavior of humpback whales,

Megaptera novaeangliae (Cetacea: Balaenopteridae): comparisons between two coastal areas of Brazil. Revista Brasileira de Zoologia 25:159-164. 69

Martins, C. C. A., M. E. Morete, M. H. Engel, A. C. Freitas, E. R. Secchi and P. G. Kinas.

2001. Aspects of habitat use patterns of humpback whales in the Abrolhos Bank, Brazil, breeding ground. Memoirs of the Queensland Museum 47:563-570.

Martins, C. C. A., A. Andriolo, M. H. Engel, P. G. Kinas and C. H. Saito. 2013. Identifying priority areas for humpback whale conservation at Eastern Brazilian Coast. Ocean & Coastal

Management 75:63-71.

Mattila, D. K., L. N. Guinee and C. A. Mayo. 1987. Humpback whale sounds on the North

Atlantic feeding grounds. Journal of Mammalogy 68:880-883.

Mattila, D. K. and P. J. Clapham. 1989. Humpback whales, Megaptera novaeangliae, and other cetaceans on Virgin Bank and in the northern Leeward Islands, 1985 and 1986.

Canadian Journal of Zoology 67:2201-2211.

Mattila, D. K., P. J. Clapham, S. K. Katona and G. S. Stone. 1989. Population composition of humpback whales (Megaptera novaeangliae) on Silver Bank. Canadian Journal of Zoology

67:281-285.

Mercado, E. III and L. N. Frazer. 1999. Environmental constraints on sound transmission by humpback whales. Journal of the Acoustical Society of America 106:3004-3016.

McSweeny, D. J., K. C. Chu, W. F. Dolphin and L. N. Guinee. 1989. North Pacific humpback whale songs: a comparison of southeast Alaskan feeding ground songs with Hawaiian wintering ground songs. Marine Mammal Science 5:139-148. 70

Moore, S. E., J. M. Waite, N. A. Friday and T. Honkalehto. 2002. Cetacean distribution and relative abundance on the central-eastern and the southern Bering Sea shelf with reference to oceanographic domains. Progress in Oceanography 55:249-261.

Moses, E. and J. T. Finn. 1997. Using geographical information systems to predict North

Atlantic right whale (Eubalaena glacialis) habitat. Journal of Northwest Atlantic Fishery

Science 22:37-46.

Moura, R. L., N. A. Secchin, G. M. Amado-Filho, et al. 2013. Spatial patterns of benthic megahabitats and conservation planning in the Abrolhos Bank. Continental Shelf Research

70:109-117.

Noad, M. J., D. H. Cato, M. M. Bryden, M.-N. Jenner and K. C. S. Jenner. 2000. Cultural revolution in whale songs. Nature 408:537.

Norris, T. F., M. McDonald and J. Barlow. 1999. Acoustic detections of singing humpback whales (Megaptera novaeanligae) in the eastern North Pacific during their northbound migration. Journal of the Acoustical Society of America 106:506-514.

Payne, R. S. and S. McVay. 1971. Songs of Humpback Whales. Science 173:585-597.

Payne, R. S. and L. N. Guinee. 1983. Humpback whale (Megaptera novaeangliae) songs as an indicator of "stocks". Pages 333-358 in R. Payne ed. Communication and behavior of whales: AAAS Selected Symposium 76. Westerview Press, Boulder, CO.

Rasmussen, K., D. M. Palacios, J. Calambokidis, M. T. Saborío, L. Dalla Rosa, E. R. Secchi,

G. H. Steiger, J. M. Allen and G. S. Stone. 2007. Southern Hemisphere humpback whales 71

wintering off Central America: insights from water temperature into the longest mammalian migration. Biology Letters 3:302-305.

Richardson, W. J., C. R. Greene Jr., C. I. Malme and D. H. Thomson. 1995. Marine Mammals and Noise. Academic Press, San Diego.

Robbins, J., M. Bérubé, P. J. Clapham, N. Friday and D. Mattila. 2001. Structure and regional composition of the Gulf of Maine humpback whale (Megaptera novaeangliae) population.

International Whaling Commission Conference, C/53/NAH12:1-11.

Rossi-Santos, M. R. 2012. Comportamento e ecologia acústica da baleia Jubarte (Megaptera novaeangliae) na região Nordeste do Brasil. Tese de Doutorado, Universidade Federal do Rio

Grande do Norte, Natal, RN, 173 pp.

Simão, S. M. and S. C. Moreira. 2002. Sound emissions from a female humpback whale in

Arraial do Cabo (RJ, Brazil). Bioacousitcs 13:201.

Simmons, M. L. and H. Marsh. 1986. Sightings of humpback whales in Great Barrier Reef waters. The Scientific Reports of the Whales Research Institute 37:31-46.

Smith, R. C., P. Dustan, D. Au, K. S. Baker and E. A. Dunlap. 1986. Distribution of cetaceans and sea-surface chlorophyll concentrations in the California Current. Marine Biology 91:385-

402.

Smith, J. N., A. W. Goldizen, R. A. Dunlop and M. J. Noad. 2008. Songs of humpback whales, Megaptera novaeangliae, are involved in intersexual interactions. Animal Behaviour

76:467-477. 72

Smultea, M. A. 1994. Segregation by humpback whale (Megaptera novaeangliae) cows with a calf in coastal habitat near the Island of Hawaii. Canadian Journal of Zoology 72:805-811.

Sousa-Lima, R. S. 2007. Acoustic ecology of humpback whales (Megaptera novaeangliae) in the Abrolhos National Marine Park, Brazil. Ph.D. thesis, Cornell University, Ithaca, NY. 205 pp.

Sousa-Lima, R. S., K. A. Cortopassi and C. W. Clark. 2010. Humpback whale posture and song propagation in very shallow water. Journal of the Acoustical Society of America

128:2467.

SPSS Inc. 2009. PASW Statistics for Windows, Version 18.0. SPSS Inc., Chicago.

Tyack, P. 1981. Interactions between singing Hawaiian humpback whales and conspecifics nearby. Behavioral Ecology and Sociobiology 8:105-116.

Tyack, P. and H. Whitehead. 1983. Male competition in large groups of wintering humpback whales. Behaviour 83:132-154.

Urick, R. J. Principles of Underwater Sound. 3ed. Peninsula Publishing, Los Altos.

Weilgart, L. S. 2006. Managing noise through Marine Protected Areas around Global Hot

Spots. IWC Scientific Committee SC/58/E25.

Whitehead, H. and M. J. Moore. 1982. Distribution and movements of West Indian humpback whales in winter. Canadian Journal of Zoology 60:2203-2211.

Winn, H. E. and L. K. Winn. 1978. The song of the humpback whale, Megaptera novaeangliae, in the West Indies. Marine Biology 47:97-114. 73

Winn, H. E., T. J. Thompson, W. C. Cummings, J. Hain, J. Hudall, H. Hays and W. W.

Steiner. 1981. Song of the humpback whale - population comparisons. Behavioral Ecology and Sociobiology 8:41-46.

Zerbini, A. N., A. Andriolo, A., M. P. Heide-JØrgensen, et al. 2011a. Migration and summer destinations of humpback whales (Megaptera novaeangliae) in the western South Atlantic

Ocean. Journal of Cetacean Research and Management Special Issue 3:113-118.

Zerbini, A. N., E. J. Ward, P. G. Kinas, M. H. Engel A. Andriolo. 2011b. A Bayesian assessment of the conservation status of humpback whales (Megaptera novaeangliae) in the western South Atlantic Ocean. Journal of Cetacean Research and Management 3:131-144.

CAPÍTULO III - Spatial overlap in distributions of vessel traffic and humpback whale singers in the navigation corridor to the Abrolhos National Marine Park

Deborah P. Fernandes1, Renata S. Sousa-Lima1,2, Cristiane C. A. Martins3

1Universidade Federal do Rio Grande do Norte

2Cornell Lab of Ornithology

3Université de Montreal

OCEAN & COASTAL MANAGEMENT (Qualis: A2, Impact factor: 1.747)

A ser submetido.

Spatial and acoustic overlaps of vessel traffic and humpback whale singers in

the navigation corridor to the Abrolhos National Marine Park

Deborah Pinto Fernandes*

Bioacoustics Laboratory,

Federal University of Rio Grande do Norte

Natal, RN, 59078-970, Brazil

Renata S. Sousa-Lima

Bioacoustics Laboratory,

Federal University of Rio Grande do Norte

Natal, RN, 59078-970, Brazil

and

Bioacoustics Research Program,

Cornell Lab of Ornithology,

159 Sapsucker Woods Road, Ithaca, NY 14850, USA

Cristiane Cavalcante de Albuquerque Martins

Geography Department,

University of Montreal,

520 Chemin de la Côte de Saint Catherine, H2V 2B8, Montréal, Canada

*Corresponding author

RESUMO

Baleias jubarte são uma espécie migratória cosmopolita. Devido à sua proximidade a áreas costeiras, estão em contato constante com atividades humanas embarcadas. No que diz respeito ao crescente número de embarcações, tanto de pesquisa, pesca quanto de turismo, pesquisadores estão constantemente juntando mais informações sobre a distribuição de baleias jubarte. O objetivo deste trabalho é caracterizar as interações espaciais e acústicas de baleias jubarte vocalmente ativas com o tráfego de embarcações no Parque Nacional Marinho dos

Abrolhos (ANMP - Bahia, Brazil). Pesquisas embarcadas foram realizadas a fim de registrar comportamento, atividade acústica e posição geográficas de grupos de baleia jubarte avistados em 2004 e 2005. Posições de GPS de 14 embarcações foram utilizadas para identificar o principal corredor de navegação ao ANMP. O programa ArcGIS foi utilizado para criar mapas de co-ocorrência afim de identificar as principais áreas onde o corredor de navegação se sobrepõe com a distribuição de baleias jubarte cantoras. Sons de embarcações foram coletados em 2005 e analisados no programa Raven Pro 1.4. Foi identificada a banda de frequência que contém 50% da energia de cada som e verificar se estas se sobrepõem com a banda de baixa frequência produzida por jubartes em Abrolhos (70-350 Hz). Um total de 105 grupos vocalmente ativos e 57.039 pontos de GPS de embarcações foram plotados no

ArcGIS. Através dos mapas criados de densidade de jubartes e embarcações, foi possível criar um mapa de co-ocorrência espacial e foi encontrado que áreas com maior densidade de jubartes também tem uma maior densidade de tráfego de embarcações. Vinte e quatro sons de

12 embarcações foram analisados e foi encontrado que todas produziam ruídos que se sobrepõem com a banda de frequência de sons de baleias jubarte em Abrolhos. Através deste trabalho foi possível identificar as áreas mais usadas por baleias jubarte cantoras ao redor do

Banco dos Abrolhos e como estas se sobrepõem com o tráfego de embarcações. Este estudo 77

fornece dados que enfatizam a necessidade de pôr em prática planos de manejo adaptativo para a espécie no Brasil.

ABSTRACT

Humpback whales are a cosmopolitan migratory species. Due to their close proximity to coastal areas, they are constantly in contact with human vessel-based activities. In regard to the growing number of vessels, including research, fishing and tourism vessels, researchers are constantly gathering more information on humpback whales' distribution, behavior and especially the effects of human activities on these animals. The purpose of this study is to characterize spatial and acoustic interactions of vocally active humpback whales and vessel traffic in the Abrolhos National Marine Park (ANMP - Bahia, Brazil). Vessel based surveys were conducted in order to register humpback whale group behavior, acoustic activity and geographical positions. GPS positions from fourteen vessels were used to identify the main navigation corridor to the ANMP. The program ArcGIS was used in order to create maps of co-occurrence to identify the main areas where the navigation corridor overlaps with humpback whale singers' distribution. Vessel sounds were collected in 2005 and were analyzed in the program Raven Pro 1.4. Vessel sounds were analyzed in the interest to identify the frequency band that contains 50% of the sound energy and verify if that overlaps with the low-frequency band produced by humpbacks in Abrolhos (70-350 Hz). A total of

105 vocally active humpback whale groups and 57.039 vessel GPS points were plotted onto

ArcGIS. From the humpback whale density and vessel density maps, it was possible to create a spatial co-occurrence map and it was found that areas with higher density of whales also have higher density of vessel traffic. Twenty-four vessel sounds from 12 vessels were analyzed and it was found that all vessels generated noise that overlapped with the frequency band of humpback whale sounds in Abrolhos. Through this work, it was possible to identify areas most used by humpback whale singers around the Abrolhos Bank and how they overlap 79

with vessel traffic. This study provides data that emphasize the need to begin practicing adaptive management plans for the species in Brazil.

INTRODUCTION

Humpback whales are mainly a coastal species that concentrates on traditional feeding and breeding grounds, but frequently travel across deep waters when migrating from an area to another (Dawbin 1966, Whitehead and Moore 1982, Clapham and Meade 1999, Horton et al. 2011, Kennedy et al. 2013). Due to their close proximity to coast lines or continental shelf waters, humpback whales are vulnerable to many human activities such as chemical pollution, anthropogenic noise, and interactions with fishing gears. Therefore, there is an increasing concern with elevated vessel speeds, growing maritime traffic and the high number of strikes on cetaceans around the world (Reeves et al. 2003, Jensen and Silber 2004, Félix and

Waerebeek 2005).

Aside from many other human activities occurring in the oceans, the growing number of vessels is also due to whale watching, a tourism activity that aims to provide to the general public the opportunity to see whales and dolphins in the wild (Hoyt 2001). This activity came as an alternative to whaling, being considered more lucrative to coastal communities while being contributive to the conservation of whales and dolphins (Hoyt 2001, Parsons et al.

2003, Parsons 2012).

Although whale watching is indeed a preferred alternative to whaling, the development of such industry unfortunately comes with a cost to the animals (Morete et al.

2007). Research shows that when cetaceans are approached by vessels they can often present changes in their behavior (e.g., Williams et al. 2002, Lusseau 2003, Corbelli 2006), leading to 81

possible long-term negative impacts not only to individuals, but also to local populations

(Lusseau 2005, Bejder et al, 2006a).

It has not been possible to determine precisely what long-term impacts or significant behavioral changes can be caused by continued disturbance from vessel-based whale watching activities. However, short term changes in behavior have been seen in many cetacean species (Orams 2004, Parsons 2012). Whale watching can cause changes in cetacean surfacing and diving behavior (Stone et al. 1992, Corkeron 1995, Janik and Thompson 1996,

Seuront and Cribb 2011), active surface behavior (Coscarella et al. 2003, Lusseau 2006,

Noren et al. 2009, Stamation et al. 2010), group size or composition (Mattson et al. 2005,

Bejder et al. 2006b, Valle and Cunha Melo 2006), swimming speed and directionality

(Williams et al. 2002, Scheidat et al. 2004, Timmel et al. 2008, Williams et al. 2009), feeding

(Stamation et al. 2007, Carrera et al. 2008, Dans et al. 2008, Lusseau et al. 2009) and resting activities (Williams et al. 2006, Stockin et al. 2008, Visser et al. 2011), and acoustic communication (Scarpaci et al. 2000, Buckstaff 2004, Foote et al. 2004, Sousa-Lima and

Clark 2008, 2009) and may even lead to temporary or permanent abandonment of the area

(Bryant et al. 1984, Lusseau 2005, Bejder et al. 2006a, Carrera et al. 2008, Sousa-Lima and

Clark 2009).

Aside from their physical presence, whale watching boats can also generate sounds that overlap in time and frequency with many marine mammal vocalizations, especially mysticetes (baleen whales) (Richardson et al. 1995). Sound is the most important 82

communication channel for large whales, mediating behaviors such as feeding (Mobley et al.

1988), social relations and group organization (Clark 1982, Darling et al. 2006). During their stay in wintering grounds, where they are supposedly breeding and calving, humpback whales produce long and complex songs (Payne and McVay 1971, Winn and Winn 1978) that are performed by males and thought to function as acoustic displays related to mating (Clark and

Clapham 2004). However, in many wintering grounds, whale watching is an activity that takes place parallel to the whales' mating, breeding and calving behavior (Hoyt 2001, Morete et al. 2007, Sousa-Lima 2007). These changes in behavior may vary with the number of vessels present in the area, proximity to the whale group, speed and directionality of the vessel, and whale group composition (Bauer 1993, Morete et al. 2007).

Sound pressure levels from noise have doubled by decade since 1990´s (McDonald et al. 2006) and are produced by shipping traffic, underwater scientific research, defense applications, aquaculture, and seafloor mapping (Urick 1983, McCarthy 2001) but the main source of man-made low-frequency noise in the ocean is shipping (Richardson et al. 1995,

McDonald et al. 2006). Whale watching boats; cruise ships; research, fishing and recreational vessels; also contribute to the noise existent in the ocean (Bejder et al. 2006a, Martins et al.

2013).

High sound pressure level is one aspect of noise pollution that can affect marine mammals, moreover a combination of all temporal and spectral characteristics of the sound being produced (noise), such as duration, repetition rate and spectral content are culprits to the 83

observed behavioral changes in whales (Cato et al. 2004). Effective acoustic communication can be reduced by interference from other signals, a phenomenon known as masking (Payne and Webb 1971, Clark et al. 2009, Rossi-Santos 2012). Intense and continuous exposure to sound pollution may have negative and even permanent effects on marine mammals' physiology (Finneran et al. 2002, Nachtigall et al. 2003, Rolland et al. 2012), behavior

(Richardson et al. 1995, McCauley et al. 1996, Madsen and Møhl 2000, Cato and McCauley

2003, Noad et al. 2004) and distribution (Bejder et al. 2006a, Carrera et al. 2008, McCarthy et al. 2011).

Authors have documented short-term displacement of marine mammals exposed to noise, which can disrupt feeding and mating behaviors, along with avoidance of the affected area temporarily or even permanently (Bryant et al. 1984, Richardson et al. 1995). The increase of a vessels sound pressure level may act as a cue to a whale indicating that there is an undesired material presence approaching it (McCauley et al. 1996, Cato et al. 2004).

Disturbance caused by vessels that disrupt singing behavior, could possibly cause a negative effect on reproduction (Norris 1994, Sousa-Lima et al. 2002, Sousa-Lima and Clark

2008, 2009, Herman et al. 2013). In Hawaii, Norris (1994) found that in the presence of vessels, humpbacks can change some elements of the song in response to approaches.

Humpbacks in Newfoundland and Labrador were found to use a short-range horizontal avoidance strategy and increase surface activities in the presence of vessels (Corbelli 2006).

Sousa-Lima and Clark (2009) assessed the spatio-temporal responses of humpback whales to 84

approaching vessels around the Abrolhos National Marine Park. The authors found that the whales displayed two types of responses: displacement followed by cessation of vocal activity; and displacement along with continued vocal activity. In most cases, humpbacks moved away from approaching vessels.

The Abrolhos National Marine Park (ANMP) is known to be one of the most important breeding and calving grounds for humpback whales in the western South Atlantic.

There is an ongoing growth of the whale population that frequents this area (Andriolo et al.

2010, Zerbini et al. 2011). Along with the increase of the humpback whale populations, the occurrence of whale watching activities has also become more frequent, with an annual numbers of park visitors between 4,000-5,000 people (Cipolotti et al. 2005, Sousa-Lima and

Clark 2008).

Quantitative and qualitative measures of the effects of the presence of vessels are necessary to better understand the impacts they can cause and also to manage vessel traffic in a sustainable manner. In this work, we attempt to characterize the spatial and acoustic interactions of humpback whale singers and vessel traffic in the ANMP.

METHODS

Study site

The Abrolhos Bank is considered the most important breeding site for humpback whales in the Southwestern Atlantic Ocean (Engel 1996, Martins et al. 2001), with the current population estimated between 6,000-10,000 individuals (Andriolo et al. 2010, Zerbini et al.

2011). The Bank is located off the coast of Brazil between 16°40’-19°30’S, covering an area of approximately 30,000 km². The ANMP was created in 1998 and its limits encompass one of the core areas of the humpback whales' breeding area (Martins et al. 2013). The Abrolhos

Archipelago is located at the center of the park. The surroundings of the Abrolhos

Archipelago were monitored in order to evaluate the presence of vocally active humpback whales (Figure 1). 86

Figure 1 - Map of the study area showing positions of vocally active humpback whales groups.

Humpback whale data

The humpback whale data was collected during the breeding seasons of 2004 and

2005. Visual vessel based surveys were conducted around the Abrolhos area with the purpose 87

of registering behavioral data on humpback whale groups. At all times, two observers were aboard the vessels and registered group behavior, size and composition, GPS positions and acoustic activity. The methods are fully described in Sousa-Lima (2007). Seeing that humpback whale data was collected from a vessel based platform, the sampling area is somewhat restricted to areas safe for navigation. Data on humpback whale group positions were plotted onto the program ArcMap from the ArcGIS® 10.1 package (Figure 1).

The merge tool from the Data Management extension was used in order to create a single file containing data from both years (2004 and 2005). We performed a point density analysis using the Kernel density tool in the Spatial Analyst Extension. A search radius of 8 nautical miles (nm), approximately 14,800 km², was used to guarantee the integration of all data.

Aside from the density model, we extracted contours identifying the areas that include certain percentages of the points' distribution (30, 50 and 90%). These contours were created using the Isopleth tool from Geospatial Modelling Environment© (Version 0.7.2.1). These contours represent the boundary of the area that contains a desired percentage of the volume of the density distribution. By this, we mean that the 90% distribution contour includes 90% of all observations, representing almost the entire range of the sample distribution. The 30% and 50% distribution contours represent areas with highest densities, that is, the core areas.

Vessel traffic spatial data

Data on vessels were collected during the year of 2005. One member of each vessel’s crew received a GPS unit before they left the continent to the Abrolhos Archipelago. The crew member responsible for the GPS was asked to have it turned on during all periods that the vessel engine was on and received additional batteries to keep the unit working during the entire trip. When the vessels returned from the islands, a research assistant collected the GPS units and the data were downloaded onto a computer for further analysis. This procedure was conducted every day that weather and tourist demand made it possible for vessels to depart from the town of Caravelas, which was the primary source of tourism vessels operating in the

Abrolhos area.

We used the GPS points from fourteen different vessels to identify the main navigation corridor by calculating a density index. The Kernel density tool was applied with the same search radius used to analyze whales' density. The resulting raster map was used in order to perform the co-occurrence analysis and gave us a view of the route most used by vessels.

The Abrolhos Bank has a very distinct geographic landscape (Fainstein and

Summerhayes 1982). The coral reefs in this area grow as large columns that can sometimes reach sea level (Leão et al. 2010) and for this reason, vessels have to travel in a defined route which does not change across years in order to avoid collision. The route travelled by vessels often overlaps with areas most frequented by humpback whales. 89

Co-occurrence qualitative analysis

We used the resulting humpback whale distribution map raster file to run a co- occurrence analysis in order to identify the main areas where the navigation corridor overlaps with humpback whale singers' distribution in the Abrolhos area. The co-occurrence areas were obtained using the Raster Calculator tool of the Spatial Analyst extension by adding together both raster files.

Classification of co-occurrence areas

For each humpback whale and vessels percentage contour (30, 50 and 90%) a value was assigned from 0 to 3 (Table 1). The final values adopted for the co-occurrence analysis presented the categories seen in Table 2.

Table 4 - Value of weights used for each density interval of humpback whales and vessels.

Whales and vessels Value percentage contour 30% contour 3

50% contour 2

90% contour 1

Other 0

Table 5 - Classification adopted for the resulting sum of whale and vessel distribution.

Sum Co-occurrence

0 Low

2 Low-mid

3 Middle

4 Mid-high

5 High

6 Higher

Vessels sound data

Arrays of 4 MARUs (“Marine Acoustic Recording Units” developed by the

Bioacoustics Research Program of the Cornell Laboratory – BRP) were used to acoustically monitor an area that varied from approximately 60 to 315 km² around the Abrolhos archipelago during three consecutive years (2003, 2004 and 2005). Vessel sounds were collected from the 2005 MARUs data. MARUs include a microprocessor, hard disks for data storage, acoustic communications circuitry and batteries, that remain sealed in a glass sphere and protected by a plastic harness with an external hydrophone on the outside. MARUs were programmed to record continuously at a sampling rate of 2,000 Hz (Sousa-Lima 2007, Sousa-

Lima and Clark 2008, 2009).

The Raven Pro 1.4 sound analysis software (Bioacoustics Research Program, 2011) was used to analyze sound data. Spectrograms were visually browsed in order to detect vessel sounds and to manually extract the most intense part of the sound of interest (drawing a 91

rectangular annotation area) by identifying higher amplitudes in the spectrogram. A Hann window function of 1024-points and a 1024-point FFT size were used. After identifying peak time (time, in seconds, at which the greatest amplitude value occurs), a box was drawn to select the sound including 30s before and 30s after peak time (Figure 2). Quartile frequencies were measured for the selections made, dividing the selection in two frequency intervals containing 25% and 75% of the energy present in the selection. By selecting the 1st and 3rd quartiles, we obtain the inter-quartile frequency values that divide 50% of the frequencies where the highest energy is concentrated (Charif et al. 2010). These values were selected in order to compare the sounds produced by vessels with humpback whales in Abrolhos to verify if the frequency band where 50% of the sound energy is concentrated overlaps with that of humpbacks. The low-frequency band produced by humpback whales in Abrolhos is approximately 70-350 Hz (Sousa-Lima et al. 2010). Bar charts were produced using the statistical analysis program PASW 18.0 (SPSS Inc. 2009) in order to plot the inter-quartile frequencies of vessel sounds.

Figure 2 - Spectrogram showing the 60s selection of the sound of a vessel recorded off the coast of Brazil in 2005 (FFT size = 1024, Hann Window). Frequency in Hz in the Y axis and time on the X axis.

RESULTS

Humpback whale data

A total of 105 vocally active humpback whale groups and 243 individuals were sighted and registered for this survey. The resulting map for vocally active groups was generated (Figure 3). The distribution values and percentage contours (30, 50 and 90%) show the core areas used by humpback singers in the survey area.

Figure 3 - Vocally active humpback whale groups' distribution model.

Vessel traffic spatial data

The vessels' analysis allowed for the identification of the main navigation corridor used in the study area. The analysis resulted in a total of 57,039 GPS points from fourteen different vessels. From the total GPS points, 8,310 belonged to research vessels, which have 94

routes that go beyond the ones used by other vessels. However, they were included due to the fact that they also travel through the navigation corridor to the Abrolhos Archipelago. The area with the higher distribution of vessels is concentrated around the Abrolhos Islands

(Figure 4).

Figure 4 - Navigation corridor resulting from the vessels' distribution model. 95

Co-occurrence analysis

The overlapping of the vocally active humpback whale groups' distribution model with the vessels' distribution model resulted in a map that shows the probability of co-occurrence in space for humpback whale singers and vessel traffic around the ANMP (Figure 5). We identified a higher co-occurrence area between vessels and singers within a distance as long as 6.39 nm from the center of the Abrolhos Archipelago. High co-occurrence areas exist at up to 7.50 nm from the central area of the Abrolhos Archipelago. 96

Figure 5 - Resulting map showing the co-occurrence areas between humpback whale singers and vessels around the ANMP.

Vessels sound data

Quartile frequencies were measured for 24 sounds from 11 different vessels that traveled to the ANMP in 2005. Bar charts were produced containing the highest and lowest 97

frequency values of the inter-quartile frequencies for each vessel. A gray area was plotted over the charts in order to highlight the low-frequency band of sounds from humpback whales in Abrolhos (Figure 6). It was possible to visualize that all vessels that passed through the navigation corridor in 2005 produced sounds that overlapped in frequency with humpback whale sounds.

Figure 6 - Plot of the frequency band of vessel sounds that contains 50% of the energy of the entire sound selection. Gray area highlights the frequency band of humpback whale sounds in Abrolhos (75-354 Hz).

DISCUSSION

Kernel estimator, as a non-parametric statistics is known to be one of the most indicated methods in estimating density (Powell and Mitchell 2012). Here, the method was 98

used to identify humpback whale singers' main concentration in the survey area and was shown to be effective. Through the analysis used, we were able to identify areas of co- occurrence of vocally active whales and vessels around the Abrolhos Archipelago. In this analysis, we assumed that the singers’ distribution model represents well the singers’ distribution within the survey area.

According to Powell and Mitchell (2012), the search radius used in the kernel density estimator, is one of the most important factors when estimating animal distribution and home range. For the purpose of this study, the search radius used was of eight nautical miles

(14.800 km²), in order to include all data from the survey. However, other search radiuses were tested before choosing the final one, and they either gave us a micro-scale detail for areas too small, or would hide important areas with a search radius too large. Also, we would be underestimating the acoustical range of humpback whale songs and vessel noise if we consider only the point where the animal or vessel was registered, seeing that sounds can propagate through long distances in the aquatic environment (Naguib and Wiley 2001, Croll et al. 2002, Darling et al. 2006).

The waters of the Abrolhos Archipelago have an average depth of about 20 meters and are full of coral reef formations, which can influence distribution of vessels and humpback whales (Martins et al. 2001, Leão et al. 2010). For example, groups with calves are more often located in shallow and protected waters (Herman and Tavolga 1980, Craig and Herman 2000,

Martins et al. 2001, Félix and Botero-Acosta 2011). In Hawaii, Frankel et al. (1995) found 99

that vocally active males are also more likely to be concentrated in shallower waters close to coast. In Abrolhos, singers prefer shallower waters and areas without the presence of coral reefs (Fernandes et al. unpublished).

The co-occurrence areas identified in the navigation corridor by means of this study, pass through areas of higher density of humpback whale singers, seeing that the vessels parting from the town of Caravelas are bound for the park. The spatial analysis here presented represents well the most used navigation route from Caravelas to the ANMP.

Acoustic interactions can potentially mask humpback whale vocalizations, interfering with the animals’ abilities to detect and distinguish signals of importance for the species

(Foote et al. 2004). Seeing that vessels and humpbacks produce sounds in the same frequency range, vessel noise can affect these animals in many ways (Watkins 1986, Richardson et al.

1995, Erbe and Farmer 2000, Cato et al. 2004, Rossi-Santos 2012, Sousa-Lima and Clark

2009). As we showed on the analysis of the vessel sounds produced in Abrolhos, the noise they generate contains the highest amount of energy in the same low-frequency band used by humpbacks. The evolution of low-frequency components in the song for long-distance communication optimize humpback whales’ signal active space (the range over which a signal can be detected) which is hypothethically adaptive when males do not know where females are located (Brenowitz 1982, Croll et al. 2002, Darling et al. 2006).

100

Masking caused by man-made noise, such as vessel noise, can effectively reduce the active space used by humpback whales and decrease the communication range for individual singers searching for potential mates (Richardson et al. 1995). A factor that may influence mate choice in humpback whales is the size of the potential mate. That is, large, mature females will most likely choose large, mature males, a preference that may have a direct influence on individual reproductive success (Crespi 1989, Pack et al, 2012, Herman et al.

2013). If males are in fact signaling their size, the singer with the lowest frequency song will be perceived as a larger male than those with higher frequencies (Alcock 2011). If that is the case, masking will cause songs of lower frequencies to be missed by females and these individuals will consequently have a lowered breeding success (Charlton et al. 2007, Alcock

2011). As it has been seen in

It is important to note that, like the sounds produced by whales, the noise produced by vessels can have a much larger area of disturbance than only the physical presence (Sousa-

Lima and Clark 2009). Whales have been seen to respond to vessels from distances up to 8km

(Frankel and Clark 1988, Baker and Herman 1989, Sousa-Lima and Clark 2009, Morete

2007). In the Abrolhos Bank, it has also been found that whales respond to the presence of vessels by displacing and/or disrupting singing activity. The average distance of response from humpback singers to vessel noise in the ANMP was of 7.5km (Sousa-Lima and Clark

2009). Dunlop et al. (2010) found that in increasing background noise levels, humpbacks changed from vocal communication to surface generated signals. The change from vocal sounds to surface generated sounds (pectoral slapping, lob tailing or tail slapping) may be an alternative means of communication enhancing the perception of the vocal signal through a 101

visual component when in the presence of increased background noise. Studies focusing on behavioral changes should consider all types of behavior and variables that can in some way have an effect on communication. Along with the noise generated, the physical presence of vessels can also affect behavior of whales (Noren et al. 2009), disrupting important activities such as mating and foraging (Williams et al. 2002, Noren et al. 2009).

The ANMP was created in order to legally guarantee the conservation of the high concentration of humpbacks, aside from protecting other species (Brasil 2000). In Brazil, the presence and behavior of recreational vessels is regulated by the 117/96 IBAMA ("Instituto

Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis") federal act and its modification 024 from February 8th, 2002. This law states that vessels may not produce any type of noise when in a distance of 300m from any cetacean and they may not approach any large whale (any mysticete, sperm whales and killer whales) with the motor turned on from a distance of 100m.

Whale watching has become an activity appreciated worldwide and has been growing at an accelerated pace. This activity helps to avoid an unsustainable use of marine mammals by increasing the general public's knowledge on the importance of protecting these animals and by contributing to the economy of many places (Hoyt 2001). Tourism boats aside from promoting environmental education can also be used as platforms for scientists to study marine mammal behavior (Martins 2004). However, these activities must be performed in a manner that favors both the animals and the local human population that is sustained by such 102

activities (Diegues 2001, Hoyt 2001). Several coastal towns benefit from ecotourism developed in Abrolhos (Palazzo et al. 1994). Tourism boats that depart from these towns towards the marine protected area of ANMP form the main navigation corridor.

Proper management of tourism, research, fishing, recreational and other vessels' activity in humpback whale concentration areas should take into consideration not only physical and acoustic presence (Norris 1994, Au and Green 2000) but also vessel speed and distance from groups when assessing the possible effects they can cause. Controlling these activities could be beneficial for humpbacks seeing that singing is an essential behavior that may guarantee the species reproductive success and maintain the population growing (Sousa-

Lima and Clark 2009, Herman et al. 2013). This work shows the path for future studies on vessel impacts on humpback whale singing behavior in the Abrolhos Bank. Management regulations should consider control vessel speed or establish speed reduction zones during the species breeding season when in the presence of humpback whales. This would allow whales to hear vessel noise and have enough time to leave the area safely, avoiding acoustic overlap and possibilities of strikes (Vanderlaan and Taggart 2007).

Also, with the development of new technologies aiming to make ships more silent

(ship quieting technologies), it would be ideal for park management to propose studies on the operating vessels' noises in order to create new guidelines on the use of the ANMP, giving preference to quieter vessels (Malakoff 2010). Reducing the noise of vessels could potentially 103

reduce masking effects and possibly reduce the overall risk of strikes (Richardson et al. 1995,

Leaper et al. 2009).

Martins et al. (2013) found that the existing MPAs of the Eastern Brazilian Coast were not ideally designed in order to guarantee the humpbacks protection and suggested the creation of new MPAs that cover all the areas of higher distribution. We found that this is true and necessary for the ANMP. As it can be seen in the co-occurrence map (Figure 5), the area designated to represent the ANMP does not properly cover areas where humpback whale singers and vessels have the highest co-occurrence. We propose that the park area should be increased at least during humpback whale breeding season (approximately July to November,

Engel 1996). Further studies should be performed in order to better choose a new definitive park area. However, we propose that in order for this measure to be put into place immediately, the park area could be mirrored towards land to cover areas of highest co- occurrence (Figure 7). The mirrored area would act as a protective zone for humpback whale singers, where vessels would need to abide by rules such as reduction of vessel speed (Kipple and Gabriele 2003, Vanderlaan and Taggart 2007), noise reduction measures (Southall and

Scholik-Schlomer 2008) and especially vessel approach to humpback whale groups . It would be essential to revisit the existing laws and regulations taking into consideration studies that focus on habitat use and distribution of the species and their interactions with human activities. 104

Figure 7 - Map of co-occurrence areas of humpback whale singers and vessel traffic showing the proposed increase of the ANMP area.

CONCLUSIONS

From this work, it was possible to identify areas intensively used by humpback whale singers' around the Abrolhos Bank and its overlapping with the vessels' navigation corridor.

Through the methods used, we were able to find the areas where singers and vessels 105

distributions overlap and to identify areas of higher co-occurrence . The Brazilian humpback whale population continues to grow in number and space, spreading throughout the coast and overlap with vessel distribution is likely to continue growing as well (Ward et al. 2011,

Zerbini et al. 2011, Martins et al. 2013). We provided complementary data supporting findings from Martins et al. (2013) that emphasize the need to put in to practice adaptive management plans (Blumstein 2007) based on the results of research experiments and that considers variables that may be important for the conservation and management of the target species and their environment.

REFERENCES

Alcock, J. 2011. Comportamento animal: uma abordagem evolutiva. 9 ed. Artmed, Porto

Alegre.

Andriolo, A., P. G. Kinas, M. H. Engel, C. C. A. Martins and A. M. Rufino. 2010. Humpback whales within the Brazilian breeding ground: distribution and population size estimate.

Endangered Species Research 11:233-243.

Au, W. W. L. and M. Green. 2000. Acoustic interaction of humpback whales and whale- watching boats. Marine Environmental Research 49:469-481.

Baker, C. S. and L. M. Herman. 1989. Behavioral responses of summering humpback whales to vessel traffic: Experimental and opportunistic observations. Final Report NPS-NR-TRS-89-

01. US Department of the Interior, National Park Service, Anchorage, Alaska, USA.

Bauer, G. B., J. R. Mobley L. M. Herman. 1993. Responses of wintering humpback whales to vessel traffic. Journal of the Acoustical Society of America 94:1848. 106

Bejder, L., A. Samuels, H. Whitehead, et al. 2006a. Decline in relative abundance of bottlenose dolphins exposed to long-term disturbance. Conservation Biology 20:1791-1798.

Bejder, L., A. Samuels, H. Whitehead and N. Gales. 2006b. Interpreting short-term behavioural responses to disturbance within a longitudinal perspective. Animal Behaviour

72:1149-1158.

Bioacoustics Research Program. 2011. Raven Pro: Interactive Sound Analysis Software

(Version 1.4) [Computer Software]. Ithaca, New York. Available from http://www.birds.cornell.edu/raven (Last viewed March 05, 2014).

Blumstein, D. T. 2007. Darwinian decision making: Putting the adaptive into adaptive management. Conservation Biology 21:552-553.

Brasil. 2000. Lei 9.985/2000. Sistema Nacional de Unidades de Conservação, Brasil.

Brenowitz, E. A. 1982. The active space of Red-winged Blackbird song. Journal of

Comparative Physiology A 147:511-522.

Bryant, P. J., C. M. Lafferty and S. K. Lafferty. 1984. Reoccupation of Laguna Guerrero

Negro, Baja California, Mexico, by gray whales. Pages 375-387 in Jones, M. L., S. L. Swartz and S. Leatherwood eds. The Gray Whale, Eschrichtius robustus. Academic Press, Orlando.

Buckstaff, K. C. 2004. Effects of watercraft noise on the acoustic behavior of bottlenose dolphins, Tursiops truncatus, in Sarasota Bay, Florida. Marine Mammal Science 20:709-725.

Carrera, M. L., E. G. P. Favaro and A. Souto. 2008. The response of marine tucuxis (Sotalia fluviatilis) toward tourist boats involves avoidance behaviour and a reduction in foraging.

Animal Welfare 17:117-123. 107

Cato, D. H. and R. D. McCauley. 2003. Ambient sea noise from manmade and natural sources and use of sound by whales. Proceedings of WESPACVIII, Eight Western Pacific Acoustics

Conference, Melbourne, April 2003, 1180L.

Cato, D. H., R. D. McCauley and M. J. Noad. 2004. Potential effects of noise from human activities on marine mammals. Proceedings of Acoustics 2004, Australian Acoustical Society

Conference, Gold Coast, 3-5 November. Pp 353-358.

Charif, R. A., A. M. Waack and L. M. Strickman. 2010. Raven Pro 1.4 User's Manual.

Cornell Lab of Ornithology, Ithaca.

Charlton, B., D. Reby and K. McComb. 2007. Female red deer prefer the roars of larger males. Biology Letters 3:382-385.

Cipolotti, S. R. C., M. E. Morete, B. L. Basto, M. H. Engel and E. Marcovaldi. 2005.

Increasing of whale watching activities on Humpback whales in Brazil: implications, monitoring and research. Paper presented to the International Whaling Commission Scientific

Committee, SC/57/WW7.

Clapham, P. J. and J. G. Meade. 1999. Megaptera novaeangliae. Mammalia Species 604:1-9.

Clark, C. W. 1982. The acoustic repertoire of the Southern Right Whale: A quantitative analysis. Animal Behavior 30:1060-1071.

Clark, C. W. and P. J. Clapham. 2004. Acoustic monitoring on a humpback whale

(Megaptera novaeangliae) feeding ground shows continual singing into late Spring.

Proceedings of the Royal Society B 271:1051-1057. 108

Clark, C. W., W. T. Ellison, B. L. Southall, L. Hatch, S. M. Van Parijs, A. Frankel and D.

Ponirakis. 2009. Acoustic masking in marine ecosystems: intuitions, analysis, and implication. Marine Ecology Progress Series 395:201-222.

Corbelli, C. 2006. An evaluation of the impact of commercial whale watching on humpback whales, Megaptera novaeangliae, in Newfoundland and Labrador, and the effectiveness of a voluntary code of conduct as management strategy. Ph.D. thesis, Memorial University of

Newfoundland, St. John's, Newfoundland.

Corkeron, P. J. 1995. Humpback whales (Megaptera novaeangliae) in Hervey Bay,

Queensland: behaviour and responses to whale-watching vessels. Canadian Journal of

Zoology 73:1290-1299.

Coscarella, M. A., S. L. Dans, E. A. Crespo and S. N. Pedraza. 2003. Potential impact of unregulated dolphin watching activities in Patagonia. Journal of Cetacean Research and

Management 5:77-84.

Craig, A. S. and L. M. Herman. 2000. Habitat preferences of female humpback whales

Megaptera novaeangliae in the Hawaiian Islands are associated with reproductive status.

Marine Ecology Progress Series 193:209-216.

Crespi, B. J. 1989. Causes of assortative mating in arthropods. Animal Behaviour 38:980-

1000.

Croll, D. A., C. W. Clark, A. Acevedo, B. Tershy, S. Flores, J. Gedamke and J. Urban. 2002.

Only male fin whales sing loud songs. Nature 417:809. 109

Dans, S. L., E. A. Crespo, S. N. Pedraza, M. Degrati and G. V. Garaffo. 2008. Dusky dolphin and tourist interaction: effect on diurnal feeding behavior. Marine Ecology Progress Series

369:287-296.

Darling, J. D., M. E. Jones and C. P. Nicklin. 2006. Humpback whale songs: Do they organize males during the breeding season? Behavior 143:1051-1101.

Davis, W. R., J. G. Ortega-Ortiz, C. A. Ribic, W. E. Evans, D. C. Biggs, P. H. Ressler, R. B.

Cady, R. R. Leben, K. D. Mullin and B. Würsig. 2002. Cetacean habitat in the northern oceanic Gulf of Mexico. Deep-Sea Research I 49:121-142.

Dawbin, W. H. 1966. The seasonal migratory cycle of humpback whales. Pages 145-170 in K.

S. Norris ed. Whales, dolphins and porpoises. University of California Press, Los Angeles.

Diegues, A. C. 2001. Ecologia humana e planejamento costeiro. 2ed. NUPAUB, São Paulo.

Dunlop, R. A., D. H. Cato and M. J. Noad. 2010. Your attention please: increasing ambient noise levels elicits a change in communication behaviour in humpback whales (Megaptera novaeangliae). Proceedings of the Royal Society B 277:2521-2529.

Erbe, C. and D. M. Farmer. 2000. A software model to estimate zones of impact on marine mammals around anthropogenic noise. Journal of the Acoustical Society of America

108:1327-1331.

Engel, M. 1996. Comportamento reprodutivo da Baleia Jubarte (Megaptera novaeangliae) em

Abrolhos. Anais de Etologia 275-284.

Fainstein, R. and C. P. Summerhayes. 1982. Structure and origin of marginal banks off eastern Brazil. Marine Geology 46:199-215. 110

Félix, F. and K. V. Waerebeek. 2005. Whale mortality from ship strikes in Ecuador and West

Africa. Latin American Journal of Aquatic Mammals 4:55-60.

Félix, F. and N. Botero-Acosta. 2011. Distribution and behaviour of humpback whale mother- calf pairs during the breeding season off Ecuador. Marine Ecology Progress Series 426:277-

287.

Finneran, J. J., C. E. Schlundt, R. Dear, D. A. Carder and S. H. Ridgway. 2002. Temporary shift in masked hearing thresholds in odontocetes after exposure to single underwater impulses from a seismic watergun. Journal of the Acoustical Society of America 111:2929-

2940.

Foote, A. D., R. W. Osborne and A. R. Hoelzel. 2004. Whale-call response to masking boat noise. Nature 428:910.

Frankel, A. S. and C. W. Clark. 1988. Results of low-frequency playback of M-sequence noise to humpback whales, Megaptera novaeangliae, in Hawai'i. Canadian Journal of

Zoology 76:521-535.

Herman, L. M. and W. N. Tavolga. 1980. The communication system of cetaceans. Pages

149-209 in: L. M. Herman ed. Cetacean Behavior: Mechanisms and Functions. Krieger

Publishing Co., Malabar. 111

Herman, L. M., A. A. Pack, S. S. Spitz, E. Y. K. Herman, K. Rose, S. Hakala and M. H.

Deakos. 2013. Humpback whale song: who sings? Behavioral Ecology and Sociobiology

67:1653-1663.

Horton, T. W., R. N. Holdaway, A. N. Zerbini, N. Hauser, C. Garrigue, A. Andriolo and P. J.

Clapham. 2011. Straight as an arrow: humpback whales swim constant course tracks during long-distance migration. Biology Letters doi: 10.1098/rsbl.2011.0279.

Hoyt, E. 2001. Whale watching 2001: Worldwide tourism numbers, expenditures, and expanding socioeconomic benefits. International Fund for Animal Welfare, Yarmouth Port,

USA.

Janik, V. M. and P. M. Thompson. 1996. Changes in surfacing patterns of bottlenose dolphins in response to boat traffic. Marine Mammal Science 12:597-602.

Jensen, A. S. and G. K. Silber. 2004. Large whale ship strike database. NOAA Technical

Memorandum NMFS-OPR, January 2004, 37 pp.

Kennedy, A. S., A. N. Zerbini, O. V. Vásquez, N. Gandilhon, P. J. Clapham and O. Adam.

2013. Local and migratory movements of humpback whales (Megaptera novaeangliae) sattelite-tracked in the North Atlantic Ocean. Canadian Journal of Zoology 92:9-18.

Kipple, B. M. and C. Gabriele. 2003. Glacier Bay Watercraft Noise. Naval Surface Warfare

Center Technical Report NSWCCD-71-TR-2003/522.

Leão, Z. M. A. N., R. K. P. Kikuchi, M. D. M. Oliveira and V. Vasconcellos. 2010. Status of

Eastern Brazilian coral reefs in time of climate changes. Pan-American Journal of Aquatic

Sciences 5:224-235. 112

Leaper, R., M. Renilson, V. Frank and V. Papastavrou. 2009. Possible steps towards reducing impacts of shipping noise. International Whaling Commission, Scientific Committee, document SC/61/E19.

Lusseau, D. 2003. The effects of tour boats on the behavior of bottlenose dolphins: Using

Markov chains to model anthropogenic impacts. Conservation Biology 17:1785-1793.

Lusseau, D. 2005. Residency pattern of bottlenose dolphins Tursiops spp. in Milford Sound,

New Zealand, is related to boat traffic. Marine Ecology Progress Series 295:265-272.

Lusseau, D. 2006. The short-term behavioral reactions of bottlenose dolphins to interactions with boats in Doubtful Sound, New Zealand. Marine Mammal Science 22:802-818.

Lusseau, D., D. E. Bain, R. Williams and J. C. Smith. 2009. Vessel traffic disrupts the foraging behavior of southern resident killer whales Orcinus orca. Endangered Species

Research 6:211-221.

Madsen, P. T. and B. Møhl. 2000. Sperm whales (Physeter catodon L. 1759) do not react to sounds from detonators. Journal of the Acoustical Society of America 107:668-671.

Malakoff, D. 2010. A push for quieter ships. Science 328:1502-1503.

Martins, C. C. A. 2004. O uso do sistema de informações geográficas como ferramenta na identificação de áreas prioritárias para a conservação da população de baleia jubarte,

Megaptera novaeangliae, em seu sítio reprodutivo na costa leste do Brasil. Masters dissertation, Universidade de Brasília, Brasília, Brasil, 119 pp. 113

Martins, C. C. A., M. E. Morete, M. H. Engel, A. C. Freitas, E. R. Secchi and P. G. Kinas.

2001. Aspects of habitat use patterns of humpback whales in the Abrolhos Bank, Brazil, breeding ground. Memoirs of the Queensland Museum 47:563-570.

Martins, C. C. A., A. Andriolo, P. G. Kinas and C. H. Saito. 2013. Identifying priority areas for humpback whale conservation at Eastern Brazilian Coast. Ocean & Coastal Management

75:63-71.

Mattson, M. C., J. A. Thomas and D. St. Aubin. 2005. The effect of boat activity on the behavior of bottlenose dolphins (Tursiops truncatus) in waters surrounding Hilton Head

Island, South Carolina. Aquatic Mammals 31:133-140.

McCarthy, E. M. 2001. International Regulation of Transboundary Pollutants: The Emerging

Challenge of Ocean Noise. Ocean and Coastal Law Journal 6:257-292.

McCarthy, E., D. Moretti, L. Thomas, N. Dimarzio, R. Morrissey, S. Jarvis, J. Ward, A. Izzi and A. Dilley. 2011. Changes in spatial and temporal distribution and vocal behavior of

Blainville's beaked whales (Mesoplodon densirostris) during multiship exercises with mid- frequency sonar. Marine Mammal Science 27:E206-E226.

McCauley, R. D., D. H. Cato, A. F. Jeffrey. 1996. A study of the impacts of vessel noise on humpback whales in Hervey Bay. James Cook University of North Queensland Report to

Queensland Department of Environment and Heritage, 137.

McDonald, M. A., J. A. Hildebrand and S. M. Wiggins. 2006. Increases in deep ocean ambient noise in the Northeast Pacific west of San Nicolas Island, California. Journal of the

Acoustical Society of America 20:711-718. 114

Mobley, J. R., Jr., L. M. Herman and A. S. Frankel. 1988. Responses of wintering humpback whales (Megaptera novaeangliae) to playback of recordings of winter and summer vocalizations and of synthetic sound. Behavioral Ecology and Sociobiology 23:211-223.

Morete, M. E. 2007. Caracterização temporal da estructura de grupos e do comportamento de baleias jubarte (Megaptera novaeangliae) na área de reprodução dos Abrolhos (Bahia, Brasil).

Dissertation, Universidade Federal de São Paulo, Brazil.

Morete, M. E., T. L. Bisi, S. Rosso. 2007. Mother and calf humpback whale responses to vessels around the Abrolhos Archipelago, Bahia, Brazil. Journal of Cetacean Research and

Management 9:241-248.

Nachtigall, P. E., J. L. Palowski and W. W. L. Au. 2003. Temporary threshold shifts and recovery following noise exposure in the Atlantic bottlenosed dolphin (Tursiops truncatus).

Journal of the Acoustical Society of America 113:3425-3429.

Naguib, M. and H. Wiley. 2001. Estimating the distance to a source of sound: mechanism and adaptations for long-range communication. Animal Behaviour 62:825-837.

Noad, M. J., D. H. Cato and M. D. Stokes. 2004. Acoustic tracking of humpback whales: measuring interactions with the acoustic environment. Proceedings of Acoustics 2004,

Australian Acoustical Society Conference, Gold Coast, 3-5 November.

Noren, D. P., A. H. Johnson, D. Rehder and A. Larson. 2009. Close approaches by vessels elicit surface active behaviors by southern resident killer whales. Endangered Species

Research 8:179-192. 115

Norris, T. F. 1994. The effects of boat noise on the acoustic behavior of humpback whales

(Megaptera novaeangliae). Journal of the Acoustical Society of America 96:3251.

Orams, M. 2004. Why dolphins may get ulcers: considering the impacts of cetacean-based tourism in New Zealand. Tourism in Marine Environments 1:17-28.

Pack, A. A., L. M. Herman, S. S. Spitz, et al. 2012. Size-assortative pairing and discrimination of potential mates by humpback whales in the Hawaiian breeding grounds.

Animal Behaviour 84:983-993.

Palazzo, J. T., M. Kammers and I. Linhares. 1994. Whalewatching sites in Brazil: a summary of available information. Working Group on Whalewatching, 46th IWC, IWC/46/WW, 8 pp.

Parsons, E. C. M., C. A. Warburton, A. Woods-Ballard, A. Hughes and P. Johnston. 2003.

The value of conserving whales: the impacts of cetacean-related tourism on the economy of rural West Scotland. Aquatic Conservation 13:397-415.

Parsons, E. C. M. 2012. The negative impacts of whale-watching. Journal of Marine Biology

2012:1-9.

Payne, R. S. and S. McVay. 1971. Songs of humpback whales. Science 173:585-597.

Payne, R. and D. Webb. 1971. Orientation by means of long range acoustic signaling in baleen whales. Annals of the New York Academy of Sciences 188:110-141.

Powell, R. A. and M. S. Mitchell. 2012. What is a home range? Journal of Mammalogy

93:948-958.

Reeves, R. R., B. D. Smith, E. A. Crespo and G. Notarbartolo di Sciara. 2003. Dolphins, whales and porpoises - 2002-2010 Conservation Action Plan for the World's Cetaceans. 116

IUCN/SSC Cetacean Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, 139 pp.

Richardson, J. W., C. R. Grenne, C. L. Malme and D. H. Thomson. 1995. Marine Mammals and Noise. Academic Press: San Diego.

Rolland, R. M., S. E. Parks, K. E. Hunt, M. Castellote, P. J. Corkeron, D. P. Nowacek, S. K.

Wasser and S. D. Kraus. 2012. Evidence that ship noise increases stress in right whales.

Proceedings of the Royal Society B 279:2363-2368.

Rossi-Santos, M. R. 2012. Comportamento e ecologia acústica da baleia Jubarte (Megaptera novaeangliae) na região Nordeste do Brasil. Tese de Doutorado, Universidade Federal do Rio

Grande do Norte, Natal, RN, 173 pp.

Scarpaci, C., S. W. Bigger, P. J. Corkeron and D. Nugegoda. 2000. Bottlenose dolphins,

Tursiops truncatus, increase whistling in the presence of "swim-with-dolphin" tour operations. Journal of Cetacean Research and Management 2:183-185.

Scheidat, M., C. Castro, J. González and R. Williams. 2004. Behavioural responses of humpback whales (Megaptera novaeangliae) to whalewatching boats near Isla de la Plata,

Machalilla National Park, Ecuador. Journal of Cetacean Research & Management 6:63-68.

Seuront, L. and N. Cribb. 2011. Fractal analysis reveals pernicious stress levels related to boat presence and type in the Indo Pacific bottlenose dolphin, Tursiops aduncus. Physica A

390:2333-2339. 117

Sousa-Lima, R. S. 2007. Acoustic ecology of humpback whales (Megaptera novaeangliae) in the Abrolhos National Marine Park, Brazil. Ph.D. thesis, Cornell University, Ithaca, NY. 205 pp.

Sousa-Lima, R. S. and C. W. Clark. 2008. Modelling the effect of boat traffic on the fluctuation of humpback whale singing activity in the Abrolhos National Marine Park, Brazil.

Canadian Acoustics 36:174-181.

Sousa-Lima, R. S. and C. W. Clark. 2009. Whale sound recording technology as a tool for assessing the effects of boat noise in a Brazilian marine park. Park Science 26:59-63.

Sousa-Lima, R. S., M. E. Morete, R. C. Fortes, A. C. Freitas and M. H Engel. 2002. Impact of boats on the vocal behavior of humpback whales off Brazil. Journal of the Acoustical Society of America 112:2430-2431.

Sousa-Lima, R. S., K. A. Cortopassi and C. W. Clark. 2010. Humpback whale posture and song propagation in very shallow water. In: 2nd PanAmerican/Iberian Meeting on Acoustics,

Cancun, Mexico. Journal of the Acoustical Society of America, 128:2467.

Southall, B. L. and A. Scholik-Schlomer. 2008. Final report on the NOAA International

Conference: "Potential Application of Vessel-Quieting Technology on Large Commercial

Vessels", 1-2 May, 2007, Silver Spring, MD, U.S.A.

SPSS Inc. 2009. PASW Statistics for Windows, Version 18.0. SPSS Inc., Chicago.

Stamation, K. A., D. B. Croft, P. D. Shaughnessy and K. A. Waples. 2007. Observations of humpback whales (Megaptera novaeangliae) feeding during their southward migration along 118

the coast of southeastern New South Wales, Australia: identification of a possible supplemental feeding ground. Aquatic Mammals 33:165-174.

Stamation, K. A., D. B. Croft, P. D. Shaughnessy, K. A. Waples and S. V. Briggs. 2010.

Behavioral responses of humpback whales (Megaptera novaeangliae) to whale-watching vessels on the southeastern coast of Australia. Marine Mammal Science 26:98-122.

Stockin, K. A., D. Lusseau, V. Binedell, N. Wiseman and M. B. Orams. 2008. Tourism affects the behavioural budget of the common bottlenose dolphin Delphinus sp. in the Hauraki

Gulf, New Zealand. Marine Ecology Progress Series 355:287-295.

Stone, G. S., S. K. Katona, A. Mainwaring, J. M. Allen and H. D Corbett. 1992. Respiration and surfacing rates of fin whales (Balaenoptera physalus) observed from a lighthouse tower.

Reports of the International Whaling Commission 42:739-745.

Timmel, G., S. Courbis, H. Sargeant-Green and H. Markowitz. 2008. Effects of human traffic on the movement patterns of Hawaiian spinner dolphins (Stenella longirostris) in Kealakekua bay, Hawaii. Aquatic Mammals 34:402-411.

Urick, R. J. 1983. Principles of Underwater Sound. 3 rd ed. Peninsula Publishing, Los Altos.

Valle, L. and F. C. Cunha Melo. 2006. Behavioral alterations in the gray dolphin Sotalia guianensis (Gervais, 1953) caused by sea traffic. Biotemas 19:75-80.

Vanderlaan, A. S. M. and C. T. Taggart. 2007. Vessel collisions with whales: the probability of lethal injury based on vessel speed. Marine Mammal Science 23:144-156.

Visser, F., K. L. Hartman, E. J. J. Rood, et al. 2011. Risso's dolphins after daily resting pattern in response to whale watching at the Azores. Marine Mammal Science 27:366-381. 119

Ward, E., A. N. Zerbini, P. G. Kinas, M. H. Engel and A. Andriolo. 2011. Estimates of population growth rates of humpback whales (Megaptera novaeangliae) in the wintering grounds off the coast of Brazil (Breeding Stock A). Journal of Cetacean Research and

Management 3:145-149.

Watkins, W. A. 1986. Whale reactions to human activities in Cape Cod waters. Marine

Mammal Science 2:251-262.

Whitehead, H. and M. J. Moore. 1982. Distribution and movements of West Indian humpback whales in winter. Canadian Journal of Zoology 60:2203-2211.

Williams, R., A. W. Trites and D. E. Bain. 2002. Behavioural responses of killer whales

(Orcinus orca) to whale-watching boats: Opportunistic observations and experimental approaches. Journal of Zoology 256:255-270.

Williams, R., D. Lusseau and P. S. Hammond. 2006. Estimating relative energetic costs of human disturbance to killer whales (Orcinus orca). Biological Conservation 133:301-311.

Williams, R., D. E. Bain, J. C. Smith and D. Lusseau. 2009. Effects of vessel on behaviour patterns of individual southern resident killer whales Orcinus orca. Endangered Species

Research 6:199-209.

Winn, H. E. and L. K. Winn. 1978. The song of the humpback whale Megaptera novaeangliae in the West Indies. Marine Biology 47:97-114.

Zerbini, A. N., E. J. Ward, P. G. Kinas, M. H. Engel and A. Andriolo. 2011. A Bayesian assessment of the conservation status of humpback whales (Megaptera novaeangliae) in the western South Atlantic Ocean. Journal of Cetacean Research and Management 3:131-144. 120

DISCUSSÃO & CONCLUSÃO

Dentre todos os métodos existentes para estudar padrões espaciais de mamíferos marinhos, os mais usados têm sido os visuais. Métodos acústicos podem ajudar a superar dificuldades existentes na pesquisa de mamíferos marinhos, como condições ambientais, áreas de estudo muito extensas, necessidade de uma equipe grande, entre outros. A acústica passiva

é relativamente uma ferramenta nova no estudo de distribuição desses animais, se comparado com métodos e técnicas visuais (Sousa-Lima et al. 2013). Com o avanço e surgimento de novas tecnologias de monitoramento acústico, é provável que tais métodos venham a ser mais utilizados com o passar do tempo. A combinação de métodos acústicos e visuais, podem gerar dados com uma maior confiabilidade para estudar padrões espaciais do que se utilizados de forma independente (Pirotta et al. 2011, Williams et al. 2011, Rako et al. 2013).

O combinado de métodos acústicos e visuais combinados foi importante para o desenvolvimento deste trabalho. Fizemos uso de dados visuais para determinar a localização de grupos de baleias jubarte e junto com essa informação, utilizamos o monitoramento acústico para identificar se havia cantores presentes no grupo. A partir da união desses dados com outras informações relevantes ao estudo, podemos descrever variáveis que influenciam a distribuição espacial de cantores no Arquipélago de Abrolhos.

Áreas como o Arquipélago de Abrolhos, onde baleias jubarte se concentram para fins reprodutivos, possuem características ambientais específicas que podem influenciar os 121

padrões de distribuição desses animais (Erst & Rosenbaum 2003, Martins et al. 2013).

Informações sobre o ambiente em que estão inseridos, comportamentos e interações sociais, são extremamente relevantes no estudo da distribuição de baleias jubarte (Martins et al. 2001,

Robbins et al. 2001, Ersts & Rosenbaum 2003, Félix & Botero-Acosta 2011). Tais características englobam variáveis como profundidade, distância à costa, temperatura, composição de grupo, entre outros (Brown et al. 1995, Hooker et al. 1999, Gregr & Trites

2001, Davis et al. 2002, Ersts & Rosenbaum 2003, Félix & Botero-Acosta 2011). Dentre essas variáveis, encontramos que presença de filhotes, distância a corais e profundidade são as que melhor preveêm atividade vocal.

Através desse estudo, vimos que grupos sem filhotes são mais prováveis de possuírem um cantor do que grupos com filhotes. A presença de um filhote no par fêmea-filhote pode ser um indicador de que a fêmea provavelmente não está apta para reprodução, apesar de haver fêmeas que se reproduzem anualmente (Smultea 1994). A distribuição de fêmeas aptas para reprodução pode ser também uma variável importante na distribuição de machos cantores

(Frankel et al. 1995). Grupos com a presença filhotes se localizam em águas mais rasas

(Martins et al. 2001, Félix & Botero-Acosta 2011) sendo estas profundidades não necessariamente adequadas para machos interessados em cortejo (Smultea 1994).

Profundidade não é uma variável que explica apenas a distribuição de grupos com filhotes presentes, podendo influenciar também os padrões espaciais de machos juvenis, cantores e grupos competitivos (Félix & Haase 2005, Martins et al. 2001, Betancourt et al. 2012).

Acredita-se que machos cantores podem dar preferência a áreas mais profundas e sem a presença de barreiras físicas (Jones & Swartz 1984). 122

No Banco de Abrolhos, a existência de formações de corais se torna uma característica em comum na definição dos padrões de distribuição de baleias e embarcações (Martins et al.

2001, Leão et al. 2010). Variáveis ambientais influenciam a distribuição de machos cantores, por também interferirem na propagação do som. Barreiras físicas como os corais existentes em Abrolhos podem causar alterações na estrutura do som (Urick 1983, Richardson et al.

1995, Leão 2010). Dessa forma, pode causar uma deficiência na comunicação entre dois indivíduos, ou seja, a mensagem inicial produzida pelo emissor, será alterada e recebida com distorções pelo receptor (Richardson et al. 1995). Isto pode ser um dos fatores que influenciam a escolha dos locais onde os machos estariam cantando. Áreas ideais para a propagação do som seriam aquelas com maior profundidade e sem a presença de barreiras físicas (Frankel et al. 1995). Além de características ambientais, atividades antrópicas também podem funcionar como variáveis importantes na escolha de hábitat para baleias jubartes.

O principal corredor de navegação ao PNMA apresenta áreas de co-ocorrências entre embarações e baleias jubartes vocalmente ativas. Inclusive, áreas de maior ocorrência de barcos, coincidem com áreas de maior ocorrência de cantores. Interações entre embarcações e baleias podem trazer impactos negativos para os animais (Parsons 2012). Efeitos observados a curto prazo foram registrados em várias espécies de cetáceos, mostrando alteração de diversos tipos de comportamento (Valle & Cunha Mello 2006, Williams et al. 2009, Stamation et al.

2010, Seuront & Cribb 2011, Visser et al. 2011).

123

Além de efeitos negativos resultantes da presença física de embarcações, cetáceos sofrem também com os efeitos dos ruídos gerados pelas embarcações (Richardson et al.

1995). Baleias jubarte dependem do som para se comunicar a longas distâncias com fins de atrair parceiros (Clark & Clapham 2004, Darling et al. 2006) e os ruídos resultantes de atividades antrópicas podem se sobrepor em tempo e frequência com vocalizações (Erbe &

Farmer 2000, Cato et al. 2004, Sousa-Lima & Clark 2009). Esta sobreposição pode estar potencialmente mascarando informações importantes codificadas no som, prejudicando o sucesso reprodutivo dos indivíduos (Richardson et al. 1995, Charlton et al. 2007, Alcock

2011, Pack et al. 2012, Herman et al. 2013). Como mostramos aqui, os sons produzidos pelas embarcações atuantes em Abrolhos no ano de 2005, possuem mais energia na mesma banda de frequência que os cantos de baleias jubartes registrados no mesmo ano (Sousa-Lima &

Clark 2010).

Dentre as embarcações que frequentam o PNMA, as principais são turísticas. O turismo de observação de cetáceos é uma atividade que pode ser considerada benéfica por contribuir para a economia local e proporcionar à população melhores conhecimentos sobre a espécie-alvo (Hoyt 2001, Martins 2004). Porém, se não realizada de forma a favorecer tanto a população humana quanto a animal, pode se tornar prejudicial (Diegues 2001, Hoyt 2001,

Sousa-Lima & Clark 2009, Rossi-Santos 2012). Se as atividades de embarcações no entorno do Banco dos Abrolhos não forem manejadas levando em consideração todas as variáveis envolvidas, a população de baleias que frequenta essa área pode vir a enfrentar dificuldades para se comunicar e ter um declínio no sucesso reprodutivo (Bejder et al. 2006, Charlton et al.

2007). A geração de dados científicos como os apresentados neste trabalho é de extrema 124

importância para dar início a futuros estudos com fins de dar início a planos de manejo adaptativo (Blumstein 2007).

REFERÊNCIAS BIBLIOGRÁFICAS

Alcock, J. 2011. Comportamento animal: uma abordagem evolutiva. 9 ed. Artmed, Porto

Alegre.

Bailey, H. & Thompson, P. M. 2009. Using marine mammal habitat modelling to identify priority conservation zones within a marine protected area. Marine Ecology Progress Series,

378, 279-287.

Bejder, L., Samuels, A., Whitehead, H., Gales, N., Mann, J., Connor, R., Heithaus, M.,

Watson-Capps, J., Flaherty, C. & Krützen, M. 2006. Decline in relative abundance of bottlenose dolphins exposed to long-term disturbance. Conservation Biology, 20, 1791-1798.

Betancourt, L., Herrera-Moreno, A. & Beddal, K. 2012. Spatial distribution of humpback whales in Samaná Bay, Dominican Republic. Journal of Cetacean Research and

Management, SC/64/O12.

Blumstein, D. T. 2007. Darwinian decision making: Putting the adaptive into adaptive management. Conservation Biology, 21, 552-553.

Brown, M. R., Corkeron, P. J., Hale, P. T., Schultz, K. W. & Bryden, M. M. 1995.

Evidence for a sex-segregated migration in the humpback whale (Megaptera novaeangliae).

Proceedings of the Royal Society B, 259, 229-234. 125

Bryant, P. J., Lafferty, C. M. & Lafferty, S. K.. 1984. Reoccupation of Laguna Guerrero

Negro, Baja California, Mexico, by gray whales. In: The Gray Whale, Eschrichtius robustus

(Org. por M. L. Jones, S. L. Swartz & S. Leatherwood), pp. 375-387. Orlando: Academic

Press.

Buckstaff, K. C. 2004. Effects of watercraft noise on the acoustic behavior of bottlenose dolphins, Tursiops truncatus, in Sarasota Bay, Florida. Marine Mammal Science, 20, 709-725.

Carrera, M. L., Favaro, E. G. P. & Souto, A. 2008. The response of marine tucuxis (Sotalia fluviatilis) toward tourist boats involves avoidance behaviour and a reduction in foraging.

Animal Welfare, 17, 117-123.

Cato, D. H., McCauley, R. D. & Noad, M. J. 2004. Potential effects of noise from human activities on marine mammals. Proceedings of Acoustics 2004, Australian Acoustical Society

Conference, Gold Coast, 3-5 November. Pp 353-358.

Cerchio, S., Jacobsen, J. K. & Norris, T. F. 2001. Temporal and geographical variation in songs of humpback whales, Megaptera novaeangliae: synchronous change in Hawaiian and

Mexican breeding assemblages. Animal Behaviour, 62, 313-329.

Charlton, B., Reby, D. & McComb, K. 2007. Female red deer prefer the roars of larger males. Biology Letters, 3, 382-385.

Cholewiak, D. M., Sousa-Lima, R. S. & Cerchio, S. 2012. Humpback whale song hierarchical structure: historical context and discussion of current classification issues. Marine

Mammal Science, 29, E312-E332. 126

Clapham, P. J. 2000. The Humpback Whale: Seasonal Feeding and Breeding in a Baleen

Whale. In: Cetacean Societies: Field Studies of Dolphin and Whales (Org. por J. Mann, R. C.

Connor, P. L. Tyack & H. Whitehead), pp. 173-196. Chicago: The University of Chicago

Press.

Clapham, P. J. & Mead, J. G. 1999. Megaptera novaeangliae. Mammalian Species, 604, 1-

Clark, C. W. & Clapham, P. J. 2004. Acoustic monitoring on a humpback whale

(Megaptera novaeangliae) feeding ground shows continual singing into late Spring.

Proceedings of the Royal Society B, 271, 1051-1057.

Newfoundland, St. John's, Newfoundland.

Coscarella, M. A., Dans, S. L., Crespo E. A. & Pedraza, S. N. 2003. Potential impact of unregulated dolphin watching activities in Patagonia. Journal of Cetacean Research and

Management, 5, 77-84.

Dans, S. L., Crespo, E. A., Pedraza, S. N., Degrati, M. & Garaffo, G. V. 2008. Dusky dolphin and tourist interaction: effect on diurnal feeding behavior. Marine Ecology Progress

Series, 369,287-296.

Darling, J. D. 1983. Migrations, abundance and behaviour of Hawaiian humpback whales

(Megaptera novaeangliae). Ph.D. thesis, University of California, Santa Cruz. 127

Darling, J. D. & Sousa-Lima, R. S. 2005. Songs indicate interaction between humpback whale (Megaptera novaeangliae) populations in the Western and Eastern South Atlantic

Ocean. Marine Mammal Science, 21, 557-566.

Darling, J. D., Jones, M. E. & Nicklin, C. P. 2006. Humpback whale songs: Do they organize males during the breeding season? Behaviour, 143, 1051-1101.

Davis, R. W., Ortiga-Ortiz, J. G., Ribic, C. A., Evans, W. E., Biggs, D. C., Ressler, P. H.,

Cady, R. B., Leben, R. R., Mullin, K. D. & Würsig, B. 2002. Cetacean habitat in the northern gulf of Mexico. Deep-Sea Research I, 49, 121-142.

Dawbin, W. H. 1966. The seasonal migratory cycle of humpback whales. In:. Whales, dolphins and porpoises (Org. por K. S. Norris), pp. 145-170. Los Angeles: University of

California Press.

Diegues, A. C. 2001. Ecologia humana e planejamento costeiro. 2ed. NUPAUB, São Paulo.

Engel, M. H. 1996. Comportamento reprodutivo da baleia jubarte (Megaptera novaeangliae) em Abrolhos. Anais de Etologia, 14, 275-284.

Erbe, C. & Farmer, D. M. 2000. A software model to estimate zones of impact on marine mammals around anthropogenic noise. Journal of the Acoustical Society of America, 108,

1327-1331.

Ersts, P. J. & Rosenbaum, H. C. 2003. Habitat preference reflects social organization of humpback whales (Megaptera novaeangliae) on a wintering ground. Journal of Zoology, 260,

337-345. 128

Félix, F. & Haase, B. 2005. Distribution of humpback whales along the coast of Ecuador and management implications. Journal of Cetacean Research and Management, 7, 21-31.

Félix, F. & Waerebeek, K. V. 2005. Whale mortality from ship strikes in Ecuador and West

Africa. Latin American Journal of Aquatic Mammals, 4,55-60.

Félix, F. & Botero-Acosta, N. 2011. Distribution and behaviour of humpback whale mother- calf pairs during the breeding season off Ecuador. Marine Ecology Progress Series, 426, 277-

287.

Folkens, P. A., Reeves, R. R., Stewart, B. S., Clapham, P. J. & Powell, J. A. 2002. Guide to Marine Mammals of the World. New York: National Audubon Society.

Foote, A. D., Osborne, R. W. & Hoelzel, A. R. 2004. Whale-call response to masking boat noise. Nature, 428, 910.

Frankel, A. S., Clark, C. W., Herman L. M. & Gabriele, C. 1995. Spatial distribution, habitat utilization, and social interactions of humpback whales, Megaptera novaeangliae, off

Hawai'i determined using acoustic and visual techniques. Canadian Journal of Zoology, 73,

1134-1146.

Frantzis, A., Airoldi, S., Notarbartolo-di-Sciara, G., Johnson, C. & Mazzariol, S. 2011.

Inter-basin movements of Mediterranean sperm whales provide insight into their population structure and conservation. Deep-Sea Research I, 58, 454-459.

Gregr, E. J. & Trites, A. W. 2001. Predictions of critical habitat for five whale species in the waters of coastal British Columbia. Canadian Journal of Fisheries and Aquatic Science, 58,

1265-1285. 129

Herman, L. M., Pack, A. A., Spitz, S. S., Herman, E. Y. K., Rose, K., Hakala, S. &

Deakos, M. H. 2013. Humpback whale song: who sings? Behavioral Ecology and

Sociobiology, 67, 1653-1663.

Higdon, J. W., Hauser, D. D. W. & Ferguson, S. H. 2012. Killer whales (Orcinus orca) in the Canadian Arctic: Distribution, prey items, group sizes, and seasonality. Marine Mammal

Science, 28, E93-E109.

Hooker, S. K., Whitehead, H. & Gowans, S.. 1999. Marine protected area design and the spatial and temporal distribution of cetaceans in a submarine canyon. Conservation Biology,

13, 592-602.

Hoyt, E. 2001. Whale watching 2001: Worldwide tourism numbers, expenditures, and expanding socioeconomic benefits. Yarmouth Port: International Fund for Animal Welfare.

Ivashchenko, Y. & Clapham, P. 2010. Bowhead whales Balaena mysticetus in the Okhtsk

Sea. Mammal Review, 40, 65-89.

Jensen, A. S. & Silber, G. K.. 2004. Large whale ship strike database. (NMFS-OPR).

NOAA Technical Memorandum, January 2004, 37 pp.

Jones, M. L. & Swartz, S. L. 1984. Demography and phenology of Gray whales and evaluation of whale-watching activities in Laguna San Ignacio, Baja California Sur, Mexico.

Pages 309-374 in Jones, M. L., S. L. Swartz and S. Leatherwood eds. The gray whale

Eschrichtius robustus. Academic Press Inc., Orlando. 130

Kaschner, K., Watson, R., Trites, A. W. & Pauly, D. 2006. Mapping world-wide distributions of marine mammal species using a relative environmental suitability (RES) model. Marine Ecology Progress Series, 316, 285-210

Langtimm, C. A., Dorazio, R. M., Stith, B. M. & Doyle, T. J. 2011. New aerial survey and hierarchical model to estimate manatee abundance. Journal of Wildlife Management, 75, 399-

412.

Leão, Z. M. A. N., Kikuchi, R. K. P., Oliveira, M. D. M. & Vasconcellos, V. 2010. Status of Eastern Brazilian coral reefs in time of climate changes. Pan-American Journal of Aquatic

Sciences, 5, 224-235.

Lusseau, D. 2005. Residency pattern of bottlenose dolphins Tursiops spp. in Milford Sound,

New Zealand, is related to boat traffic. Marine Ecology Progress Series, 295, 265-272.

Lusseau, D. 2006. The short-term behavioral reactions of bottlenose dolphins to interactions with boats in Doubtful Sound, New Zealand. Marine Mammal Science, 22, 802-818.

Lusseau, D., Bain, D. E., Williams, R. & Smith, J. C. 2009. Vessel traffic disrupts the foraging behavior of southern resident killer whales Orcinus orca. Endangered Species

Research, 6, 211-221.

Martins, C. C. A. 2004. O uso do sistema de informações geográficas como ferramenta na identificação de áreas prioritárias para a conservação da população de baleia jubarte,

Megaptera novaeangliae, em seu sítio reprodutivo na costa leste do Brasil. Masters dissertation, Universidade de Brasília, Brasília, Brasil, 119 pp. 131

Martins, C. C. A., Morete, M. E., Engel, M. H., Freitas, A. C., Secchi E. R., & Kinas, P.

G. 2001. Aspects of habitat use patterns of humpback whales in the Abrolhos Bank, Brazil, breeding ground. Memoirs of the Queensland Museum, 47, 563-570.

Martins, C. C. A., Andriolo, A., Engel, M. H., Kinas, P. G. & Saito, C. H. 2013.

Identifying priority areas for humpback whale conservation at Eastern Brazilian Coast. Ocean

& Coastal Management, 75, 63-71.

Mattson, M. C., Thomas, J. A. & St. Aubin, D. 2005. The effect of boat activity on the behavior of bottlenose dolphins (Tursiops truncatus) in waters surrounding Hilton Head

Island, South Carolina. Aquatic Mammals, 31, 133-140.

Mellinger, D. K., Stafford, K. M., Moore, S. E., Dziak, R. P. & Matsumoto, H. 2007. An overview of fixed passive acoustic observation methods for cetaceans. Oceanography, 20, 36-

45.

Mercado, E. III & Frazer, L. N.. 1999. Environmental constraints on sound transmission by humpback whales. Journal of the Acoustical Society of America, 106, 3004-3016.

Newhall, A. E., Lin, Y.-T., Lynch, J. F., Baumgartner, M. F. & Gawarkiewicz, G. G.

2012. Long distance passive localization of vocalizing sei whales using an acoustic normal mode approach. Journal of the Acoustical Society of America, 131, 1814-1825.

Noren, D. P., Johnson, A. H., Rehder, D. & Larson, A. 2009. Close approaches by vessels elicit surface active behaviors by southern resident killer whales. Endangered Species

Research, 8, 179-192. 132

Norris, T. F., McDonald, M. & Barlow, J. 1999. Acoustic detections of singing humpback whales (Megaptera novaeangliae) in the eastern North Pacific during their northbound migration. Journal of the Acoustical Society of America, 106, 506-514.

Pack, A. A., Herman, L. M., Spitz, S. S., Craig, A. S., Hakala, S., Deakos, M. H.,

Herman, E. Y. K., Milette, A. J., Carroll, E., Levitt, S. & Lowe, C. 2012. Size-assortative pairing and discrimination of potential mates by humpback whales in the Hawaiian breeding grounds. Animal Behaviour, 84, 983-993.

Parsons, E. C. M. 2012. The negative impacts of whale-watching. Journal of Marine

Biology, 2012, 1-9.

Parsons, E. C. M., Warburton, C. A., Woods-Ballard, A., Hughes, A. & Johnston, P.

2003. The value of conserving whales: the impacts of cetacean-related tourism on the economy of rural West Scotland. Aquatic Conservation, 13, 397-415.

Payne, R. S. & McVay, S. 1971. Songs of Humpback Whales. Science, 173, 585-597.

Pirotta, E., Matthiopoulos, J., MacKenzie, M., Scott-Hayward, L. & Rendell, L. 2011.

Modelling sperm whale habitat preference: a novel approach combining transect and follow data. Marine Ecology Progress Series, 436, 257-272.

Rako, N., Fortuna, C. A., Holcer, D., Mackelworth, P., Nimak-Wood, M., Plesić, G.,

Sebastianutto, L., Vilibić, I., Wiemann, A. & Picciulin, M. 2013. Leisure boating noise as a trigger for the displacement of the bottlenose dolphins of the Cres-Lošinj archipelago

(northeastern Adriatic Sea, Croatia). Marine Pollution Bulletin, 68, 77-84. 133

Rasmussen, K., Palacios, D. M., Calambokidis, J., Saborío, M. T., Rosa, L. D., Secchi, E.

R., Steiger, G. H., Allen, J. M. & Stone, G. S. 2007. Southern Hemisphere humpback whales wintering off Central America: insights from water temperature into the longest mammalian migration. Biology Letters, 3, 302-305.

Redfern, J. V., Ferguson, M. C., Becker, E. A., Hyrenbach, K. D., Good, C., Barlow, J.,

Kaschner, K., Baumgartner, M. F., Forney, K. A., Balance, L. T., Fauchald, P., Halpin,

P., Hamazaki, T., Pershing, A. Z., Qian, S. S., Read, A., Reilly, S. B., Torres, L. &

Werner, F. 2006. Techniques for cetacean-habitat modeling. Marine Ecology Progress

Series, 310, 271-295.

Reeves, R. R., Smith, B. D., Crespo, E. A. & Notarbartolo di Sciara, G. 2003. Dolphins, whales and porpoises - 2002-2010 Conservation Action Plan for the World's Cetaceans. In:

IUCN/SSC Cetacean Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, 139 pp.

Richardson, J. W., Grenne, C. R., Malme, C. L. & Thomson, D. H. 1995. Marine

Mammals and Noise. Academic Press: San Diego.

Robbins, J., Bérubé, M., Clapham, P. J., Friday, N. & Mattila, D. 2001. Structure and regional composition of the Gulf of Maine humpback whale (Megaptera novaeangliae) population. International Whaling Commission Conference, C/53/NAH12:1-11.

Rossi-Santos, M. R. 2012. Comportamento e ecologia acústica da baleia Jubarte (Megaptera novaeangliae) na região Nordeste do Brasil. Tese de Doutorado, Universidade Federal do Rio

Grande do Norte, Natal, RN, 173 pp. 134

Santos, M. C. DE O., Siciliano, S., Vicente, A. F. DE C., Alvarenga, F. S., Zampirolli, É.,

Souza, S. P. & Maranho, A. 2010. Cetacean records along São Paulo state coast, southeastern Brazil. Brazilian Journal of Oceanography, 58, 123-142.

Scarpaci, C., Bigger, S. W., Corkeron, P. J. & Nugegoda, D. 2000. Bottlenose dolphins,

Tursiops truncatus, increase whistling in the presence of "swim-with-dolphin" tour operations. Journal of Cetacean Research and Management, 2, 183-185.

Scheidat, M., Castro, C., González, J. & Williams, R. 2004. Behavioural responses of humpback whales (Megaptera novaeangliae) to whalewatching boats near Isla de la Plata,

Machalilla National Park, Ecuador. Journal of Cetacean Research & Management, 6, 63-68.

Seuront, L. & Cribb, N. 2011. Fractal analysis reveals pernicious stress levels related to boat presence and type in the Indo Pacific bottlenose dolphin, Tursiops aduncus. Physica A, 390,

2333-2339.

Siciliano, S. 1997. Características da população de baleias jubarte (Megaptera novaeangliae) na Costa Brasileira, com especial referência aos Bancos dos Abrolhos. MSc. Thesis,

Universidade Federal Rural do Rio de Janeiro.

Smultea, M. A. 1994. Segregation by humpback whale (Megaptera novaeangliae) cows with a calf in coastal habitat near the Island of Hawaii. Canadian Journal of Zoology, 72, 805-811.

Sousa-Lima, R. S. & Clark C. W. 2008. Modelling the effect of boat traffic on the fluctuation of humpback whale singing activity in the Abrolhos National Marine Park, Brazil.

Canadian Acoustics, 36, 174-181. 135

Sousa-Lima, R. S. & Clark, C. W. 2009. Whale sound recording technology as a tool for assessing the effects of boat noise in a Brazilian marine park. Park Science 26:59-63.

Sousa-Lima, R. S., Cortopassi, K. A. & Clark, C. W. 2010. Humpback whale posture and song propagation in very shallow water. Journal of the Acoustical Society of America, 128,

2467.

Sousa-Lima, R. S., Norris, T. F., Oswald, J. N. & Fernandes, D. P. 2013. A review and inventory of fixed autonomous recorders for passive acoustic monitoring of marine mammals.

Aquatic Mammals, 39, 23-53.

Stamation, K. A., Croft, D. B., Shaughnessy, P. D. & Waples, K. A. 2007. Observations of humpback whales (Megaptera novaeangliae) feeding during their southward migration along the coast of southeastern New South Wales, Australia: identification of a possible supplemental feeding ground. Aquatic Mammals, 33, 165-174.

Stamation, K. A., Croft, D. B., Shaughnessy, P. D., Waples, K. A. & Briggs, S. V. 2010.

Behavioral responses of humpback whales (Megaptera novaeangliae) to whale-watching vessels on the southeastern coast of Australia. Marine Mammal Science, 26, 98-122.

Stockin, K. A., Lusseau, D., Binedell, V., Wiseman, N. & Orams, M. B. 2008. Tourism affects the behavioural budget of the common bottlenose dolphin Delphinus sp. in the Hauraki

Gulf, New Zealand. Marine Ecology Progress Series, 355, 287-295. do Valle, L. & Cunha Melo, F. C. 2006. Behavioral alterations in the gray dolphin Sotalia guianensis (Gervais, 1953) caused by sea traffic. Biotemas, 19, 75-80. 136

Thompson, T. J., Winn, H. E. & Perkins, P. J. 1979. Mysticete sounds. In: Behavior of marine animals, current perspectives in research, Vol. 3, Cetaceans. (Org. por H. E. Winn, B.

L. Olla), pp. 403-431. New York: Plenum Press.

Thompson, P. O., Cummings, W. C. & Ha, S. J. 1986. Sounds, source levels, and associated behavior of humpback whales, southeast Alaska. Journal of the Acoustical Society of America, 80, 735-740.

Timmel, G., Courbis, S. Sargeant-Green, H. & Markowitz, H. 2008. Effects of human traffic on the movement patterns of Hawaiian spinner dolphins (Stenella longirostris) in

Kealakekua bay, Hawaii. Aquatic Mammals, 34, 402-411.

Valle, L. & Cunha Melo, F. C. 2006. Behavioral alterations in the gray dolphin Sotalia guianensis (Gervais, 1953) caused by sea traffic. Biotemas, 19, 75-80.

Van Parijs, S. M., Clark, C. W., Sousa-Lima, R. S., Parks, S. E., Rankin, S., Risch, D. &

Van Opzeeland, I. C. 2009. Management and research applications of real-time and archival passive acoustic sensors over varying temporal and spatial scales. Marine Ecology Progress

Series, 395, 21-36.

Visser, F., Hartman, K. L., Rood, E. J. J., Hendriks, A. J. E., Zult, D. B., Wolff, W. J.,

Huisman, J. & Pierce, G. J. 2011. Risso's dolphins after daily resting pattern in response to whale watching at the Azores. Marine Mammal Science, 27, 366-381.

Ward, J., Morrissey, R., Moretti, D., DiMarzio, N., Jarvis, S., Johnson, M., Tyack, P. &

White, C. 2008. Passive acoustic detection and localization of Mesoplodon densirostris

(Blaiville’s Beaked Whale) vocalizations using distributed bottom-mounted hydrophones in conjunction with a digital tag (DTAG) recording. Canadian Acoustics, 36, 60-66. 137

Weir, C. R. 2010. A Review of cetacean occurrence in West African waters from the Gulf of

Guinea to Angola. Mammal Review, 40, 2-39.

Whitehead, H. & Moore, M. J. 1982. Distribution and movements of West Indian humpback whales in winter. Canadian Journal of Zoology, 60, 2203-2211.

Williams, R., Trites, A. W. & Bain, D. E. 2002. Behavioural responses of killer whales

(Orcinus orca) to whale-watching boats: Opportunistic observations and experimental approaches. Journal of Zoology, 256, 255-270.

Williams, R., Bain, D. E., Smith, J. C. & Lusseau, D. 2009. Effects of vessel on behaviour patterns of individual southern resident killer whales Orcinus orca. Endangered Species

Research, 6, 199-209.

Williams, R., Hedley, S. L., Branch, T. A., Bravington, M. V., Zerbini, A. N. & Findlay,

K. P. 2011. Chilean blue whales as a case study to illustrate methods to estimate abundance and evaluate conservation status of rare species. Conservation Biology, 25, 526-535.

Williams, R., Lusseau, D. & Hammond, P. S. 2006. Estimating relative energetic costs of human disturbance to killer whales (Orcinus orca). Biological Conservation, 133, 301-311.

Williams, R., Bain, D. E., Smith, J. C. & Lusseau D. 2009. Effects of vessel on behaviour patterns of individual southern resident killer whales Orcinus orca. Endangered Species

Research, 6, 199-209.

Wursig, B. 1988. The behavior of baleen whales. Scientific American, 258, 102-107.

Zerbini, A. N., Andriolo, A., Da Rocha, J. M., Simões-Lopes, P. C., Siciliano, S.,

Pizzorno, J. L., Waite, J. M., DeMaster, D. P. & VanBlaricom, G. R. 2004. Winter 138

distribution and abundance of humpback whales (Megaptera novaeangliae) off Northern

Brazil. The Journal of Cetacean Research and Management, 6, 101-107.

Zerbini, A. N., Andriolo, A., Heide-Jørgensen, M. P., Moreira, S. C., Pizzorno, J. L.,

Maia, Y. G., VanBlaricom, G. R. & DeMaster, D. P. 2011. Migration and summer destination of humpback whales (Megaptera novaeangliae) in the western South Atlantic

Ocean. The Journal of Cetacean Research and Management, 3, 113-118.

139

APPENDIX A - SURVEY

1. On a scale of 1 to 7 (1 being least important and 7 most important), please rate how

important (limiting influence) each item below was in planning your research and how

they influenced your choice of the technique or method used. Please focus your rating on

what was used in your research paper mentioned above, whether it was acoustic, visual or

a combination of both

a) The “umbrella” project of which my study was a part, had more general 1 2 3 4 5 6 7 research objectives.

b) The study itself was motivated by specific research questions that

depended directly on the technique or method used, i. e., studies about 1 2 3 4 5 6 7

sounds depended on the use of some acoustic recording technique.

c) The lack of available equipment. 1 2 3 4 5 6 7

d) The high cost of equipment. 1 2 3 4 5 6 7

e) A small staff size or lack of personnel to collect and/or process data. 1 2 3 4 5 6 7

f) The survey area was very large and/or difficult to access, and/or 1 2 3 4 5 6 7 presented extreme/challenging environmental conditions.

g) The total range/area of the study, whether it was local, regional or 1 2 3 4 5 6 7 global.

h) Personnel not qualified or specifically trained to collect and/or process 1 2 3 4 5 6 7 data.

i) Time consuming and/or complex data processing requirements. 1 2 3 4 5 6 7 140

2. Please describe on the following items, as specifically as possible, how these issues

influenced positively or negatively the choice of the technique or method used. Remember

to focus your description on what was used in your research paper mentioned above,

whether it was acoustic, visual or a combination of both:

a) Equipment and techniques were applied in a broader or more general research project

- Advantages

- Disadvantages

b) Research questions depended on the technique or methodology used

- Advantages

- Disadvantages

c) Equipment availability

- Advantages

- Disadvantages

d) Equipment cost

- Advantages

- Disadvantages

e) Size and availability of research staff

- Advantages

- Disadvantages

f) Size, access and environmental conditions of survey area

- Advantages

- Disadvantages 141

g) Total range/area of the study (local, regional or worldwide)

- Advantages

- Disadvantages

h) Lack of qualified or specifically trained personnel to collect and/or process data

- Advantages

- Disadvantages

i) Data processing time and complexity

- Advantages

- Disadvantages

3. Please describe any other advantages or disadvantages that you considered when planning

your research project. Please focus your description on the technique that was used in your

research paper mentioned above, whether it was acoustic, visual or a combination of both.