UNIVERSIDADE FEDERAL DO PARÁ INSTITUTO DE CIÊNCIAS BIOLÓGICAS PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA AQUÁTICA E PESCA MAMÍFEROS AQUÁTICOS DA COSTA AMAZÔNICA E DELTA DO PARNAÍBA: DIVERSIDADE E RELAÇÕES TRÓFICAS ALEXANDRA FERNANDES COSTA Orientador: Dr. Tommaso Giarrizzo Co-orientador: Dr. Salvatore Siciliano Belém – Pará 2015
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UNIVERSIDADE FEDERAL DO PARÁ INSTITUTO DE CIÊNCIAS BIOLÓGICAS
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA AQUÁTICA E PESCA
MAMÍFEROS AQUÁTICOS DA COSTA AMAZÔNICA E DELTA DO PARNAÍBA:
DIVERSIDADE E RELAÇÕES TRÓFICAS
ALEXANDRA FERNANDES COSTA
Orientador: Dr. Tommaso Giarrizzo
Co-orientador: Dr. Salvatore Siciliano
Belém – Pará 2015
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UNIVERSIDADE FEDERAL DO PARÁ INSTITUTO DE CIÊNCIAS BIOLÓGICAS
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA AQUÁTICA E PESCA
ALEXANDRA FERNANDES COSTA
MAMÍFEROS AQUÁTICOS DA COSTA AMAZÔNICA E DELTA DO PARNAÍBA:
DIVERSIDADE E RELAÇÕES TRÓFICAS
Tese apresentada ao Programa de Pós-Graduação em Ecologia Aquática e Pesca da Universidade Federal do Pará
como requisito parcial para obtenção do título de Doutor em Ciências Biológicas
na área de Ecologia Aquática e Pesca.
Orientador: Dr. Tommaso Giarrizzo
Co-orientador: Dr. Salvatore Siciliano
Belém – Pará 2015
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AGRADECIMENTOS Em primeiro lugar agradeço à minha família, sempre ao meu lado me apoiando e acreditando neste caminho profissional tortuoso que escolhi. À minha mãe Eunice por ter ajudado sempre em todos os sentidos me deixando carregar boto morto dentro do seu carro. A minha irmã, Ninha toda sua ajuda nas formatações, consultorias diversas e coleta de material. Ao Mike por ajudar nas revisões de inglês. A minha filha Catarina por ter entendido minhas ausências por conta do trabalho em todos esses anos. Ao meu pai por ter sempre dito que o mais importante da vida é o nosso estudo. A minha Tchuchu por estar sempre ao meu lado, minha companheira. Ao Salvatore Siciliano por ter sido sempre meu mentor e minha inspiração no trabalho com os mamíferos aquáticos. Obrigada Sal por ter sempre acreditado em mim, e ser além de orientador um grande amigo. Ao meu orientador Tommaso Giarrizzo, obrigada por ter aceitado entrar no mundo dos mamíferos aquáticos, por todo apoio ao meu grupo de pesquisa abrindo as portas do GEA a mim e a todos que carreguei para executar seus trabalhos. A todos os companheiros que passaram pelo GEMAM ao longo desses anos por terem ajudado em todos os campos, encalhes difíceis e tudo o mais. Nosso trabalho não é fácil, mas vamos continuar acreditando. Ao Cazuza por ter acreditado no GEMAM e aberto as portas do Museu Emílio Goeldi ao nosso grupo. Sem o seu apoio não teríamos chegado até aqui.
Agradeço in memoriam aos naturalistas e pesquisadores do MPEG que coletaram os exemplares de peixes-boi e botos de rio na bacia Amazônica. Agradeço especialmente a você Rê por ter sempre me apoiado, incentivando a seguir em frente mesmo em meio a todas as dificuldades. Se não fosse seu incentivo não teria entrado no doutorado. Obrigada pela nossa caminhada profissional no GEMAM. Tantas conquistas, vamos continuar acreditando que vale a pena. À tia Neusa e tio Jorge por terem me recebido por mais de um ano em sua casa e serem minha família paraense. À Maura por todos os seus porquês, por ter me feito acreditar que valia a pena nos momentos difíceis. Agradeço a você e a toda a sua família por tudo que fizeram e fazem por mim. Obrigada a você e ao Renan pela confecção dos mapas ao longo do caminho, e por serem meus filhotes crescidos. Ao Victor Carvalho pelos anos de companheirismo e por me proporcionar um lar até o fim dessa jornada. À Jacqueline Vieira por ter acreditado no nosso trabalho, ajudando nas coletas dos exemplares do Delta e do Pará e fornecendo com teu estudo informações tão importantes para a discussão do meu trabalho. Vamos seguir em frente. Obrigada Jac pela amizade e por ter quebrado tantos galhos pessoais.
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Aos amigos que me permitiram entrar na família GEA. Rory obrigada por todo empenho no processo das amostras e Allan por me apresentar o mundo “R”, sem você não teria rodado as análises. Fabiola obrigada por todos os cafezinhos, por liberar material do laboratório sempre que precisei e por ser uma ótima companheira de campo.
À Pri Miorando por ter me dado apoio profissional nas discussões ecológicas e isotópicas sobre os “chupa leite”, ajudado na revisão dos textos finais e ter sido tão boa amiga nos momentos mais difíceis do final dessa caminhada.
Ao Alejo por ter mostrado que o mundo isotópico podia ser belo. Todas as nossas conversas e discussões foram importantes na construção desse trabalho.
À Malu Claudino por ter repassado tantas dicas sobre os isótopos mostrando que a ferramenta não era um bicho de sete cabeças.
À Ingrid Clark por ter acreditado no meu trabalho, dividindo as responsabilidades junto ao Instituto Ilha do Caju (PROCEMA). Obrigada por todas as concessões feitas a mim e por além de chefe ter se transformado em uma grande amiga.
Às minhas amigas de Parnaíba de quem sinto tanta falta por sempre torcerem por mim, mesmo não entendendo nada do que faço. Ana, Dri, Pat vocês me deram tanto apoio mesmo sem saber.
À minha querida Aline Cerqueira. Amiga, tuas palavras de apoio e ordem foram sempre um estímulo a mais. Começamos juntas nessa caminhada ainda nadando com os botos em Fortaleza. Obrigada por todo apoio, mesmo estando do outro lado do Atlântico. Depois disso tudo vamos comemorar juntas.
Ao querido Maíca por me carregar para cima e para baixo no Delta do Parnaíba. Ninguém conhece como você essa região. Obrigada por ser do seu jeito um grande defensor desse ambiente.
Ao Quadrado por toda dedicação nas coletas de tantos exemplares de botos. Meu amigo, sem você eu não teria tanta diversidade de espécies do Delta. Obrigada por ter sido sempre “meus olhos” monitorando a Pedral mesmo eu estando longe. Valeu!!!
À Silvina Botta por ter me inspirado neste trabalho, e por ter me acolhido no Laboratório de Ecologia e Conservação da Megafauna Marinha/FURG me repassando tantos conhecimentos, tanto em relação aos isótopos quanto à determinação de idade. Obrigada Sil por ter sido informalmente minha orientadora, ajudando em todos os passos do processo.
Ao Dr. Seth Newsome por ter acreditado em nossa pesquisa analisando todas as amostras no Centro de Isótopos da University of New Mexico. Thank you very much for all logistical support to the study and to show the best way to analyze our data.
Ao Programa de Pós-Graduação em Ecologia Aquática e Pesca (PGEAP) por proporcionar suporte nesses anos de curso, especialmente à nossa coordenadora Jussara Martinelli por sempre quebrar os galhos dos alunos e pelo empréstimo da balança analítica. A CAPES pela concessão da bolsa de estudo.
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Amar-se é respeitar-se,
É ensejar-se as conquistas
superiores da vida”.
Joana de Angelis
Foto
Ro
dri
go B
alei
a
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RESUMO
A costa Amazônica e parte do Nordeste são as áreas menos pesquisadas em relação aos
mamíferos aquáticos na costa brasileira. A formação de grupos de pesquisa e o incremento na
coleta de informações advindas dos eventos de encalhes são aspectos recentes para a Região
Norte e vem contribuindo para diminuir as lacunas do conhecimento sobre este grupo animal.
Informações sobre a biologia das espécies, uso do habitat e as relações tróficas devem ser
coletadas. Espécies como o peixe-boi-da-Amazônia (Trichechus inunguis), o boto-cinza (Sotalia
guianensis) e os botos de rio (Inia geoffrensis e I. araguaiaensis) sofrem sérias ameaças à sua
sobrevivência e necessitam que sejam desenvolvidas estratégias de manejo e conservação para
as espécies e seu habitats. O estudo reporta eventos incomuns de encalhes de mamíferos
aquáticos, registrados no período de 2003 a 2014 na zona costeira dos estados do Pará,
Maranhão e Piauí. Desde a publicação em 2008 da lista mais recente de mamíferos aquáticos,
registramos a ocorrência de outras quatro espécies na área de estudo: a baleia-Sei
(Balaenoptera borealis), a baleia-Fin (Balaenoptera physalus), o golfinho-cabeça-de-melão
(Peponocephala electra) e a falsa-orca (Pseudorca crassidens) ampliando a riqueza de espécies
para a costa Amazônica para vinte e seis, englobando desde golfinhos oceânicos até as maiores
baleias existentes. O presente estudo comparou trabalhos pretéritos que registraram
comunidades de cetáceos do Norte e Nordeste do Brasil com registros realizados na região sul
do Caribe. Os resultados mostraram que existe uma alta similaridade entre as composições
destas regiões, comprovando a conexão da costa Amazônica com a fauna de cetáceos do
Caribe. Outra ferramenta utilizada neste estudo foi a análise de isótopos estáveis realizada com
o material ósseo coletado durante os eventos de encalhe mencionados anteriormente. A análise
de isótopos de carbono e nitrogênio foi utilizada a fim de: 1) investigar o uso do habitat e as
relações tróficas entre espécies marinhas e de água doce; 2) avaliar a partição de nicho
isotópico entre as espécies mais abundantes na costa Amazônica (S. guianensis, Inia spp. e T.
inunguis) e 3) estimar as diferenças de nicho isotópico entre estoques ecológicos do boto-cinza
na costa Amazônica e no Delta rio Parnaíba. Na costa brasileira ainda são poucos os estudos que
utilizam os isótopos estáveis como ferramenta para elucidar as relações tróficas entre as
comunidades de mamíferos aquáticos. Neste estudo, foram analisadas amostras de 14 espécies
entre cetáceos e sirênios (N=267). Foi observado um padrão espacial costa-oceano para as
espécies marinhas, apresentando valores de 13C mais enriquecidos nas costeiras, enquanto as
oceânicas mostraram valores mais empobrecidos de carbono. Os estoques de boto-cinza do
Delta do Parnaíba (NC) e costa Amazônica (AE) apresentaram valores similares de 15N.
Contudo, o grupo NC apresentou valores mais enriquecidos de 13C. Os nichos isotópicos foram
altamente diferenciados entre as espécies mais abundantes (T. inunguis, S. guianensis e Inia
spp.) não apresentando sobreposição de nicho indicando forte segregação de nicho isotópico
pelo menos na baía do Marajó. Este estudo fornece a primeira avaliação da composição
isotópica de mamíferos aquáticos do norte do Brasil.
Palavras-chave: Amazônia. Delta do Parnaíba. Encalhes. Ecologia trófica. Cetacea. Sirenia.
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ABSTRACT
The Amazon and most of the Northeastern coast of Brazil are some of the least researched
areas in the country with regards to aquatic mammals. The organization of new specialized
research groups and the increase in data sampling frequency from stranding events in these
regions, help to fill in the knowledge gaps about this group of animals. It is therefore of
paramount importance that information focusing on species biology, habitat use and trophic
relationships are gathered. The Amazonian manatee (Trichechus inunguis), Guiana dolphin
(Sotalia guianensis) and river dolphins (Inia geoffrensis e I. araguaiaensis) face serious threats to
their survival and require the development of effective management and conservation
strategies both at species and habitat level. This study reports on rare stranding events of
aquatic mammals recorded between the years of 2003 and 2014, in the coasts of the states of
Pará, Maranhão and Piauí. Since the publication of the latest list of aquatic mammals in 2008,
we have recorded the occurrence of other four new species for these regions: Sei whale
(Balaenoptera borealis), Fin whale (Balaenoptera physalus), Melon-headed whale
(Peponocephala electra) and False killer whale (Pseudorca crassidens), expanding the number of
species in the Amazon coast to 26 species, that range from oceanic dolphins to some of the
largest existing whales. This study also compared cetacean communities’ records between the
North and the Northeastern coasts of Brazil with the Southern Caribbean. The results from this
comparison show a high similarity between the communities’ compositions of these regions,
indicating a connection between the cetacean fauna of the Amazon region and the Southern
Caribbean. Another tool used in this study was the analysis of stable isotopes using bone
material collected during the stranding events mentioned above. The analysis of carbon and
nitrogen isotopes was used in order to: 1) investigate the habitat use and trophic relationships
among marine and freshwater species; 2) evaluate the isotopic niche partitioning among the
most abundant species in the Amazon coast (S. guianensis, Inia spp. and T. inunguis), and 3)
estimate the isotopic differences between ecological niche of the estuarine dolphin stocks in the
Amazon coast and in the Parnaíba River Delta. There are still few studies using stable isotopes
as a tool to elucidate the trophic relationships between aquatic mammal communities in the
Brazilian coast. In this study, samples from 14 species of cetaceans and sirenians (N= 267) were
analyzed. A coastal-oceanic spatial pattern was observed in the marine species, showing more 13C enriched values in the coastal species, while oceanic species showed depleted carbon values.
Guiana dolphin stocks from the Parnaíba River Delta (NC) and the Amazon coast (AE) showed
similar values of 15N. The NC group however, showed enriched values of 13C. The isotopic
niches were highly differentiated among the most abundant species (T. inunguis, S. guianensis
and Inia spp.), showing no niche overlap and indicating strong niche segregation isotopic at least
in Marajó bay. This study provides the first assessment of the isotopic composition of aquatic
N values for Inia genus: Inia geoffrensis (n=8), I. araguaiaensis (n=3) and Inia
spp. not identified (n=9). Samples were collected along the Amazon Lowland (AL) and Amazon Estuary and
adjacent coastal zone (AE), Northern and Northeastern Brazil, respectively. ....................................................... 88
Figure 4. Stable isotope bi-plot (13
C versus 15
N) showing the isotope niche area of Inia_spp. (n= 20, red line),
T_inunguis (n= 11, ligth blue line), Sgui_AE (n=175, dark blue line), Sgui_NC (n= 32, green line) and Delphinids (n=
26, black line). Solid lines represent SEAc (standard ellipses areas) adjusted for small sample sizes, containing c.
40% of data (Jackson et al., 2011) within each group. There is no overlap among the most representative species
of the study area (Sotalia guianensis, Inia spp. and Trichechus inunguis). The overlap expressed the significant
isotope niche partitioning among Delphinids and populations of S. guianensis. .................................................. 89
Figure 5. Plots showing the variation in 13
C and 15
N values for Delphinids (n= 26), Inia_sp. (n=20), Sgui_NC (n=
32), Sgui_AE (n= 175) and T_inunguis (n=11) from Northern and Northeastern Brazil. Black circles (mode)
represent the SEA, boxes indicate 50%, 75% and 95% credible intervals from dark grey to light grey, respectively.
Red square indicate the SEAc (SEA corrected for small samples sizes) of Bayesian standard ellipse areas. .......... 90
Figure 6. Zoom of the plots showing the variation in 13
C and 15
N values for Guiana dolphin Sotalia guianensis
from Northeastern coast (NC) and Amazon Estuary and adjacent coastal zone (AE), respectively (Sgui_NC and
Sgui_AE). Black circles represent mode of SEA. Boxes indicate 50%, 75% and 95% credible intervals from dark
grey to light grey, respectively. Red square indicate the SEAc (SEA corrected for small samples sizes) of Bayesian
standard ellipse areas. ......................................................................................................................................... 90
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LISTA DE TABELAS
CAPÍTULO I - Stranding survey as a framework to investigate rare cetacean records of the North and
North-eastern Brazilian coasts.
Table 1. Records of cetaceans stranded from 2003 to 2014 on the North and Northeastern Brazilian coast. TL
(total length in meters), NI (not identified). The study area was divided in three sectors: Eastern Pará state (EP),
Marajó bay (MB) and Maranhão/Piauí coastline (MA/PI). ................................................................................... 70
CAPÍTULO II - Stable Isotopes of Carbon and Nitrogen Reveal Resource Partitioning Among Aquatic Mammals
from Amazon and Northeastern Coast of Brazil.
Table 1. Isotope values of 13
C and 15
N (in ‰) for aquatic mammal bone samples. Specimens were collected
from Northern (Amazon Lowland, AL and Amazon Estuary and adjacent coastal zone, AE) and Northeastern Brazil
(coastline of Maranhão and Piauí states, NC). ...................................................................................................... 86
Table 2. Isotope niche width of five groups of aquatic mammals: Trichechus inunguis (T_inunguis), Inia spp. (Inia
geoffrensis, I. araguaiaensis), Delphinids and Sotalia guianensis (Sgui_NC and Sgui_AE). SEA represents standard
ellipses area and SEAc standard ellipses adjusted for small sample sizes. ................................................ 89
maritima, Spartina sp.) (GUTERRES et al., 2008; SOUSA, 2011; SOUSA et al., 2014), além das
espécies de manguezal já descritas na dieta da espécie marinha (BEST, 1981; BORGES;
EMMANUEL; MIRANDA, 2008). Os espécimes que vivem na baía do Marajó não sofrem com os
efeitos das alterações dos níveis de cheias e secas como acontece com espécimes que vivem na
Amazônia central, que realizam migrações para lagos onde encontram maior oferta de alimento
(ARRAUT, 2008).
O peixe-boi-da-Amazônia é considerado uma espécie vulnerável que exerce um
importante papel ecológico no complexo bioma da Amazônia (BRASIL, 2014). A principal
ameaça, desde tempos históricos, continua sendo a captura intencional para alimentação da
população ribeirinha. Outras ameaças diretas à espécie são relativas à degradação do ambiente
com o intenso tráfego hidroviário, ocupação humana, contaminação ambiental, e projetos
agropecuários (ANDRADE; LUNA; REIS, 2011). Em resposta a estas intensas ameaças, a espécie
está categorizada como “Vulnerável” tanto pela IUCN (SECCHI, 2012) quanto pelo documento
nacional (BRASIL, 2014).
Neste estudo, utilizamos a análise de isótopos estáveis para caracterizar as relações
tróficas inter e intraespecíficas das espécies que coexistem em simpatria na baía do Marajó,
Sotalia guianensis, Inia spp. e Trichechus inunguis, visando compreender o uso do habitat por
estas espécies, avaliar a partição de nicho isotópico como forma de incrementar o
conhecimento sobre os mamíferos aquáticos na costa Amazônica.
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2. OBJETIVOS
2.1. Geral
Produzir conhecimento sobre a diversidade e relações tróficas dos mamíferos aquáticos na costa Amazônica, região Norte e no Delta do Parnaíba, Nordeste do Brasil.
2.2. Específicos
Descrever os novos registros de cetáceos para a costa dos estados do Pará, Maranhão e Piauí e a similaridade dessa fauna com aquela da região do sul do Caribe;
Investigar o uso do habitat e as relações tróficas entre espécies de mamíferos aquáticos de água doce e marinha na costa norte e nordeste do Brasil;
Avaliar a partição de nicho isotópico entre as espécies mais representativas (Sotalia guianensis, Inia spp. e Trichechus inunguis) da fauna de mamíferos aquáticos do estuário amazônico;
Caracterizar os nichos isotópicos para dois estoques populacionais do boto-cinza (Sotalia guianensis) no estuário amazônico e Delta do rio Parnaíba.
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3. MATERIAL E MÉTODOS
3.1. Área de Estudo
As amostras analisadas neste estudo foram obtidas de exemplares de mamíferos
aquáticos encalhados em três setores: 1) ambientes de várzea da Amazônia Oriental; 2)
estuário amazônico e zona costeira adjacente no litoral do Pará, na região Norte; e 3) litoral
dos estados do Maranhão e Piauí, na região que compreende o Delta do Parnaíba, nordeste
do Brasil (Fig. 1).
O setor denominado de “Amazon lowland” (AL) compreende áreas de planície
alagada denominadas de várzea. O rio Amazonas é caracterizado por águas de aspecto
turvo, ricas em nutrientes devido às grandes quantidades de sedimentos que são carreados
desde os Andes, fazendo com que sejam conhecidas como água branca (SIOLI, 1991). As
várzeas sustentam abundantes florestas nas partes altas e extensos bancos de gramíneas
nas partes mais baixas, enquanto nos cursos d’água prevalecem bancos de vegetação
flutuante e macrófitas (JUNK et al., 2011).
O estuário do rio Amazonas (AE) é formado principalmente pela descarga do rio
Amazonas no Oceano Atlântico através de dois grandes canais, Canal Norte e Canal Sul
(GEYER et al., 1996) (ver Fig. 1). Este é um estuário extremamente dinâmico influenciado por
macromarés semidiurnas, ventos alísios vindos do leste, além da enorme descarga de água
doce oriunda do rio Amazonas (NITTROUER; DEMASTER, 1996). A região é
permanentemente afetada pela interface rio-mar e por fatores como uma marcada estação
chuvosa. Além do desague do Amazonas, nesta região também desagua o sistema Araguaia-
Tocantins e rios menores (GOULDING; BARTHEM; FERREIRA, 2003; SOUZA-FILHO et al.,
2009).
O setor AE abrangeu o estuário do Amazonas e zonas costeiras como o norte e leste
da Ilha de Marajó e a costa nordeste do Estado do Pará. Na costa leste da ilha encontra-se a
baía do Marajó formada pelas descargas dos rios Pará e Tocantins, e pela baía de Guajará.
Esta baía recebe intrusão salina superficial no período de baixa descarga dos rios (BEZERRA;
ROLLNIC, 2011), e é submetida a regimes de macromarés. Nesta baía, coexistem em
simpatria as duas espécies de peixes-boi, T. inunguis e T. manatus, além de quatro cetáceos,
Inia spp. (I. geoffrensis e I. araguaiaensis), S. guianensis e S. fluviatilis (DOMNING, 1981;
CUNHA et al., 2010; SICILIANO et al., 2007, 2008, 2015 dados não publicados), esta última
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não incluída no presente estudo. No nordeste do Pará, as baías de Marapanim e Maracanã
foram as regiões mais monitoradas. No estuário do rio Marapanim ocorre a maior
concentração de S. guianensis registrada para a costa do Pará (EMIN-LIMA et al., 2010a).
O terceiro setor, na costa Nordeste (NC), compreendeu principalmente o extremo
leste do Maranhão e o litoral do Piauí. A mais importante descarga de água doce nesta
região vem do rio Parnaíba, segundo maior sistema fluvial brasileiro, atrás apenas do rio
Amazonas (SZCZYGIELSKI et al., 2014). O Parnaíba, ao encontrar o Oceano Atlântico, forma
um delta com cinco baías que sofrem grande influência das marés, quais sejam: Tutóia, Caju,
Melancieiras, Canárias e Igaraçu, que unidas formam o Delta do Parnaíba (MOREIRA;
MAVIGNER, 2007). Este ambiente, que é submetido a um regime de mesomarés
semidiurnas, contém campos de dunas costeiras e vegetadas, largas praias e uma vasta área
de florestas de mangue. De agosto a dezembro existe uma diminuição na descarga do rio
que faz com que prevaleçam condições de regiões semiáridas, além de uma restrita estação
chuvosa que vai de dezembro a abril.
Figura 1. Área de estudo representando os três setores amostrados ao longo da costa Amazônica englobando o litoral do Pará e parte do Maranhão e o Delta do Parnaíba no nordeste do Brasil (1). Detalhe dos setores: (2) Amazônia oriental, áreas de várzea (AL), (3) estuário amazônico (indicação do Canal Norte e Sul) e áreas costeiras adjacentes (AE) e (4) costa nordeste, evidenciando o litoral dos estados do Maranhão e Piauí (NC).
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Figura 1. Setor 1 – Mapa do setor 1 evidenciando grandes rios da bacia do rio Amazonas (Trombetas, Tapajós e Xingu). Círculos pretos são locais de coleta dos exemplares de mamíferos aquáticos. Ambientes de várzea mostrando vegetação típica deste habitat na baía dos Botos, município de Portel (PA).
Figure 4. Setor 3 – Mapa do setor 3 mostrando algumas das baías que formam o Delta do Parnaíba no extremo leste do Maranhão e oeste do Piauí. Campos de dunas e manguezal na baía do Caju, município de Araioses (MA).
Figura 2. Setor 2 – Mapa do setor 2 evidenciando a costa nordeste do Pará e oeste do Maranhão. As baías mais representativas deste setor para este estudo estão nomeadas, Marajó, Marapanim e Maracanã. Praia da costa leste da ilha de Marajó (Barra Velha), município de Soure (PA).
(b)
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3.2. Coleta de amostras
3.2.1. Registros de encalhes
As amostras foram obtidas por meio de monitoramentos sistemáticos das praias dos
setores de estudo, por meio do atendimento a chamados de encalhe ou esporadicamente de
exemplares obtidos de capturas acidentais em artefatos de pesca, no caso de S. guianensis
(Fig. 5). As carcaças foram recolhidas em qualquer estágio de decomposição, seguindo os
protocolos de Geraci & Lounsbury (1993). Quando possível foi realizada biometria e
sexagem, informações como local, data e material coletado foram anotadas em caderno de
campo. Ao término das campanhas, todo o material foi transportado para o Museu Paraense
Emílio Goeldi (MPEG), onde o material ósseo foi preparado para tombamento a seco na
Coleção de Mamíferos.
A biometria externa foi tomada sempre que possível, seguindo os padrões estabelecidos por
Norris (1961). Dependendo do estado de decomposição da carcaça foram coletadas
amostras de pele, músculo, gordura e órgãos internos, inclusive estômagos, além de todo o
material ósseo disponível. As carcaças foram identificadas em campo de acordo com
características específicas como coloração, formato da cabeça, número de dentes. Para o
caso específico do gênero Inia, análises moleculares foram necessárias para identificação de
alguns exemplares a nível molecular.
Na costa do Pará, a costa leste da ilha de Marajó foi monitorada regularmente desde
2005 até 2014, englobando aproximadamente 60 km de praias percorridas nos municípios
de Soure e Salvaterra (0o37'10.0"S, 48°28'54.6"W/ 0o56’26.19”S, 48o34’17.25”W).
Expedições pontuais à porção norte da ilha, conhecida como contra costa, foram realizadas
em 2012 e 2013 (00o15’9.97”S, 48o43’5.09”W). No nordeste do estado, praias dos
municípios de Maracanã (0o35’48.29”S, 47o32’50.50”W) e Marapanim (0o35’47.83”S,
47o38’11.66”W) foram monitoradas regularmente, enquanto praias do município de
Bragança (0°49'41''S, 46°36'16''W), por exemplo, foram atendidas de acordo com os
chamados aos atendimentos de encalhe.
Na região do Delta do Parnaíba, os eventos de encalhe foram regularmente
monitorados entre 2008 e 2011, com coletas esporádicas após este período. As praias foram
percorridas por veículos tracionados ou, alternativamente, a pé, perfazendo em torno de
100 km percorridos nos municípios de Paulino Neves (2°40'28.15"S, 42°34'42.71"W), Tutóia
32
(2°45'10.97"S, 42°18'29.96"W) e Araioses (2°42'54.53"S, 42°0'49.27"W), no Maranhão e Luís
Correia (2°54'10.44"S, 41°33'57.53"W) e Parnaíba (2°47'57.58"S, 41°44'55.11"W), no Piauí.
Para elaboração do Capítulo II desta tese foram utilizadas adicionalmente amostras
de exemplares de T. inunguis e I. geoffrensis coletados no rio Amazonas e em alguns de seus
tributários (rio Ayaya, 2°34'30"S, 54°21'50"W; rio Trombetas, 1°38'44"S, 55°58'38"W; baixo
rio Xingu, 2o41’16”S, 52o00’45”W) e próximo à capital, Belém, na baía de Guajará (1°17'19"S,
48°29'5"W). Este material foi coletado por técnicos e pesquisadores do MPEG entre as
décadas de 1910 e 1980, reforçando a importância do tombamento histórico de vertebrados
na coleção do MPEG.
O recolhimento das carcaças foi autorizado por meio de licenças do Sistema de
Autorização e Informação em Biodiversidade – SISBIO. Licenças sob Nos 26520-1, 19605,
24431,30327-1 para região norte e Nos 38653, 25523 para o nordeste.
33
3.2.2. Isótopos estáveis
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CAPÍTULO I
STRANDING SURVEY AS A FRAMEWORK TO INVESTIGATE RARE CETACEAN RECORDS OF THE NORTH AND NORTH-EASTERN BRAZILIAN COASTS
Artigo elaborado e formatado para publicação no periódico Journal of the Marine Biological Association of the United Kingdom para o Special Issue Cetaceans. O artigo foi resubmetido em 01/12/2015 após revisão pelos autores e aguarda parecer final para publicação.
54
RUNNING HEAD – Cetacean records from Northern and North-eastern Brazilian coast
Stranding survey as a framework to investigate rare cetacean records of the North and North-
eastern Brazilian coasts
ALEXANDRA F. COSTA1,3
, SALVATORE SICILIANO1,2
, RENATA EMIN-LIMA1, BRUNA M.L.
MARTINS1,4
, MAURA E.M. SOUSA1,5
, TOMMASO GIARRIZZO3,6
AND JOSÉ DE SOUSA E
SILVA JÚNIOR1
1Museu Paraense Emílio Goeldi, Coordenação de Zoologia, Setor de Mastozoologia, Grupo de
Estudos de Mamíferos Aquáticos da Amazônia (GEMAM), Av. Perimetral, 1901, Terra Firme, 66077-
530 Belém, PA, Brazil
2Instituto Oswaldo Cruz/FIOCRUZ, Pavilhão Mourisco – sala 122, Av. Brasil, 4365 - Manguinhos,
21040-360, Rio de Janeiro, RJ Brazil
3PPG em Ecologia Aquática e Pesca, Universidade Federal do Pará-UFPA, Instituto de Ciências
Biológicas, Cidade Universitária José da Silveira Netto, Av. Augusto Corrêa n° 1, Guamá, 66075-110,
Belém, PA, Brazil
4PPG em Ecologia e Conservação da Biodiversidade, Universidade Estadual de Santa Cruz–UESC.
Rodovia Jorge Amado, km 16–Pav. Maz de Menezes, 1º andar, sala 1DA, Salobrinho, 45662-900
Ilhéus, BA, Brazil
5PPG em Biologia Ambiental, Universidade Federal do Pará–UFPA, Campus de Bragança. Alameda
Leandro Ribeiro s/n, Aldeia, 68600-000 Bragança, PA, Brazil
6Laboratório de Biologia Pesqueira e Manejo dos Recursos Aquáticos, Universidade Federal do Pará-
UFPA, Av. Perimetral, 2651 Terra Firme, 66077-830 Belém, PA, Brazil
ABSTRACT
Marine mammal stranding events are used as an important tool for understanding cetacean biology
worldwide. Nonetheless, there are vast gaps of knowledge to be filled in for a wide range of species.
Reputable information is required regarding species from large baleen whales to sperm and beaked
whales, as well as pelagic dolphins. This paper describes new cetacean records from North and
North-eastern Brazil, which are both the least surveyed areas regarding aquatic mammals. Regular
beach surveys were conducted to recover cetacean carcasses along the coast of Pará beginning
November 2005, covering approximately 88 km of the state’s coast. At the coasts of the Maranhão and
Piauí states, the surveys were conducted between 2008 and 2013. From 2003 to 2014, 34 strandings
of cetaceans were registered. The study provides four additional species records’ in the area based on
strandings (Balaenoptera borealis, Balaenoptera physalus, Peponocephala electra and Pseudorca
crassidens). A mass stranding of Guiana dolphins (Sotalia guianensis, N= 12), the most common
species for the region, was reported for the first time. The records presented herein are of special
concern, since they expand the knowledge on cetaceans from the Brazilian coast. In addition, this
study conducted an analysis to verify the similarity between cetacean compositions described for
55
North and North-eastern Brazil and the southern Caribbean region. The results showed a high
similarity between these regions, proving the connection with the Caribbean cetacean fauna.
Table 1. Records of cetaceans stranded from 2003 to 2014 on the Northern Brazilian coast (N= 34; 15 species). TL (total length in meters),
NI (not identified). The study area was divided in three sampling sectors: (1) Marajó bay (MB), (2) Eastern Pará state (EP) and (3)
Maranhão/Piauí coastline (MA/PI). Live stranding (LS) and Carcass (CA).
Species by Family Category TL (m) Sex Sector Location Date Voucher
specimen
Balaenopteridae
Balaenoptera borealis LS 10.32 F EP (2) Viseu 13/09/2008 MPEG 39691
Balaenoptera brydei CA 4.20 NI MB (1) Salvaterra 15/09/2012 MPEG 42154
Balaenoptera physalus LS 14.90 M EP (2) São João de
Pirabas 21/01/2010 MPEG 39690
Megaptera novaeangliae CA 16.7 F MA/PI (3) Pedra do Sal 15/01/2003 -
CA - NI MA/PI (3) Luís Correia 2005 -
CA ~10.00 M EP (2) Quatipuru 08/10/2008 MPEG 39692
CA 13.00 NI MA/PI (3) Tutóia 22/05/2009 MPEG 42184
Physeteridae
Physeter macrocephalus CA 11.80 F MA/PI (3) Pedra do Sal 02/02/2010 MPEG 42088
CA - F MA/PI (3) Paulino
Neves 14/05/2010 MPEG 42173
LS 10.50 F EP (2) Marapanim 07/04/2014 MPEG 42166
CA 4.22 NI MB (1) Soure 07/08/2014 -
Delphinidae
Delphinus sp. CA 2.06 NI MA/PI (3) Pedra do Sal 12/08/2011 MPEG 42095
Globicephala
macrorhynchus CA - NI MA/PI (3)
Paulino
Neves 2009 -
CA - NI MA/PI (3) Pedra do Sal 15/01/2009 MPEG 42128
Grampus griseus CA - NI MA/PI (3) Pedra do Sal 13/04/2011 MPEG 42130
Lagenodelphis hosei LS - M MA/PI (3) Araioses 03/04/2009 MPEG 42080
Peponocephala electra CA - NI MA/PI (3) Araioses 2007 MPEG 42067
CA - NI MA/PI (3) Araioses 19/06/2008 MPEG 42069
Pseudorca crassidens CA 3.30 NI EP (2) Marapanim 20/04/2012 MPEG 42132
Sotalia guianensis LS - NI EP (2) Salinópolis 31/01/2013 -
Stenella attenuata CA - NI MA/PI (3) Araioses 14/03/2009 MPEG 42077
CA 1.59 M MA/PI (3) Pedra do Sal 10/12/2009 MPEG 42085
Steno bredanensis CA - NI EP (2) Maracanã 19/04/2009 MPEG 39635
CA - NI MA/PI (3) Pedra do Sal 15/08/2011 MPEG 42096
CA - NI EP (2) Marapanim 20/11/2011 MPEG 42066
CA - NI EP (2) Marapanim 20/11/2011 MPEG 42102
CA 2.68 M EP (2) Bragança 04/04/2012 MPEG 42131
CA - NI MA/PI (3) Pedra do Sal 23/08/2013 MPEG 42176
Tursiops truncatus
CA - NI MA/PI (3) Araioses 24/04/2009 MPEG 42129
CA - NI MA/PI (3) 26/07/2009 MPEG 42081
CA - NI MA/PI (3) Apicum-Açu 05/03/2010 -
CA - NI EP (2) Maracanã 12/03/2010 MPEG 39612
CA 3.17 M EP (2) Maracanã 13/02/2013 MPEG 42174
CA 2.87 F EP (2) Marapanim 04/03/2013 MPEG 42175
69 Fig. 2. Sei whale Balaenoptera borealis stranded at Fernandes Belo (01o10’59.16”S, 46o5’48.52”W), Viseu municipality, near the border between
the Pará and Maranhão states. The particular coloration of the baleen plates and slightly arched head are diagnostic characters to identify the
species (photos by DEMA/PA and Jairo Moura).
70
Fig. 3. Fin whale Balaenoptera physalus stranded at the São João de Pirabas municipality (00o45’31.29”S, 47o4’26.41’W), Eastern coast of the
Pará state. Note the good condition of the carcass and a strange swelling on the top of the head (photo by GEMAM/MPEG).
71
Fig. 4. Diagram of cetaceans reported from the North-eastern (inverted triangle) and North coast of Brazil (triangle) and southern Caribbean
(square), resulting from a cluster analysis of cetacean stranding and sighting records reported in seven articles and the present study. Arrows indicate the two distinct groups formed (Group 1 and 2). A similarity profile (SIMPROF) permutation test highlights dashed clusters that show
significant internal structure. Shaded cells indicate occurrence of species.
72
CAPÍTULO II
RESOURCE PARTITIONING AMONG AQUATIC MAMMALS FROM AMAZON AND
NORTHEASTERN COAST OF BRAZIL REVEAL THROUGH THE ANALYSIS OF STABLE ISOTOPES OF
CARBON AND NITROGEN
ALEXANDRA F. COSTA1,2, SILVINA BOTTA3, SALVATORE SICILIANO1,4, SETH NEWSOME5, TOMMASO GIARRIZZO2,6
1Museu Paraense Emílio Goeldi, Coordenação de Zoologia, Setor de Mastozoologia, Grupo de Estudos de Mamíferos Aquáticos da Amazônia (GEMAM), Av. Perimetral, 1901, Terra Firme, 66077-530 Belém, PA, Brazil. Programa de Capacitação Institucional, Museu Paraense Emílio Goeldi, Coordenação de Botânica. Av. Perimetral, Terra Firme, CEP 66077-830, Belém, PA, Brazil.
2PPG em Ecologia Aquática e Pesca, Universidade Federal do Pará-UFPA, Instituto de Ciências Biológicas, Cidade Universitária José da Silveira Netto, Av. Augusto Corrêa n° 1, Guamá, 66075-110, Belém, PA, Brazil
3Laboratório de Ecologia e Conservação da Megafauna Marinha − EcoMega, Instituto de Oceanografia, Universidade Federal do Rio Grande, Rio Grande RS 96203-900, Brazil
4Instituto Oswaldo Cruz/FIOCRUZ, Pavilhão Mourisco – sala 122, Av. Brasil, 4365 - Manguinhos, 21040-360, Rio de Janeiro, RJ Brazil
5Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA
6Laboratório de Biologia Pesqueira e Manejo dos Recursos Aquáticos, Universidade Federal do Pará-UFPA, Av. Perimetral, 2651 Terra Firme, 66077-830 Belém, PA, Brazil
Corresponding author: [email protected] Artigo elaborado para publicação no periódico MARINE MAMMAL SCIENCE. Esta versão está em processo de revisão pelo co-autor Seth Newsome aguardando para breve submissão.
73
ABSTRACT
Different methodologies have been used to establish the ecological and biological parameters of
marine mammals. In the last decades the use of stable isotope analysis (SIA) has become a
powerful tool for understanding some aspects of aquatic mammals ecology and useful in
studying ecology, habitat use, migration, population connectivity as well as for investigating
niche parameters and trophic relationships. Variation in isotopic composition, particularly in
hard tissues, helps to elucidated isotopic niche of species providing a long-term response that
can be linked directly to geographical regions. Although trophic ecology of aquatic mammals
using SIA were carried out in the Southeastern and Southern Brazilian coast, there are few
studies in the Northeastern and none for Northern coast. This paper describes the habitat use
and trophic relationships among freshwater and marine mammal species, evaluate isotopic
niche partitioning among the most representative species (Sotalia guianensis, Inia spp. and
Trichechus inunguis) within the Amazon Estuary and characterize differences in isotopic niches
between ecological stocks of Guiana dolphin (S. guianensis). In this study, we analyzed stable
isotopes of carbon and nitrogen in bone-collagen of 14 species of cetaceans and one of sirenia.
Samples were obtained from stranded carcasses or from incidental catches collected from the
Amazon coastal zone (AE), Amazon lowland (AL) and Parnaíba River Delta (NC). We detected
interspecific variations for both isotopes. Among freshwater species a wide range, while marine
species exhibited narrow-range values. Among marine species were observed a coastal-oceanic
spatial pattern showing more 13C enriched values in the coastal species, excepted for S.
guianensis, while oceanic species showed depleted carbon values. Guiana dolphin stocks,
Sgui_NC and Sgui_AE, showed similar values of 15N, however NC group, showed enriched
values of 13C. There is no overlap among the most representative species of the study area,
showing no niche overlap and indicating strong isotopic niche segregation at least in Marajó
bay. The largest isotopic niche overlap (63.1%) occurred among populations of S. guianensis
from AE and NC. Average values of carbon and nitrogen showed no significant differences
between Amazon river dolphin and Araguaia boto, I. geoffrensis and I. araguaiaensis,
respectively. Trophic relationships among aquatic mammals were not previously investigated in
the study area. Furthermore, carbon and nitrogen stable isotope compositions in tissues of
Northern Brazilian cetaceans are reported for the first time.
74
RESOURCE PARTITIONING AMONG AQUATIC MAMMALS FROM AMAZON AND
NORTHEASTERN COAST OF BRAZIL REVEAL THROUGH THE ANALYSIS OF STABLE ISOTOPES OF
CARBON AND NITROGEN
1. INTRODUCTION
Multiple tools have been used to understand ecological and biological aspects and provide
information of the population structure on distinct timescales. Worldwide, the conservation of
marine mammals is focused on the knowledge of the population structure, whether on an
individual level or at community level (NEWSOME et al., 2007, 2012). Aspects of foraging
strategies, relative trophic positions and resource partitioning of top predators are prerequisite
if the intention is to design strategies of management and conservation of species (PAULY et al.,
2002; RYAN et al., 2013).
Diversity of species that coexist in a community is determinate by the way they share the
available resources. In order to avoid competitive exclusion between species, they must differ in
some ecological aspects such as spatial and temporal segregation of resources and habitats
(HUTCHINSON, 1957; PIANKA, 1974). Dealing with conspecifics, the competition could be strong
and reflect in intrapopulation variance. This variation on resource use (i.e. diet, habitat and
geographical location) must greatly change the ecology of populations and have ecological,
evolutionary and conservational consequences (BOLNICK et al., 2003; VANDER ZANDEN et al.,
2010). Intraspecific and interspecific competition will occur if the available resources have
limited supplies, affecting directly on niche parameters (ROUGHGARDEN, 1972; BEARHOP et al.,
2004). Definitions of niche has undergone changes over time, but even the most current,
postulate that the niche is an n-dimensional space that can be represented by the bi-plot 13C
versus 15N. These axis provide information about species niche showing data about diet
consumption (13C) and species habitat (15N) (NEWSOME et al., 2007).
Analysis of stomach contents was the most traditional method to understand feeding habits of
aquatic mammals and is the most direct way to access diversity of diet resources (TRITES, 2001).
Although, it presents many biases in their interpretation, since only provide a snapshot of diet
consumed in a small timescale and not prey assimilation by organisms over time (HOBSON,
1999).
75
In the last decades the use of stable isotopes analysis has become the most common
biochemical markers used to trace animal movements and to quantify what individuals
assimilate (see NEWSOME et al., 2010). The isotopic variation in animal’s tissues may determine
the isotopic niche of species (i.e. via consumption and tissue synthesis) and is appropriate to
calculate niche width (BEARHOP et al., 2004; NEWSOME et al., 2007). Intra- and inter-individual
variation in isotopic composition helps to elucidated isotopic niche of species providing a time-
integrated response that can be linked directly to geographical regions (RUBENSTEIN; HOBSON,
2004; MICHENER; KAUFMAN, 2007).
The isotope signature (i.e. the isotopic composition) of an organism is determined by the diet
(food resources) and habitat (local where it lives). Variations in isotopic signatures of habitats
are due to biogeochemical processes and pass through higher levels of the food webs (DENIRO;
EPSTEIN, 1978).
In other words, isotopic values of consumers reflect their relative trophic position (nitrogen
isotope, MINAGAWA; WADA, 1984; POST, 2002) and their foraging main habitats and baseline
producers (carbon isotope, DE NIRO, 1978). Isotopic variation on carbon values of consumers
reflect spatial and temporal shifts among food webs and this spatial variability is directly related
to differences of habitat use, i.e. foraging habitats (neritic vs. oceanic, inshore vs. offshore,
marine vs freshwater) (CLEMENTZ; KOCH, 2001).
Stable isotope analysis (SIA) is a powerful tool to understand aspects of aquatic mammals
ecology and useful in studies on foraging ecology, habitat use, migration, population
connectivity as well as for investigating niche parameters and trophic relationships (BEARHOP et
al., 2004; NEWSOME et al., 2010; LAYMAN et al., 2011). Main approaches clarify aspects of
migration patterns (MENDES et al., 2007; WITTEVEEN et al., 2009), resource partitioning (RYAN
et al., 2013; BROWNING et al., 2014; GAVRILCHUK et al., 2014), ontogenetic shifts in diet
(NEWSOME et al., 2009), differences on foraging habitats (PINELA et al., 2010; RICCIALDELLI et
al., 2010), ecological differences among populations (FOOTE et al., 2009; BISI et al., 2013; VIGHI
et al., 2014) and trophic relationships with trace elements (DAS et al., 2003; CAPELLI et al.,
2008).
Marine mammals, considered the top predators in marine ecosystems, occur in sympatry along
their habitat areas (e.g. Delphinids, Pinnipeds) and share common habitat use (TRITES, 2001;
76
HÜCKSTÄDT et al., 2012), many times having similar feeding habits and foraging strategies
(BEARZI, 2005).
Several species that occur off Northern and Northeastern Brazil undergo serious threats to their
survival and require outlined strategies for their management and conservation (BARRETO et
al., 2010). An important step to reverse the information gap is to understand the dynamics of
the trophic relationships among these communities of aquatic mammals and their habitats.
Four species of cetacean and two of sirenia probably coexist in sympatry in Pará River Estuary
(DOMNING, 1981; SICILIANO et al., 2007 CUNHA et al., 2010), commonly referred to Marajó
Bay. Cetaceans belong to distinct families Delphinidae (Sotalia guianensis, Guiana dolphin and
Sotalia fluviatilis, tucuxi), Iniidae (Inia geoffrensis, Amazon river dolphin and Inia araguaiaensis,
Araguaian boto) and the manatees belong to Trichechidae (Trichechus manatus, Antillean
manatee and Trichechus inunguis, Amazonian manatee). Despite the surveys in this region,
questions on habitat use and confirmation of sympatry between S. guianensis and S. fluviatilis
remains unknown in this region. Recently, through stranding events, was confirmed the
presence of two species of river dolphins in the northern portion of Marajo Island and Eastern
Pará coast (COSTA et al., 2013; SICILIANO et al., 2015 unpub. data), I. geoffrensis and I.
araguaiaensis, the later recently described (HRBEK et al., 2014). In this peculiar region, Sotalia
and Trichechus comprise species with marine and fluvial habits. Previous studies, are trying to
elucidate questions on feeding habits of Guiana dolphin (VIEIRA, 2014) and availability of
potential food resources for manatees (SOUSA, 2011; SOUSA et al., 2014).
However, it is still unknown the strong influence of large estuaries like the Amazon and Pará
rivers and regions with lower freshwater input and strong marine influence such as Parnaíba
Delta on the distribution and availability of preys. The influence of Amazon River discharge on
Northern coast determine the establishment of fish assemblages (Camargo & Isaac, 2002), thus
directly affecting the trophic ecology of aquatic mammal’s species.
On the coast of Brazil, most studies used the traditional analysis of stomach contents to
evaluate feeding ecology of marine mammals (ANDRADE et al., 2001; SANTOS et al., 2002;
GURJÃO et al., 2003). The main studies about trophic ecology of aquatic mammals using SIA
were carried out in the Southeastern and Southern (DI BENEDITTO et al., 2011, 2013; BOTTA et
77
al., 2012; ZENTENO et al., 2013; VIGHI et al., 2014; DRAGO et al., 2015), very few in the
Northeastern (CIOTTI et al., 2014) and none for Northern coast.
Different tissues are used in SIA according to the timescale and ecological questions that need
to be answered (BEARHOP et al., 2004). Thus, tissues with quick turnover, such as blood, skin or
muscle, are used to obtain information about recent diet, last weeks or months (HOBSON; et al.,
1993), while hard tissues, due to the fact that incorporate the isotope signatures very slowly are
used for feeding ecology over species lifetimes (HOBSON; CLARK, 1992; NEWSOME et al., 2007;
NEWSOME et al., 2010). Inert tissues (e.g. tooth dentin and enamel, bones, baleen plates,
vibrissae) has been widely used to clarify aspects of marine mammals trophic ecology (WALKER;
MACKO, 1999; RICCIALDELLI et al., 2010; BENTALEB et al., 2011; VIGHI et al., 2014). In this study,
we analyzed stable isotopes of carbon and nitrogen in bone-collagen of aquatic mammals
comprise species strictly oceanic (e.g. Physeter macrocephalus), coastal/marine (e.g. Tursiops
truncatus, Steno bredanensis), coastal/estuarine (S. guianensis) to exclusively freshwater (I.
geoffrensis, I. araguaiaensis, T. inunguis).
Based on a previous study, Guiana dolphin was separated in six Management Units (MUs,
(CUNHA et al., 2010), so we assumed that: i) isotope composition could provide evidences of
population structure between distinct ecological stocks of S. guianensis, ii) this species probably
present isotopic niche variation comparing different ecological stocks; and iii) individuals inhabit
the Amazon Estuary would present a wider trophic niche than their conspecific inhabiting the
Northeastern coast of Brazil.
Our main goals were to: (1) investigate the habitat use and trophic relationships among
freshwater and marine aquatic mammal species, (2) evaluate isotopic niche partitioning among
the most representative species (Sotalia guianensis, Inia spp. and Trichechus inunguis) within
the Amazon Estuary and (3) characterize differences in isotopic niches between ecological
stocks of Guiana dolphin (S. guianensis).
78
2. MATERIAL AND METHODS
Study sites
Samples used in this study were obtained from beach surveys conducted along three main
sectors: 1) Amazon lowland (AL); 2) Amazon Estuary and adjacent coastal zone (AE) and, 3)
Northeastern coast of Brazil (NC) (Fig. 1).
The Northern Brazilian coast extends from Cabo Orange, the most extremely point near French
Guiana border (4oN, 51oW) up to Ponta do Tubarão (2oS, 43oW), the westernmost portion of São
José Bay, Maranhão state. Its coastline is submitted to different freshwater inputs, principally
the huge discharge of the Amazon River (GOULDING et al., 2003; SOUZA-FILHO et al., 2009).
The sector designated as Amazon lowland (AL) comprises the floodplain habitat named várzea.
In this region there are records of the tucuxi, Sotalia fluviatilis (FLORES; DA SILVA, 2009), the
Amazonian manatee, Trichechus inunguis (see DOMNING, 1981), the Amazon river dolphin, Inia
geoffrensis (BEST; DA SILVA, 1993). Stranded specimens were collected in rivers around
Santarém municipality, Ayaya River (2°34'30"S, 54°21'50"W), a small Amazon River tributary; at
Oriximiná, Trombetas River (1°38'44"S, 55°58'38"W); at Vitória do Xingu, lower Xingu river
(2o41’16”S, 52o00’45”W); and near Belém, Guajará Bay (1°17'19"S, 48°29'5"W). Amazon rivers
are classified according to its color water in physical and chemical characteristics. Amazon River
is characterized by a rich-nutrient water with muddy aspect due to the high amounts of
sediment that carry from Andes, known as white water (SIOLI, 1991). Whitewater floodplains
support a luxurious forest on higher grounds and extensive grasslands at lower areas, whilst in
the water extensive banks of free floating and floating-leaved macrophytes prevail (MCGRATH,
1993; JUNK et al., 2011). Clearwater rivers, such as Xingu and Trombetas, has nutrient-poor
waters with high transparency and a characteristic greenish color. In this system aquatic
macrophytes and herbaceous plants are less abundant. Tides affects low courses of rivers
reaching more than 100 km upriver, and in part is due to the flat relief of the coastal zone (JUNK
et al., 2011).
The Amazon Estuary is formed mainly by the discharge of Amazon River into the Atlantic Ocean
through the North and South channels (GEYER et al., 1996). This is a highly dynamic estuary
affected by river-ocean interface, influenced by semidiurnal macro-tides, easterly trade winds, a
marked rainfall season and the enormous discharge of freshwater come from the Amazon River,
79
the Araguaia-Tocantins system and smaller coastal rivers (NITTROUER; DEMASTER, 1996;
GOULDING et al., 2003; ROSÁRIO et al., 2009; SOUZA-FILHO et al., 2009).
In this study the sector designated as Amazon Estuary and adjacent coastal zone (AE) comprises
the Northern and Eastern coast of Marajó Island (i.e. Marajó Bay), as well as the Eastern coast of
Pará state. Marajó Bay is formed mainly by the discharges of Pará and Tocantins rivers and
Guajará Bay. This bay receives a superficial saline intrusion during low discharge of rivers
(BEZERRA; ROLLNIC, 2011) and undergoes a macrotidal regime, with maximum tides around 4 m
on both sides of the bay (ROSÁRIO; SANTOS, 2014). In this sector, the manatees Trichechus
inunguis and T. manatus, S. guianensis, S. fluviatilis, Inia geoffrensis and I. araguaiaensis occur in
sympatry (DOMNING, 1981; DA SILVA, 1983; CUNHA et al., 2010; SICILIANO et al., 2007, 2015
unpub. data). At eastern Pará coast, Marapanim River Estuary is a very important ecosystem
which is the most studied population of Guiana dolphin (S. guianensis) occur (EMIN-LIMA et al.,
2010a).
The NC region encompasses the coastline of Maranhão and Piauí states considered a semiarid
region of Northeastern Brazil. The most important freshwater input in this region is the Parnaíba
River considered the largest river system amongst São Francisco in the Northeastern and
Amazonas River in the Northern (SZCZYGIELSKI et al., 2014). The discharge of Parnaíba River into
the Atlantic Ocean forms a delta with five bays tidally influenced: Tutóia, Caju, Melancieiras,
Canárias and Igaraçu that forms the Parnaíba Delta (MOREIRA; MAVIGNER, 2007). The region
comprises a mesotidal coast, with tides range from 1.1 m to 3.3 m (SZCZYGIELSKI et al., 2014).
The region contains coastal and vegetated dune fields, beaches with up to 200 m wide and vast
areas of mangrove forests. From August to December there is a decrease in river discharge
prevailing semiarid conditions and restricted rainfall seasonality goes from December to April.
Surveys from 2008 to 2011 registered strandings of a large diversity of cetaceans since small
dolphins to large whales. The most representative species in this sector is S. guianensis. Groups
of this species have been regularly sighted in some of the Parnaíba Delta bays (pers. obs.).
80
Figure 1. Maps of the study sites representing the three sampling sectors along the Northern and Northeastern Brazil (1). Detailed maps of regions: (2) Northeastern coast, at the coast of the Maranhão (MA) and Piauí (PI) states (NC), (3) Amazon Lowland (AL), showing collection rivers and (4) Amazon Estuary and adjacent coastal zone (AE). AP (Amapá state), PA (Pará state), MA (Maranhão state), PI (Piauí state) and CE (Ceará state). Sector AE only includes the collecting area of the study and not the Northern region as a whole. Dots are collection locations.
81
Sampling material
Aquatic mammal’s sampling material were obtained from floating or stranded carcasses during
sampling surveys or from incidental catches in fishing gears (i.e. S. guianensis). Carcasses were
recovered at any stage of decomposition (GERACI; LOUNSBURY, 1993) and taken to the Museu
Paraense Emílio Goeldi (MPEG, Belém, Pará, Brazil) where their hard parts (i.e. bones and teeth)
were cleaned from outer soft tissues and stored dry at MPEG’s Mammal Collection. Surveys to
recover carcasses were conducted since 2005 to 2014 at the AE. Stranding events were regularly
carried out at NC region between 2008 and 2011, and in the last years (2012 to 2015) are
sporadic. The oldest specimens were collected by naturalists (i.e. Émil August Goeldi) and
researchers from MPEG at the Pará state (AL) in the 1910’s, 1970’s and 1980’s (e.g. Inia spp. and
T. inunguis).
We obtained bone and teeth samples from 267 aquatic mammals, representing 14 taxa and
four families: Physeteridae (Physeter macrocephalus); Delphinidae (Delphinus sp., Globicephala
13C values from freshwater primary producers. Inshore (i.e. S. bredanensis and T. truncatus)
and offshore (G. macrorhynchus, Delphinus sp., G. griseus, L. hosei, P. electra, S. attenuata)
species exhibited carbon isotope values that reflect the expected pattern of decreasing 13C
values towards more offshore habitats. P. macrocephalus presented the most depleted 13C
values of all marine species (-14.4 ± 1.9‰, range -16.6 to -12.9) and was the most 15N-enriched.
The only P. crassidens specimen analyzed presented high 13C and 15N values (Table 1; Fig. 2).
84
Table 1. Isotope values of 13
C and 15
N (in ‰) from bone samples of aquatic mammals. Specimens were collected from Northern (Amazon Lowland, AL and Amazon Estuary and adjacent coastal zone, AE) and Northeastern Brazil (coastline of Maranhão and Piauí states, NC).
N values from bone-collagen of aquatic mammals collected from the Amazon Estuary and adjacent coastal zone (AE) and Northeastern coast of Brazil (NC). Trichechus inunguis (T_inunguis), Inia spp. (Inia_spp), Sotalia guianensis, AE (Sgui_AE), S. guianensis, NC (Sgui_NC), Grampus griseus (Ggr), Physeter macrocephalus (Pma), Steno bredanensis (Sbr), Delphinus sp. (Dsp), Tursiops truncatus (Ttr), Pseudorca crassidens (Pcr), Peponocephala electra (Pel), Globicephala macrorhynchus (Gma), Lagenodelphis hosei (Lho) and Stenella attenuata (Sat).
Freshwater species inhabit both AL and AE regions and this could be reflected in the wide range
of carbon isotope values exhibited. T. inunguis and Inia spp. did not differ in their 13C values (t-
test, t = 1.58, p = 0.12) but presented significantly different 15N values (t-test, t = 14.2, p <
0.0001).
Specimens of T. inunguis from AL, exhibited great range dispersion in 13C values (-25.5 to -
15.8‰) and presented significantly differences (t-test, t = 3.38, p < 0.008), whilst those from AE
showed narrow range (-16.2 to -12.9‰) with no significant differences in carbon values (t-test, t
= 1.87, p < 0.09). T. inunguis occupied the lowest position in isospace with 15N values of 7.6 ±
1.2‰ (range 6.0 to 10.3‰).
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Among Inia spp. sampled, non-significant differences in mean 13C and 15N values were found
between I. geoffrensis and I. araguaiaensis, the last genetically identify (Table 1, Fig. 3,
Student’s t-tests, t = 1.02, p = 0.33 and t =- 0.13, p = 0.90, for 13C and 15N, respectively).
Figure 3. Bone-collagen 13
C and 15
N values for Inia genus: Inia geoffrensis (n=8), I. araguaiaensis (n=3) and Inia spp. not identified (n=9). Samples were collected along the Amazon Lowland (AL) and Amazon Estuary and adjacent coastal zone (AE), Northern and Northeastern Brazil, respectively.
Isotopic niche variation
The isotopic niches were highly distinct among the four aquatic mammals that inhabit the AE
region (T. inunguis, S. guianensis, and Inia spp.) with no overlaps in their standard ellipse areas
(SEAc). Moreover, the SEAc of the two freshwater species, T. inunguis and Inia spp., were higher
compared to S. guianensis collected from AE (Table 2, Figs. 4, 5).
Species that comprised the Delphinid group presented similar 13C and 15N values, hence the
analysis of niche space were carried out as a single group. Delphinids showed some overlap with
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S. guianensis from both regions (AE and NC), a 39.2% overlap between the former and Sgui_AE
and a 32.5% between that group and Sgui_NC (Table 2, Figs. 4, 5).
The smallest isotopic niche area was occupied for Sgui_NC followed by Sgui_AE. Populations of
S. guianensis showed an overlap of 63.1% between them (Table 2; Figs. 4, 6).
Table 2. Isotope niche width of five groups of aquatic mammals: Trichechus inunguis (T_inunguis), Inia spp. (I. geoffrensis, I. araguaiaensis), Delphinids and Sotalia guianensis (Sgui_NC and Sgui_AE). SEA represents standard ellipses area and SEAc standard ellipses adjusted for small sample sizes.
Group Sample size (n) SEA (‰2) SEAc (‰
2)
T_inunguis 11 14.6 16.2
Inia_spp 20 12.7 13.4
Delphinids 26 2.9 3.0
Sgui_AE 175 2.8 2.8
Sgui_NC 32 1.6 1.7
Figure 4. Stable isotope bi-plot (13
C versus 15
N) showing the isotope niche area of Inia_spp (n= 20, red line), T_inunguis (n= 11, ligth blue line), Sgui_AE (n=175, dark blue line), Sgui_NC (n= 32, green line) and Delphinids (n= 26, black line). Solid lines represent SEAc (standard ellipses areas) adjusted for small sample sizes, containing c. 40% of data (Jackson et al., 2011) within each group. There is no overlap among the most representative species of the study area (Sotalia guianensis, Inia spp. and Trichechus inunguis). The overlap expressed the significant isotope niche partitioning among Delphinids and populations of S. guianensis.
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Figure 5. Plots showing the variation in 13
C and 15
N values for Delphinids (n= 26), Inia_spp (n=
20), Sgui_NC (n= 32), Sgui_AE (n= 175) and T_inunguis (n= 11) from Northern and Northeastern
Brazil. Black circles (mode) represent the SEA, boxes indicate 50%, 75% and 95% credible
intervals from dark grey to light grey, respectively. Red square indicate the SEAc (SEA corrected
for small samples sizes) of Bayesian standard ellipse areas.
Figure 6. Zoom of the plots showing the variation in 13
C and 15
N values for Guiana
dolphin Sotalia guianensis from Northeastern coast (NC) and Amazon Estuary and
adjacent coastal zone (AE), respectively (Sgui_NC and Sgui_AE). Black circles represent
mode of SEA. Boxes indicate 50%, 75% and 95% credible intervals from dark grey to light
grey, respectively. Red square indicate the SEAc (SEA corrected for small samples sizes)
of Bayesian standard ellipse areas.
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4. DISCUSSION
Trophic relationships among aquatic mammals were not previously investigated in the study
area. Furthermore, carbon and nitrogen stable isotope compositions in tissues of northern and
northeastern Brazilian cetaceans are reported for the first time.
We used the carbon and nitrogen isotopic composition in bone collagen to evaluate the feeding
ecology and trophic niche width of the most representative species from the Amazon region.
Data included species considered strictly freshwater to coastal/estuarine (e.g. Inia geoffrensis, I.
araguaiaensis, Trichechus inunguis and Sotalia guianensis) providing a representative overview
of ecological aspects of aquatic mammals from Northern and Northeastern Brazil.
Aquatic mammals diversity previously reported from this region included residents and
migrating cetaceans from tropical oligotrophic waters (SICILIANO et al., 2008). Marine and
freshwater species showed the expected significant variation in carbon isotopes derived from
distinct basal 13C values characteristic of freshwater vs. marine primary producers (MICHENER;
KAUFMAN, 2007), although nitrogen isotope values, did not differ between them. Furthermore,
carbon isotope values in delphinid species (except for S. guianensis) reflected the decrease
trend toward more offshore 13C-depleted environments previously reported for several marine
areas (southwestern South Atlantic, RICCIALDELLI et al., 2010; northwest coast of Africa, PINELA
et al., 2010; Southern Brazil, BOTTA et al., 2012; Southeastern Brazil, BISI et al., 2013).
Tursiops truncatus showed 13C and 15N-enriched isotopic values consistent with a coastal
distribution and a high trophic level. Indeed, the species is considered to have a coastal habit in
other areas of occurrence as well as offshore ecotypes were described in some regions
(BASTIDA et al., 2007; PERRIN et al., 2011). Along the Southern Brazilian coast, the species is
usually associated to estuaries with resident populations inhabiting those areas (FRUET et al.,
2011, 2014). Recently, Costa et al. (2015) reveals a new population structure of three distinct
groups determined by genetic analysis for T. truncatus in Southern Brazil. Group 1 consists of
individuals living with high fidelity site, group 2 was composed for one individual previously
photo-identified and group 3 formed for dolphins stranded near the Tramandaí Lagoon but
without origin that forms part of an offshore community. In Northern, however, the diet and
habitat use of this species is poorly known, with some stranding events in
Northern/Northeastern, at the coast of Maranhão state (COSTA; EMIN-LIMA, 2010) and
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Northern (SICILIANO et al., 2008). In Northeastern, Alves-Junior et al. (1996) reported the
presence of T. truncatus in coastal waters of Ceará state.
The only specimen of P. crassidens analyzed also presented high isotopic values of carbon and
nitrogen, which could reflect a mainly coastal foraging area for this species. However, this
cetacean is considered primarily oceanic, foraging cephalopods and fish from deep waters
(ALONSO et al., 1999; BAIRD, 2009; RICCIALDELLI; GOODALL, 2015). Nevertheless, in Southern
Brazil high carbon and nitrogen values were reported dividing specimens in isotopic groups of P.
crassidens indicating a coastal habitat and a high trophic position (BOTTA et al., 2012; PARO,
2013). Further data on stable isotopes or sighting records are needed to confirm the most
probable foraging habit for the species in Northern Brazil.
Although S. bredanensis is considered an offshore species (BASTIDA et al., 2007) in Southeastern
Brazil it is regularly sighted in shallow bays and other coastal areas (OTT; DANILEWICZ, 1996;
SICILIANO; FLACH, 2007). On Northern and Northeastern Brazil little is known about S.
bredanensis distribution patterns, but the increase in strandings and fishermen reports about
this species reinforces its regular presence in neritic waters, principally off Northern Brazil
(SICILIANO et al., 2008; MARTINS, 2015). Almost nothing is known about the distribution and
habitat use of Delphinus sp. in Northern and Northeastern Brazil (TAVARES et al., 2010). Carbon
and nitrogen isotope values for the species found in this study were similar to those in D.
delphis specimens from Southern Brazil (BOTTA et al., 2012), probably resulting from foraging
along the continental shelf (i.e. in the intermediate/inner shelf). However, the species was
considered coastal in other regions (i.e. Gulf of California, NIÑO-TORRES et al., 2006), but see
(AURIOLES-GAMBOA et al., 2013) including Southeastern Brazilian waters (TAVARES et al.,
2010).
Risso’s dolphin (G. griseus) is a theutophagous species inhabiting deep waters from tropical and
temperate oceans (BAIRD, 2009). Carbon and nitrogen values were different between
specimens. One was an immature from NC with higher values of both isotopes and the other
was a mature male from AE with signatures consistent with low trophic level on offshore
feeding grounds.
Other theutophagous species (e.g. G. macrorhynchus and P. electra) and those feeding on small
pelagic fish and squid (e.g. L. hosei and S. attenuata) presented similar values of 13C and 15N
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coinciding with their low trophic level predation in offshore areas. Alves et al. (1996) and Costa
& Emin-Lima (2010) registered G. macrorhynchus and P. electra through stranding events in
Northeastern and Erber et al. (2005) through sightings by ocean cruises in Eastern Pará. The
presence of S. attenuata was reported for Siciliano et al. (2008), further two records from Piauí
coast were reported (COSTA et al., 2015, unpub. data). Isotopic values of 13C showed a
decrease in values typical with an ocean pattern.
It is noteworthy mentioning that both records of L. hosei were based on live individuals
stranded on the coast of Maranhão ( TOSI; MAGALHÃES; GARRI, 2008; COSTA et al., 2015,
unpub. data). So far, no previous isotopic data for G. macrorhynchus and P. electra were
reported for Brazilian waters, thus values presented here are unique for these species.
Adult males, females and immature males of P. macrocephalus forage over different regions of
the oceans. The former are usually found in deep waters up to the ice-edge from both
hemispheres while females and immature males inhabit lower latitudes in subtropical and
tropical oceans (WHITEHEAD, 2009). Ruiz-Cooley et al. (2004) found significantly differences in
13C and 15N between tissues of females and immature males and those of adult males,
showing different diets and/or habitat use. Females prefer mesopelagic squids and fishes, while
males prey upon larger squids and demersal fish in Antarctic and Artic waters (WHITEHEAD,
2009). On the Northeastern Brazilian coast, Gurjão et al. (2003) identified at least 15 squid
families in stomach contents of sperm whales, belonging principally to pelagic cephalopods.
In this study two specimens that presented similar values of 13C were females while the more
13C enriched individual did not have its sex confirmed. All P. macrocephalus samples showed the
most 15N-enriched values than all other taxa, suggesting higher trophic level than the other
marine species analyzed (see TRITES, 2001). Low carbon values indicate more offshore foraging
areas as expected for the known foraging ecology of the species (RUIZ-COOLEY et al., 2012). Our
values were similar to those found for P. macrocephalus from the Mauritania coast, Northwest
coast of Africa (PINELA et al., 2010) and for Northwestern Spain (BORRELL et al., 2013).
Niche partitioning of aquatic mammals in the Amazon Estuary
Usually species have sufficient differences in their ecological niches (e.g. diet, habitats
preferences) allowing their coexistence or niche partitioning between them. When these niches
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are not sufficiently different, is expected that competition among species result in competitive
exclusion (HUTCHINSON, 1957). The competitive exclusion can be minimized if species differ in
some ecological aspects either in spatial or temporal scale, segregating food resources and
habitats (HUTCHINSON, 1957; PIANKA, 1974). On the other hand it is noteworthy that the
intraspecific competition for resources (between-individual variation can sometimes comprise
the majority of the population’s niche width, (sensu, BOLNICK et al., 2003) is consider the main
way for maintenance of individual diet specialization (i.e. individual uses a smaller portion of
resources relative to the whole population). This is an important feature to cause
intrapopulation niche variation (SVANBÄCK; BOLNICK, 2005; NEWSOME et al., 2015a).
In this study was analyzed isotopic composition of aquatic mammal communities in the Amazon
Estuary, adjacent coastal areas and the Parnaíba Delta, when it comes a scenery at community
level. Beyond were characterized the isotopic variation at a population level for two ecological
stocks of S. guianensis for the same study sites.
Herein, Marajó Bay is considered as part as the Amazon Estuary sector (AE) where these
manatee species occur (T. inunguis and T. manatus). Further, one estuarine-marine (Sotalia
guianensis) and three freshwater (S. fluviatilis, Inia geoffrensis and I. araguaiaensis) cetacean
species are also present (DOMNING, 1981; DA SILVA, 1983; CUNHA et al., 2010; SICILIANO et al.,
2007, 2015 unpub. data). The tucuxi, S. fluviatilis was not analyzed in this study. No overlap in
SEAc among freshwater species (T. inunguis and Inia spp., the latter including both Inia species)
and S. guianensis, indicating a complete trophic segregation among these sympatric at least in
Marajó Bay.
Freshwater species, (Inia spp. and T. inunguis) showed a larger isotopic niche area, mainly
resulting from a wide range of 13C values, which may reflect higher trophic plasticity than the
estuarine-marine S. guianensis. Specimens analyzed here include those found in estuarine
habitats (e.g. Marajó Bay, AE), and also those collected in areas of continental waters (AL)
associated with typically more 13C-depleted primary producers of the floodplain (MARTINELLI; et
al., 1994). This could be influencing the great range in carbon isotope values found in T. inunguis
and Inia spp. samples.
Amazonian manatees are exclusively herbivore, mainly feeding on aquatic and semiaquatic
macrophytes (BEST, 1981; GUTERRES et al., 2008). In Marajó bay some primary producers like