UNIVERSIDADE FEDERAL DE PERNAMBUCO
CENTRO DE TECNOLOGIA E GEOCIÊNCIAS
DEPARTAMENTO DE OCEANOGRAFIA
Habitats da megafauna marinha na costa nordeste do Brasil,
com ênfase em peixes-bois.
Danise Alves
Janson Job
Alexandra Costa
Maria Danise de Oliveira Alves
UNIVERSIDADE FEDERAL DE PERNAMBUCO
CENTRO DE TECNOLOGIA E GEOCIÊNCIAS
DEPARTAMENTO DE OCEANOGRAFIA
Habitats da megafauna marinha na costa nordeste do Brasil,
com ênfase em peixes-bois.
Tese submetida ao curso de Doutorado do
Programa de Pós Graduação em Oceanografia
da Universidade Federal de Pernambuco,
como parte dos requisitos para a obtenção do
título de Doutor em Oceanografia.
Orientadora: Profa Drª Maria Elisabeth de Araújo
Co-orientadora: Drª Miriam Marmontel
Fevereiro/2013
UNIVERSIDADE FEDERAL DE PERNAMBUCO
CENTRO DE TECNOLOGIA E GEOCIÊNCIAS
DEPARTAMENTO DE OCEANOGRAFIA
Habitats da megafauna marinha na costa nordeste do Brasil,
com ênfase em peixes-bois.
Maria Danise de Oliveira Alves
Tese submetida em 27 de fevereiro de 2013 ao
curso de Doutorado do Programa de PósGraduação em Oceanografia da Universidade
Federal de Pernambuco, como requisito para
obtenção do título de Doutor em Oceanografia
e aprovada pela seguinte banca examinadora:
_____________________________________
Drª. Maria Elisabeth de Araújo
_____________________________________
Dr. Antônio da Silva Souto
_____________________________________
Dr. Cristiano Leite Parente
_____________________________________
Dr. José Souto Rosa Filho
_____________________________________
Dr. Leonardo Liberali Wedekin
“Não tenho a anatomia de uma garça pra receber
em mim os perfumes do azul. Mas eu recebo. É uma
bênção. / Às vezes se tenho tristeza, as andorinhas
me namoram mais de perto. Fico enamorado. É
uma bênção. / Logo dou aos caracóis ornamentos
de ouro para que se tornem peregrinos do chão.
Eles se tornam. É uma bênção. / Até alguém já
chegou de me ver passar a mão nos cabelos de
Deus! Eu só queria agradecer”.
Manoel de Barros
Dedico este estudo a todos que fazem da
ciência uma luta constante pela conservação da
vida, com dignidade, respeito e humildade, que
se integram à natureza como filhos, e nunca
donos.
Agradecimentos
A minha família, o alicerce que justifica todo o meu êxito acadêmico e de vida. Cada
vitória, diante das inúmeras dificuldades, também é de vocês. E ao meu amor, Joab
Quental, pela compreensão e apoio durante as ausências e atribulações da pesquisa.
A minha orientadora Maria Elisabeth de Araújo por, finalmente, ter me aceitado como
orientanda. Serei eternamente grata por tudo que você me ensinou, e trarei sempre
comigo o seu exemplo de profissionalismo e amizade. Obrigada por tudo, gata!
A Fundação Mamíferos Aquáticos e, em particular, aos pesquisadores João Borges
(hoje um grande amigo) e Magnus Severo, pela confiança e grande responsabilidade
dada a mim para a idealização e execução do trabalho de censo aéreo.
A minha co-orientadora Miriam Marmontel pelos ensinamentos, sugestões e
disponibilidade sempre que necessário.
Ao Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) pela bolsa
de estudo concedida, e às agências de fomento Programa Petrobras Ambiental e
Fundação Grupo o Boticário, pelo financiamento dos projetos Censo Aéreo do Peixeboi marinho e Mapeamento dos habitats do peixe-boi marinho, respectivamente.
Ao Departamento de Oceanografia, por todo o suporte acadêmico e, em especial, a
Myrna, secretária do Curso de Pós Graduação, por todo o suporte ao longo do curso, e
seu Mano, pelo carinho.
Aos orientadores informais, doutores Ralf Schwamborn, Paul Kinas e Karine
Magalhães, pelos ensinamentos e ajuda fundamental.
A amiga Maria Elisa Pitanga (Magali), pela parceria em campo e inúmeros
ensinamentos sobre as angiospermas marinhas.
Aos amigos-pesquisadores que contribuíram durante as coletas de campo: Alexandra
Costa, Marcus Vinícius, Janson Job, Cláudio Cabelo, Caroline Feitosa, Helen Maria,
Daniel Lippi, Sidney Vieira, Henrique Maranhão, Viviane Melo, Pedro Cescon, Silmar
Luiz, Cássio França, Isabele Leal, Natália Carla e Farofa. E a todos os membros do IMAT,
pelo companheirismo no cotidiano do laboratório.
A NVO Táxi Aéreo pela parceria na pesquisa aérea (Geraldo, Laís e o piloto Paulo).
Aos pescadores ambientalmente conscientes do litoral nordeste do Brasil, pelos ricos
ensinamentos.
Ao Instituto Baleia Jubarte pelo empréstimo dos clinômetros.
A grande amiga Carol Feitosa, por ter me incentivado a fazer este doutorado e
vivenciar ao meu lado tantos momentos de alegria e sufoco. Obrigada, coleguinha!
As amigas e eternas parceiras profissionais, que iniciaram comigo esse grande desafio
de estudar os mamíferos aquáticos, Helen Maria e Carol Meirelles. Chegamos lá!
Aos amigos de sempre Lalá, Preta, Ane, Zezinho, Mel, Fureleza, Alê, Fernanda, Andréa
e tantos outros que me alegraram ao longo desses nove anos em Pernambuco.
Por fim, agradeço a Deus por todo o aprendizado, pela oportunidade de voar e
mergulhar em prol da conservação marinha.
Sumário
Página
Resumo.......................................................................................................................
III
Abstract......................................................................................................................
V
Lista de Figuras...........................................................................................................
VII
Lista de Tabelas..........................................................................................................
X
Apresentação.............................................................................................................
1
Introdução geral.........................................................................................................
3
Referências.................................................................................................................
5
Chapter 1 - Pilot aerial study of the marine megafauna in northern coast Alagoas,
Brazil………………………………………………………………………………………………………………………
12
Abstract…………………………………………………………………………………………………………….
12
Introduction……………………………………………………………………………………………………...
13
Study Area…………………………………………………………………………………………………………
14
Material and Methods……………………………………………………………………………………….
16
Results……………………………………………………………………………....................................
18
Discussion………………………………………………………………………………………………………….
23
References…………………………………………………………………………………………………………
25
Chapter 2 - First abundance estimate of the Antillean manatee (Trichechus
manatus manatus) in Brazil using aerial survey………………………………………………………
31
Abstract…………………………………………………………………………………………………………….
32
Introduction………………………………………………………………………………………………………
33
Material and Methods……………………………………………………………………………………….
35
Results……………………………………………………………………………....................................
42
Discussion………………………………………………………………………………………………………….
49
Conclusion and implications for conservation……………………………………………………
55
Literature cited …………………………………………………………………………………………………
56
I
Chapter
3
-
Aerial
survey
of
manatees,
dolphins
and
sea
turtles
off northeastern Brazil: correlations with coastal features and human activities……
64
Abstract…………………………………………………………………………………………………………….
65
Introduction……………………………………………………………………….................................
66
Materials and Methods……………………………………………………………………………………..
67
Results……………………………………………………………………………....................................
72
Discussion………………………………………………………………………………………………………….
80
Conclusion…………………………………………………………………………………………………………
90
References ……………………………………………………………………………………………………….
91
Chapter 4 - Distribution of Antillean manatee in relation to seagrass in
northeastern Brazil…………………………………………………………………………………………………
103
Abstract…………………………………………………………………………………………………………….
104
Introduction……………………………………………………………………….................................
105
Methods……………………………………………………………………………………………………………
107
Results……………………………………………………………………………....................................
111
Discussion………………………………………………………………………………………………………….
116
Conclusion…………………………………………………………………………………………………………
123
References……..…………………………………………………………………………………………………
124
Considerações finais..................................................................................................
133
Apêndice……………………………………………………………………………………………………………….
136
II
Resumo
Mamíferos e tartarugas marinhas são considerados organismos-chave para a
conservação marinha, sendo fundamental o desenvolvimento de pesquisas que
avaliem a distribuição e a abundância de espécies ameaçadas, como o peixe-boi
marinho (Trichechus manatus manatus). O objetivo deste estudo foi avaliar a
distribuição e a abundância da megafauna marinha no nordeste do Brasil, com ênfase
em peixes-bois marinhos e seus potencias habitats de forrageio (prados de
angiospermas marinhas), por meio de pesquisas aéreas e terrestres. A viabilidade das
pesquisas aéreas foi testada satisfatoriamente no norte de Alagoas, devido à ótima
transparência da água, com avistagem de 10 peixes-bois, 15 golfinhos (sete Sotalia
guianensis) e 13 tartarugas marinhas. No entanto, foram necessários ajustes
metodológicos para minimizar as limitações características de cada táxon e/ou habitat.
Posteriormente, foram sobrevoados 2.590,2 km2 da costa nordeste do Brasil, entre
Piauí e Alagoas, para estimar a abundância do peixe-boi marinho. Foi adotada uma
abordagem bayesiana, utilizando-se dados de avistagens aéreas e registros
bibliográficos. Este princípio foi idealizado devido à dificuldade de amostragem de uma
população dispersa em uma grande área. O número estimado de T. m. manatus foi de
1.146 indivíduos, atestando um coeficiente de variação posterior de 29% e intervalo de
probabilidade de 95%, com os extremos de 610 e 1.955 animais. No estudo de
distribuição da megafauna marinha foram registrados 41 peixes-bois, 78 golfinhos (10
S. guianensis) e 286 tartarugas marinhas (família Cheloniidae). Peixes-bois e tartarugas,
que compartilham o mesmo hábito alimentar e o habitat costeiro, correlacionaram-se
positivamente, ao contrário de golfinhos, que tem distribuição mais longe da costa. A
densidade de peixes-bois foi maior nas Áreas Marinhas Protegidas caracterizadas por
extensos estuários preservados (“Barra do Rio Mamanguape” e “Delta do Rio
Parnaíba”), enquanto que golfinhos e tartarugas por àquelas com formações recifais
(“Costa dos Corais” e “Recifes de Corais”, respectivamente). Estes resultados mostram
a importância vital de proteção e manejo adequado desses ecossistemas para garantir
um futuro sustentável às populações ameaçadas pelo desenvolvimento costeiro
urbano. A estimativa de abundância O mapeamento dos potenciais habitats de
forrageio do peixe-boi marinho foi realizado entre a costa do Rio Grande do Norte e
III
Alagoas, utilizando-se registros bibliográficos e estudos in loco para o registro de praias
com ocorrência de angiospermas marinhas. A distribuição espacial dessas plantas foi
correlacionada com os registros bibliográficos de ocorrência de peixes-bois (registros
aéreos, de encalhes e informações de pescadores). As espécies Ruppia maritima,
Halophila decipiens e Halodule wrightii foram identificadas em 53 praias, porém não
apresentaram correlação positiva com os registros de ocorrência de T. m. manatus.
Este resultado pode estar relacionado à redução desses potenciais habitats de
forrageio ao longo da costa nordeste do Brasil e/ou ao hábito generalista de herbivoria
dos peixes-bois, sendo caracterizado pelo consumo de diversos tipos de alimento ao
longo de sua extensa área de vida, principalmente de macroalgas. A visão global obtida
na presente pesquisa envolveu metodologias complementares e eficazes de
levantamentos aéreo e terrestre, e forneceu uma caracterização dos ambientes
costeiros utilizados pela megafauna marinha. Em especial, reavaliou o status
populacional do peixe-boi marinho e correlacionou a distribuição desses animais com
as angiospermas marinhas. Todas essas informações são inéditas e primordiais para a
elaboração de planos de manejo e conservação das espécies e seus habitats.
Palavras-chave: peixes-bois, golfinhos, tartarugas, nordeste do Brasil, levantamentos
aéreos, angiospermas marinhas.
IV
Abstract
Marine mammals and sea turtles are considered key organisms for marine
conservation. It is therefore important to carry out studies on the distribution and
abundance of endangered species, such as the Antillean manatee (Trichechus manatus
manatus). The aim of the present study was to assess the distribution and abundance
of marine megafauna in northeastern Brazil, with an emphasis on Antillean manatees
and its potential foraging grounds (seagrass beds), through aerial and terrestrial
surveys. The viability of aerial surveys was satisfactorily tested in the northern portion
of the state of Alagoas due to the adequate transparency of the water, which allowed
the sighting of 10 manatees, 15 dolphins (7 specimens of Sotalia guianensis) and 13
sea turtles. However, methodological adjustments were needed to minimize the
characteristic limitations of each taxon and/or habitat. Flyovers covering 2590.2 km 2 of
coastline along northeastern Brazil (between the states of Piauí and Alagoas) for
estimate the abundance of Antillean manatee. The Bayesian approach was adopted,
using data from aerial sightings and bibliographic records. This principle was conceived
due to the difficulty sampling a dispersed population a large area. The estimated
number of T. m. manatus was 1146 individuals, demonstrating a coefficient of
variation of 29% and a 95% probability interval (range: 610 to 1955 individuals). In the
study of distribution of marine megafauna were recorded 41 manatees, 78 dolphins
(10 specimens of S. guianensis) and 286 sea turtles (family Cheloniidae). Manatees and
sea turtles, which share the same feeding habits and coastal habitats, were positively
correlated. In contrast, the distribution of dolphins was farther offshore. The density of
manatees was higher in Marine Protected Areas characterized by extensive preserved
estuaries ("Barra do Rio Mamanguape" and "Delta do Rio Parnaíba"), while dolphins
and sea turtles for those with reef formations ("Costa dos Corais" and "Recifes de
Corais”, respectively). These findings demonstrate the vital importance of the
protection and adequate management of these ecosystems to ensure a sustainable
future for populations threatened by coastal urban development. The mapping of the
spatial distribution of seagrass (between the coast of Rio Grande do Norte and
Alagoas) was analyzed in relation to bibliographic records of the occurrence of the
Antillean manatee (aerial records, cases of stranding and information from fishermen).
V
This species Ruppia maritima, Halophila decipiens and Halodule wrightii were
identified on 53 beaches, but showed no correlation with the occurrence records of T.
m. manatus. This result may be related to reducing these potential foraging habitats
along the northeast coast of Brazil and/or the generalist habit of herbivory on the part
of the Antillean manatee, which feeds on different types of food resources, especially
macroalgae, throughout its variable home range. The overview obtained in the present
study involved effective, complementary methods of land and aerial surveys and
provided a characterization of coastal environments used by endangered marine
megafauna. Moreover, this study reevaluated the population status of the Antillean
manatee and related the distribution of this species with seagrass beds. This
information is has not previously been published and is essential to the drafting of
management plans for the conservation of these species and their habitats.
Keywords: manatees, dolphins, sea turtles, northeastern Brazil, aerial surveys,
seagrass
VI
Lista de Figuras
Página
Chapter 1 - Pilot aerial study of the marine megafauna in northern coast Alagoas,
Brazil.
Figure 1 - Northern coast of Alagoas showing the aerial transects (zigzag)
between Peroba Beach and Ponta Verde Beach. Highlight for the coverage area
of the Marine Protected Area “Costa dos Corais” within the study area (dotted
line)….......................................................................................................................
15
Figure 2 - Spatial distribution of Antillean manatees, dolphins and sea turtles
during aerial survey with zigzag trajectory on northern coast of Alagoas,
northeastern Brazil. Highlighting the transect sampling irregular-shaped in
estuary of “Barra de Santo Antônio”, and sightings of manatees near
Tatuamunha and Camaragibe Rivers. ………………………………………………………………….
19
Figure 3 - Aerial photo showing favorable conditions (optimal water
transparency and calm sea - Beaufort Sea state 1) for sightings of marine
mammals and sea turtles during flyover on northern coast of Alagoas……………..
20
Figure 4 - Aerial photo of validation of viability of aerial survey of estuaries
performed in natural captivity of three Antillean manatees in estuary of
Tatuamunha River, Alagoas; Image reveals non-viability of visual detection due
to high water turbidity …………………………………………………………………………………..…
21
Figure 5 - Schematic of strip transect sampling method from aircraft indicating
constant altitude, maximum sighting angle and length of base scanned (tread
area) by each observer………………………………………………………………………………..…….
22
Chapter 2 - First abundance estimate of the Antillean manatee (Trichechus
manatus manatus) in Brazil using aerial survey.
Figure 1 - Study area between the states of Piauí and Alagoas, northeastern
Brazil (A). Aerial transects in a zigzag pattern in the estuarine mouth Delta do
Rio Parnaíba (B)……………………………………………………………………………………………………
36
Figure 2 - Map representing parameters of statistical model used to analyze
sightings of manatees (manatee drawing): i – identifier index of sampling units
VII
(numbers); Ai – total area (rectangular spotted polygon), and ai – area tracked by
observers (wavy band)…………………………………………………………………………………..…….
39
Figure 3 - Manatee sightings between Piauí and Alagoas states, during on effort
(manatee drawings) and off effort (red circle) periods………………………..……………….
43
Figure 4 - Manatee sightings (black circles) under different scales of visibility,
during aerial surveys in northeastern Brazil: (1) Excellent – two manatees
submerged in a seagrass bed, Quitéria's beach (4° 40' S, 37° 18' W) in Ceará
state (2); Good – one manatee close to the water surface, Pirangi do Sul beach
(5° 58' S, 35° 6' W) in Rio Grande do Norte state; (3) Medium – two manatees,
with one identified only because of the rostrum emergence in the water (black
arrow), Oiteiro beach (6° 51' S, 34° 53' W) in Paraíba state; and (4) Poor – one
manatee visible after almost total body exposure on water surface, estuarine
mouth in Guajú River (6° 29' S, 34° 57' W) in Rio Grande do Norte state……………..
45
Figure 5 - A priori (dotted line) and a posterior (continuous line) distribution for
the probability of p detection………………………….……………………………………………..……
46
Figure 6 - A priori (dotted line) and posterior (continuous line) distribution for
the density of individuals μ………………………………………………………………………………….
47
Figure 7 - Posterior distribution of manatee abundance (N) in the study area……..
48
Chapter
3
-
Aerial
survey
of
manatees,
dolphins
and
sea
turtles
off northeastern Brazil: correlations with coastal features and human activities.
Figure 1 - Map of the study area between the states of Piauí and Alagoas,
northeastern Brazil (A) showing the main Marine Protected Areas (DP - Delta do
Rio Parnaíba, RC - Recifes de Corais, BM - Barra do Rio Mamanguape, CC - Costa
dos Corais) and coastal cities (black squares). Inlet: Aerial transects in a zigzag
pattern in the marine protected area Delta do Rio Parnaíba (B)………………………….
68
Figure 2 - Spatial distribution of manatees, dolphins and sea turtles between the
states of Piauí and Alagoas, northeastern Brazil. Marine protected areas are
indicated as gray rectangles (DP: Delta do Rio Parnaíba, RC: Recifes de Corais,
BM: Barra do Rio Mamanguape, CC: Costa dos Corais). White rectangle: area
with scarce sightings. A single sighting of manatee mother and calf is highlighted
VIII
in a circle, and specimens of Sotalia guianensis in light blue color. Dotted lines:
state borders.………………………………………………………………………………………………………
73
Figure 3 - Frequency histograms of depth (m) and distance from shore (km) at
the sighting locations for manatees (a, b), dolphins (c, d), and sea turtles (e, f) in
northeastern Brazil. Data are based on 27 hours of aerial surveys carried out
along the northeastern Brazilian coast from the states of Piauí to Alagoas............
75
Figure 4 - Density of manatees (left), dolphins (center) and sea turtles (right) in
marine protected areas in northeastern Brazil (DP: Delta do Rio Parnaíba, RC:
Recifes de Corais, BM: Barra do Rio Mamanguape, CC: Costa dos Corais, Outside:
areas outside marine protected areas). Data are based on 27 hours of aerial
surveys from the states of Piauí to Alagoas. N = 294 coastal segments of 5 km
length………………………………………………………………………………………………………………….
78
Chapter 4 - Distribution of Antillean manatee in relation to seagrass in
northeastern Brazil.
Figure 1 - Study area with demarcation of sampling units (70 km) for analysis of
the spatial distribution of seagrass between the states of Rio Grande do Norte
and Alagoas along the northeastern coast of Brazil …………………………………….……...
108
Figure 2 - Distribution of seagrass in present study (A) and based on data from
the literature (B) (Laborel-Deguen, 1963; Den Hartog, 1972; Oliveira-Filho et al.,
1983; Magalhães and Cazuza, 2005; Vieira, 2006; Reis, 2007; Silva, 2010; Silva et
al., 2012). The details show the areas with the greatest numbers of these plants.
112
Figure 3 - Bray-Curtis dendogram (A) and graph (B) of occurrence of seagrass in
sampling sectors based on data from the literature and the present study………….
113
Figure 4 - Spatial distribution of records of occurrence of seagrass in the study
area based on data from the literature (A) and the present study (B) as well as
the occurrence of manatees based on aerial sightings (A, B – airplane), stranding
(A, B – cross) and information from fishermen (A, B – fisherman)……………………….
114
Figure 5 - Bray-Curtis dendogram (A) and graph (B) of occurrence of manatees in
sampling sectors based on aerial sightings, stranding and information from
fisherman……………………………………………………………………..……………………………………..
115
IX
Lista de Tabelas
Página
Chapter 1 - Pilot aerial study of the marine megafauna in northern coast Alagoas,
Brazil.
Table 1 - Summary of sightings of Antillean manatees (Trichechus manatus
manatus), dolphins and sea turtles during aerial survey on northern coast of
Alagoas, northeastern Brazil....................………………………………………….…………………
19
Chapter 2 - First abundance estimate of the Antillean manatee (Trichechus
manatus manatus) in Brazil using aerial survey.
Table 1 - Criteria to determine occurrence probabilities (z values) relative to
occurrence of Antillean manatee in sampling units in northeastern Brazil…………..
40
Table 2 - Occurrence of manatees on and off effort, and the demographic
density by stretch of coast (DC = org/km) and area (DA* = org/km 2) for each
state…………………………………………………………………………………………………………………….
44
Table 3 - Distribution of 899 regions according to probability of manatee
occurrence (z) and number of sighted individuals "on effort" (Y)…………………………
48
Table 4 - Statistical summaries of posterior distributions of main parameters
(2.5% and 97.5% quantis delimit the 95% creditability intervals; "Mean"
corresponds to the specific estimate in the study………………...................................
Chapter
3
-
Aerial
survey
of
manatees,
dolphins
and
sea
49
turtles
off northeastern Brazil: correlations with coastal features and human activities.
Table 1 - Summary of the sightings of manatees, dolphins and sea turtles during
aerial surveys in northeastern Brazil. N = number………………………………………..….….
73
Table 2 - Results of Spearman correlation analysis of sightings of manatees,
dolphins, sea turtles, selected coastal features and human activities, based on
27 hours of aerial surveys in northeastern Brazil. Values given in the table are
“p” values of the analyses based on N = 294 coastal segments of 5 km in
length………………………………………………………………………………………………………………….
76
X
Table 3 - Marine Protected Areas (MPAs) in northeastern Brazil and total
sightings of manatees, dolphins and sea turtles. Data are based on 27 hours of
aerial surveys. N = 294 coastal segments of 5 km length. Values given in the
table are total number of organisms (N) and density (N per km coastline).…..…….
79
XI
Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
Apresentação
A presente tese aborda duas problemáticas envolvendo a conservação da
megafauna marinha no nordeste do Brasil, representada por espécies vulneráveis a
criticamente ameaçadas de extinção. São elas: (1) padrões de distribuição espacial do
peixe-boi
marinho
(Trichechus
manatus
manatus),
golfinhos
correlacionando-os com fatores ecológicos, como a presença de
e
tartarugas,
estuários e
angiospermas marinhas, e fatores antropogênicos, como atividades de pesca e
crescimento urbano costeiro; (2) Estimativa de abundância do mamífero aquático mais
ameaçado de extinção do país, o peixe-boi marinho. Foram empregadas metodologias
pioneiras no nordeste do Brasil para o mapeamento dos habitats de ocorrência desses
grupos taxonômicos costeiros, definidas pelos levantamentos aéreos, para a detecção
e contagem dos indivíduos, e pelo mapeamento terrestre, para identificação dos
habitats de forrageio do peixe-boi marinho, caracterizados pelos prados de
angiospermas marinhas.
A tese está estruturada em quatro capítulos que incluem seus respectivos
objetivos específicos a seguir:
I. Avaliar a aplicabilidade metodológica dos levantamentos aéreos para estudos de
distribuição e abundância da megafauna marinha costeira do nordeste do Brasil,
utilizando o norte de Alagoas como área para o estudo piloto;
II. Estimar a abundância de peixes-bois marinhos ao longo da costa nordeste do Brasil
(entre os estados do Piauí e Alagoas), para subsidiar uma reavaliação do status de
conservação das populações criticamente ameaçadas de extinção.
III. Quantificar e analisar a distribuição espacial de peixes-bois, golfinhos e tartarugas
em larga-escala geográfica no nordeste do Brasil (entre os estados do Piauí e Alagoas),
1
Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
correlacionando-a com o tipo de habitat, atividades humanas e importância das Áreas
Marinhas Protegidas;
IV. Mapear as áreas de ocorrência das angiospermas marinhas no nordeste do Brasil
(entre os estados do Rio Grande do Norte e Alagoas), visando avaliar a importância
desses ecossistemas como potenciais habitats de forrageio do peixe-boi marinho.
2
Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
Introdução geral
Mamíferos e tartarugas marinhas são considerados organismos-chave para a
conservação dos mares em diversas partes do mundo (Chatwin 2007). Muitas
populações ocorrem em áreas costeiras que são intensamente exploradas por
humanos (Ojeda-Martínez et al. 2011), tornando-as vulneráveis ou ameaçadas de
extinção (IUCN 2012), e o estabelecimento de Áreas Marinhas Protegidas (AMPs) são
essenciais na proteção desses grupos e seus ecossistemas (Hooker & Gerber 2004).
No litoral nordeste do Brasil, as principais ameaças à biodiversidade costeira são
as atividades de pesca e o intenso desenvolvimento urbano, tornando essa região uma
das mais vulneráveis da América do Sul (Chatwin 2007). Os mamíferos aquáticos mais
comuns dessa região são o peixe-boi marinho, Trichechus manatus manatus Linnaeus
1758 (Lima et al. 2011), o mais ameaçado de extinção do Brasil (ICMBio 2011), e o
boto-cinza, Sotalia guianensis (van Bénéden 1864) (Alvite et al. 2004). Dentre as cinco
espécies registradas de tartarugas marinhas, a mais comum é tartaruga-verde,
Chelonia mydas (Linnaeus 1758) (Marcovaldi & Marcovaldi 1999).
No Brasil, pesquisas de distribuição e abundância da megafauna marinha
utilizaram principalmente dados de encalhes e informações de pescadores (Marcovaldi
& Marcovaldi 1999, Parente et al. 2004, Luna et al. 2008, Meirelles et al. 2009, Lima et
al. 2011). Em particular, estudos com peixes-bois marinhos foram desenvolvidos com
base no conhecimento tradicional de pescadores, a partir da década de 80. Os
resultados evidenciaram um padrão de distribuição descontínuo ao longo do litoral
norte e nordeste do país, com abundância de menos de 500 indivíduos (Albuquerque
& Marcovaldi 1982, Luna et al. 2008, Lima et al. 2011).
3
Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
Estudos mundiais de distribuição e estimativa de abundância da megafauna
marinha utilizam comumente os levantamentos aéreos (Preen 2004, Edwards et al.
2007, Jean et al. 2010, Langtimm et al. 2011). No entanto, esta técnica possui fatores
limitantes para a sua aplicação, como a turbidez da água aliada ao viés de percepção
do observador sobre as avistagens dos animais (Marsh & Sinclair 1989, Pollock et al.
2006, Katsanevakis et al. 2012). No Brasil, essa metodologia foi aplicada
principalmente na região sul (Secchi et al. 2001, Danilewicz et al. 2010, Zerbini et al.
2010, 2011), com o golfinho Pontoporia blainvillei, destacando-se na região nordeste
os trabalhos com a baleia jubarte, Megaptera novaeangliae (Andriolo et al. 2006,
2010, Wedekin 2011) e o peixe-boi marinho (Costa 2006).
Os habitats do peixe-boi estão situados nos rios, estuários e águas costeiras rasas
do leste do México, América Central, e norte e nordeste da América do Sul (Lefebvre et
al. 2001). Sua distribuição é determinada fundamentalmente pela presença de água
doce e de vegetação aquática (Hartman 1979, Olivera-Gómez & Mellink 2002, 2005).
No Brasil, o padrão de distribuição desses animais é praticamente desconhecido,
principalmente em relação às áreas de alimentação, com poucos trabalhos realizados
por meio do monitoramento de animais nativos, em áreas restritas (Paludo & Langguth
2002, Alves 2003, 2007, Costa 2006), ou de espécimes reintroduzidas à natureza (Lima
2008). Sugere-se que essa distribuição seja consideravelmente ampla, em virtude da
grande diversidade de vegetais identificados na sua dieta (Borges et al. 2008).
Os ecossistemas de angiospermas marinhas, que abrangem diversas espécies
consumidas pelos peixes-bois (Hartman 1979, Borges et al. 2008, Lima et al. 2011), são
extremamente afetados por atividades antropogênicas, com reduções na sua área de
cobertura em áreas costeiras rasas e estuarinas de todo o mundo (Short et al. 2006,
4
Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
Ceccherelli et al. 2007, Pitanga et al. 2012). Na costa do Brasil, o conhecimento sobre a
distribuição dessas plantas é reduzido, consistindo em trabalhos desatualizados ou de
escalas locais (Laborel-Deguen 1963, den Hartog 1972, Oliveira-Filho et al. 1983,
Magalhães & Cazuza 2005, Marques & Creed 2008, Sordo et al. 2011). O conhecimento
sobre a distribuição das potenciais áreas de forrageio dos peixes-bois é essencial para
o estabelecimento de estratégias conservacionistas a nível local e regional, garantindo
a proteção da espécie e seus habitats (Paludo & Langguth 2002, Olivera-Gómez &
Mellink 2005, Alves-Stanley et al. 2010).
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Andriolo A, Kinas PG, Engel MH, Martins CCA, Rufino AM (2010) Humpback whales
within the Brazilian breeding ground: distribution and population size estimate.
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alimentares constituintes da dieta dos peixes-boi marinhos (Trichechus
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seagrass Posidonia oceanica to simulated anchor impact. Mar Environ Res 63:
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manatus manatus (Sirenia: Trichechidae) no litoral leste do Estado do Ceará.
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Florida. Am Soc Mammalog, Special Publ. 5:153
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Severo MM (eds) Instituto Chico Mendes de Conservação da Biodiversidade,
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Fiorentino F, Garofalo G, Giacalone VM, Hawley KL, Issaris Y, Jansen J, Knight
CM, Knittweis L, Kröncke I, Mirto S, Muxika I, Reiss H, Skjoldal HR, Vöge S (2012)
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imperfect detectability. Aquat Biol 16:31–52
Laborel-Deguen F (1963) Nota preliminar sobre a ecologia das pradarias de
fanerógamas marinhas nas costas dos estados de Pernambuco e da Paraíba.
Trab Inst Biol Mar Ocean 3/4:39–50
Langtimm CA, Dorazio RM, Stith BM, Doyle TJ (2011) New Aerial Survey and
Hierarchical Model to Estimate Manatee Abundance. J Wildl Manage 75:399–
412
Lefebvre LW, Marmontel M, Reid JP, Rathbun GB, Domning DP (2001) Status and
Biogeography of the West Indian Manatee. In: Woods CA, Sergile FE (eds)
Biogeography of the West Indies: patterns and perspectives, CRC Press., Boca
Ratón, Florida, p 425–474
Lima RP (2008) Distribuição espacial e temporal de peixes-bois (Trichechus manatus)
reintroduzidos no litoral nordestino e avaliação da primeira década (1994-2004)
do programa de reintrodução. Tese de Doutorado, Universidade Federal de
Pernambuco, Recife
Lima RP, Paludo D, Soavinski RJ, Silva KG, Oliveira EMA (2011) Levantamento da
distribuição, ocorrência e status de conservação do Peixe‐Boi Marinho
(Trichechus manatus, Linnaeus, 1758) no litoral nordeste do Brasil. Nat Resour
Aquidabã 1:41–57
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Luna FO, Lima RP, Araújo JP, Passavante JZO (2008) Status de conservação do peixe-boi
marinho (Trichechus manatus manatus Linnaeus, 1758) no Brasil. Rev Br
Zoocien 10:145–153
Magalhães KM, Cazuza SM (2005) Distribuição das angiospermas marinhas no litoral
do estado de Pernambuco, Brasil - 1ª Parte: Levantamentos de herbários e
literatura. Cad Fafire 4:20–26
Marcovaldi MA, Marcovaldi GG (1999) Marine turtles of Brazil: the history and
structure of Projeto TAMAR-IBAMA. Biol Conserv 91:35–41
Marques LV, Creed JC (2008) Biologia e ecologia das fanerógamas marinhas do Brasil.
Oecol Bras 12:315–331
Marsh H, Sinclair DF (1989) Correcting for visibility bias in strip transect aerial surveys
of aquatic fauna. J Wildl Manage 53:1017–1024
Meirelles ACO, Monteiro-Neto C, Martins AMA, Costa AF, Barros HMDR, Alves MDO
(2009) Cetacean strandings on the coast of Ceará, north-eastern Brazil (19922005). J. Mar. Biol. Assoc. U. K. 89:1083–1090
Ojeda-Martínez C, Bayle-Sempere JT, Sánchez-Jerez P, Salas F, Stobart B, Goñi R, Falcón
JM, Graziano M, Guala I, Higgins R, Vandeperre F, Le Direach L, Martín-Sosa P,
Vaselli S (2011) Review of the effects of protection in marine protected areas:
current knowledge and gaps. Anim Biodivers Conserv 34:191–203
Olivera-Gómez LD, Mellink E (2002) Spatial and temporal variation in counts of the
Antillean manatee (Trichechus manatus manatus) during distribution surveys at
Bahıa de Chetumal, Mexico. Aquat Mamm 28:285–293
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Olivera-Gómez LD, Mellink E (2005) Distribution of the Antillean manatee (Trichechus
manatus manatus) as a function of habitat characteristics, in Bahía de
Chetumal, Mexico. Biol Conserv 121:127–133
Oliveira-Filho EC, Pirani JR, Giulietti AM (1983) The Brazilian Seagrasses. Aquat Bot
16:251–267
Paludo D, Langguth A (2002) Use of space and temporal distribution of Trichechus
manatus manatus Linnaeus in the region of Sagi, Rio Grande do Norte State,
Brazil (Sirenia, Trichechidae). Rev Bras Zool 19:205–215
Parente CL, Vergara-Parente JE, Lima RP (2004) Strandings of Antillean Manatees,
Trichechus manatus manatus, in Northeastern Brazil. Lat Am J Aquat Mamm
3:69–75
Pitanga ME, Montes MJF, Magalhães KM, Reis TNV (2012) Quantification and
classification of the main environmental impacts on a Halodule wrightii
seagrass meadow on a tropical island in northeastern Brazil. An Acad Bras Cienc
84:35–42
Pollock K, Marsh H, Lawler IR, Alldredge MW (2006) Estimating animal abundance in
heterogenous environments: an application to aerial surveys for dugongs. J Wildl
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Preen A (2004) Distribution, abundance and conservation status of dugongs and
dolphins in the southern and western Arabian Gulf. Biol Conserv 118:205–218
Secchi ER, Ott PH, Crespo EA, Kinas PG, Pedraza SN, Bordino P (2001) A first estimate of
franciscana (Pontoporia blainvillei) abundance off southern Brazil. J Cetac Res
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SeagrassNet monitoring across the Americas: case studies of seagrass decline.
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morphology and biomass of vulnerable Halodule wrightii meadows at their southernmost
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Wedekin LL (2011) Ecologia populacional da baleia-jubarte (Megaptera novaeangliae
Borowski, 1871) em sua área reprodutiva na costa do Brasil, Oceano Atlântico
Sul. Tese de Doutorado, Universidade Federal do Paraná, Curitiba.
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and distribution of the franciscana (Pontoporia blainvillei) in the Franciscana
Management Area II (southeastern and southern Brazil). IWC Scientific
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JL (2011) Assessing bias in abundance estimates from aerial surveys to improve
conservation of threatened franciscana dolphins: preliminary results from a
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Norway. 13pp
11
Capítulo 1*† - Estudo aéreo piloto da megafauna marinha na costa norte de Alagoas,
Brasil.
Chapter 1*† - Pilot aerial study of the marine megafauna in northern coast Alagoas,
Brazil.
* Capítulo em formato de artigo e padronizado de acordo com as normas da revista
Tropical Oceanography
† Artigo aceito na revista Tropical Oceanography (no prelo)
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
ISSN: 1679-3013
D.O.I.: 10.5914/V. 41; N° 2; 2013.
1
2
PILOT AERIAL STUDY OF THE MARINE MEGAFAUNA IN NORTHERN COAST
3
ALAGOAS, BRAZIL.
4
Maria Danise de Oliveira ALVES1,2
5
João Carlos Gomes BORGES2,3
6
Maria Elisabeth de ARAÚJO4
7
8
ABSTRACT
9
This study aimed to investigate the feasibility of strip-transect aerial survey for the study of
10
the marine megafauna in northern coast of Alagoas, chosen as the pilot area due to the
11
better water clarity and the occurrence of the Antillean manatee. It was sighted 15 dolphins,
12
13 sea turtles and 10 manatees. From five aspects tested on the experimental flight, three
13
adjustments were necessary on the methodology as following: 1) reduction of the transect
14
angle to 40º to increase the sampling area; 2) constant transects of 1.5 nautical miles from
15
shore to standardize the area of coverage; and 3) transects restricted to the mouths of
16
estuaries due to low visibility in turbid waters. This study demonstrated the effectiveness of
17
aerial surveys for the detection of marine megafauna. However, the adjustments proposed
18
are necessary to minimize the characteristic limitations of each species and/or habitat.
19
Keywords: aerial method, manatees, dolphins, sea turtles, limitations.
20
21
RESUMO
22
O estudo objetivou investigar a viabilidade do censo aéreo no estudo da megafauna
23
marinha no norte de Alagoas, escolhida como área piloto devido à melhor transparência da
24
água e presença de peixes-bois marinhos. Foram avistados 15 golfinhos, 13 tartarugas e 10
25
peixes-bois. Dentre os cinco parâmetros testados no voo piloto, três sofreram ajustes
26
metodológicos: 1) redução do ângulo de abertura das transecções aéreas para 40°,
12
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
27
aumentando a área amostrada; 2) transecções constantes a 1,5 milhas náuticas da costa,
28
padronizando-se a área de cobertura; e 3) transecções restritas às desembocaduras dos
29
estuários, devido à impossibilidade de detecções de animais dentro dos estuários, onde há
30
águas muito turvas. Os resultados mostraram a eficácia metodológica das pesquisas aéreas
31
na detecção da megafauna marinha. No entanto, os ajustes propostos são necessários para
32
minimizar as limitações características de cada táxon e/ou habitat.
33
Palavras-chave: método aéreo, peixe-boi marinho, golfinhos, tartarugas, limitações.
34
35
INTRODUCTION
36
Aerial surveys have been used throughout the world to estimate the distribution and
37
abundance of aquatic animals, the most studied of which are sea turtles and marine
38
mammals (MCCLELLAN, 1996; PREEN et al., 1997; ROOS et al., 2005; LANGTIMM et al.,
39
2011). However, such surveys are rare in Brazil and mainly restricted to the southern
40
region of the country (SECCHI et al., 2001; DANILEWICZ et al., 2010; ZERBINI et al.,
41
2010; ZERBINI et al., 2011). Indeed, published studies have been carried out in the
42
northeastern region, addressing the humpback whale [Megaptera novaeangliae (Borowski,
43
1781)] (ANDRIOLO et al., 2006; 2010; WEDEKIN, 2011) and Antillean manatee (Trichechus
44
manatus manatus LINNAEUS, 1758) (COSTA, 2006). Other studies in the region have relied
45
mainly on data from stranded animals and the reports of fishermen (MARCOVALDI;
46
MARCOVALDI, 1999; PARENTE; VERGARA-PARENTE; LIMA, 2004; LUNA et al., 2008;
47
MEIRELLES et al., 2009; LIMA et al., 2011).
48
The perception and availability bias regarding the sighting of marine animals are the main
49
limiting factors to aerial surveys (MARSH; SINCLAIR, 1989; KATSANEVAKIS et al., 2012).
50
According to COSTA (2006), the high cost of aircraft rental and the difficulty sighting
51
specimens in turbid coastal waters at particular times of the year limit the use of this
52
method in northeastern Brazil. Sampling difficulties can render the identification of species
53
and the precise count of individuals in a population impossible. However, this method is
54
useful in understanding population tendencies (REYNOLDS, 1999), especially among species
13
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
55
vulnerable to extinction, such as the manatee, which is considered the most endangered
56
aquatic mammal in Brazil (ICMBIO, 2011).
57
The megafauna on the northeastern coast of Brazil is represented by a single species from
58
the order Sirenia, the Antillean manatee (T. m. manatus) (LIMA et al., 2011), 19 species of
59
cetaceans (ALVITE et al., 2004), the most frequent of which is the Guiana dolphin [Sotalia
60
guianensis (VAN BÉNÉDEN, 1864)], and five of the seven living species of sea turtles: green
61
sea turtle [Chelonia mydas (LINNAEUS, 1758)], loggerhead sea turtle [Caretta caretta
62
(LINNAEUS, 1758)], hawksbill sea turtle [Eretmochelys imbricata (LINNAEUS, 1766)], olive
63
Ridley sea turtle [Lepidochelys olivacea (ESCHSCHOLTZ, 1829)] and leatherback sea turtle
64
[Dermochelys coriacea (VANDELLI, 1761)] (GOMES; SANTOS; HENRY, 2006). The Antillean
65
manatee has particular characteristics of occurrence in comparison to other species, such as
66
warm, shallow waters (OLIVERA-GÓMEZ; MELLINK, 2005), abundant aquatic vegetation
67
(PALUDO; LANGGUTH, 2002; COSTA, 2006) and human activities (PARENTE; VERGARA-
68
PARENTE; LIMA, 2004; BORGES et al., 2007). Therefore, estuaries are essential habitats as
69
foraging, breeding and resting grounds for the manatee (REYNOLDS; POWELL, 2002; LIMA
70
et al., 2011).
71
The aim of the present study was to investigate the applicability of aerial surveys using
72
strip-transect
73
northeastern Brazil, using the northern coast of the state of Alagoas as a pilot area.
for
studies
of
distribution
and
abundance
of
marine
megafauna
in
74
75
STUDY AREA
76
The geographic limits of the sampling area on the northern coast of the state of Alagoas
77
were Peroba Beach [northernmost portion of the state (08°07'52"S/34°55'33"W)] to Ponta
78
Verde Beach in the capital city Maceió (09°30'39"S/35°47'56"W), totaling approximately
79
114 km of coastline (Fig. 1). This area was chosen mainly due to its higher water
80
transparency in comparison to other areas of northeastern Brazil as well as the constant
81
occurrence of manatees of either native populations or reintroduced specimens (LIMA,
82
2008; LIMA et al., 2011). This ideal conditions were decisive for validate the aerial
83
sampling.
14
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
84
85
Figure 1 – Northern coast of Alagoas showing the aerial transects (zigzag) between Peroba
86
Beach and Ponta Verde Beach. Highlight for the coverage area of the Marine Protected Area
87
(MPA) “Costa dos Corais” within the study area (dotted line).
88
89
This area has different coastal ecosystems, such as estuaries and lagoons with mangroves
90
positioned transversally to the coastline as well as coral and sandstone reefs occurring from
91
the coastline to several meters in depth (CORREIA; SOVIERZOSKI, 2005). A large part of
92
the study area is located within the Marine Protected Area (MPA) “Costa dos Corais” (Fig.
93
1), considered the largest marine protected area in Brazil. This MPA was established to
94
protect the reef ecosystems, maintain the integrity of the mangroves and preserve the
95
manatee population (FERREIRA; CAVA, 2001; LIMA 2008).
96
The present study was designed as a pilot plan for a subsequent study from the coast of the
97
state of Piauí to the state of Alagoas, initially focusing on T. m. manatus, with the
98
subsequent inclusion of dolphins and sea turtles.
99
100
15
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
101
MATERIAL AND METHODS
102
The main analyzed factors for the detection success of animals were as follows: (1) strip
103
transect methodology, using zigzag transects perpendicular to the coast; (2)
104
angle measure for sighting marine animals and a subsequent calculation of the threshold
105
area scanned; (3) conditions of the flight altitude, speed and visualization of the sea surface
106
(bubbles windows); (4) morphology and behavior of each taxon as influential factors in the
107
detection and identification of species; and (5) environmental conditions of the Beaufort
108
scale and transparency of water (coastal and estuarine) for the ideal aerial survey.
109
The present study was carried out in January 2010, a month of dry season, with a sampling
110
effort of two hours of flight. The total area covered was 264 km2, with more than 312 km of
111
distance travelled in a zigzag pattern.
the largest
112
113
Identification of animals
114
The identification of the species was based on the diagnostic morphological and behavioral
115
characteristics of each species. In cases of dubious sightings or imprecise counts of
116
individuals, recounts were performed (LANGTIMM et al., 2011) through circular flights over
117
the location of the sight and imprecise records were discarded. A group was defined as two
118
or more animals (MORALES-VELA et al., 2000).
119
The main morphological characteristics used for the aerial identification of T. m. manatus
120
were brownish-gray coloration, robust fusiform body shape, flat oar-shaped caudal fin
121
(HUSAR, 1978) and slow movement (HARTMAN, 1979). A calf was a specimen measuring
122
1/3 of the adult animal by its side (HARTMAN op. cit.). The distinctive characteristics of
123
dolphins were the fusiform shape, body coloration, morphology of the head and dorsal fin
124
(JEFFERSON; LEATHERWOOD; WEBBER, 1993) and fast swimming with occasional leaps.
125
The
126
(Dermochelydae) shell, circular body shape (with fusiform and curvilinear carapace
127
composed of plates) and oar-shaped pectoral fins used simultaneously for swimming
128
(WYNEKEN, 2001).
references
for
sea
turtles
were
the
greenish-brown
(Cheloniidae)
or
black
16
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
129
Aerial survey
130
“Strip transect” was the sampling method, which is defined by monitoring a strip of
131
predetermined width in which each observer records all sightings. This method allows
132
acquiring data on distribution and estimating the representative density in the area
133
samples, thereby allowing the estimation of abundance (JOLLY, 1969). To conduct this
134
method is recommended initially a pilot sample, according to the particular characteristics of
135
each environment and species, never assuming their application a priori (KATSANEVAKIS et
136
al., 2012). The sampling area (strip) was demarcated from the tip of the wing of the aircraft
137
to the strip directly below the wings (Fig. 5). Clinometers were used to determine the
138
largest angle measure for sighting marine animals and a subsequent calculation of the
139
threshold area scanned.
140
Sampling was performed in systematic zigzag transects (Fig. 1) with a 60º open angle
141
perpendicular to the coast, accompanying the width of the continental shelf. This transects
142
were designed to better cover the area and to maximize flying effort (ANDRIOLO et al.,
143
2006; 2010). Estuaries were also sampled, as these sites are habitats for manatees (LIMA
144
et al., 2011). Flights over these ecosystems occurred parallel to the margins of river,
145
traveling approximately 1 km inland (Fig. 1 and 2).
146
The aircraft used was a single-engine high-wing Cessna 172 A, with bubble windows
147
adapted in the posterior portion (ZERBINI et al., 2011), ideal for the observers to view the
148
ocean surface. Flyovers standardized occurred at an altitude of 150 m and a velocity of 140
149
km.h-1 (coast and estuaries), which is within the minimum range recorded in previous
150
studies (MORALES-VELA et al., 2000; WRIGHT et al., 2002; COSTA, 2006) and corresponds
151
to the minimum safety conditions of the crew during the study. The flyover crew was
152
composed of a pilot, positioned on the left of the plane, two independent observers laterally
153
covering each sampling strip (detection bias) in the rear portion of the plane and an
154
annotator alongside the pilot. The observers were equipped with clinometers to measure the
155
width of the strip sampled.
156
The annotator was equipped with a GPS to register the location of the sightings as well as
157
the GPS of the plane for recording the flight path, two photographic cameras, nautical
17
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
158
charts of the study area and standardized charts to record data on the flight conditions
159
(altitude in feet and velocity in km.h-1), environmental conditions (visibility, Beaufort Sea
160
state and tide), human activities and sightings of marine megafauna (species, abundance,
161
social structure, time and geographic position). The flight took place in the dry season
162
(summer) during the rising tide, which allowed an increase in the spatial use of the animals,
163
especially those with coastal habits and those that use estuaries. Data collection involved
164
the identification of the specimens, sighting number, size of group, composition of group
165
(presence of offspring), geographic position of sighting within the transect), habitat
166
location/type, time and geographic position of takeoff and landing, time and geographic
167
position of sampling.
168
The ideal environmental conditions expected for aerial survey were Beaufort Sea state 2 or
169
less, absence of rain or mist (PREEN, 2004; LANYON, 2003), and water transparency
170
"excellent" (animals clearly visible even underwater).
171
172
Data analysis
173
The survey design and locations of the sightings were transferred to the “GPS TrackMaker
174
Pro” program (ANDRIOLO et al., 2010) for subsequent spatialization using the Arcmap
175
program (version 9.3), identified nominally and by two coordinates (lat/long), to determine
176
the spatial pattern of species occurrence.
177
178
RESULTS
179
A total of 16 sightings and 38 specimens of manatees, dolphins and sea turtles were
180
recorded (Tab. 1), with higher occurrence number in the southern portion of the sampling
181
area (Fig. 2).
182
183
184
18
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
185
Table 1 – Summary of sightings of Antillean manatees (Trichechus manatus manatus),
186
dolphins and sea turtles during aerial survey on northern coast of Alagoas, northeastern
187
Brazil.
Manatee
Dolphin
Sea Turtle
Number of sighting
7
4
5
Total animals
10
15
13
Mean animals/sighting
1.4
3.75
2.6
Maximum animals/sighting
3
7
4
188
189
Figure 2 – Spatial distribution of Antillean manatees, dolphins and sea turtles during aerial
190
survey with zigzag trajectory on northern coast of Alagoas, northeastern Brazil. Highlighting
191
the transect sampling irregular-shaped in estuary of “Barra de Santo Antônio”, and sightings
192
of manatees near Tatuamunha and Camaragibe Rivers.
19
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
193
The environmental conditions were favorable to the detection of marine megafauna from
194
the air, with optimal water transparency and the absence of clouds and strong winds, which
195
that corresponds Beaufort Sea state 1 (Fig. 3).
196
Figure 3 – Aerial photo showing favorable conditions (optimal water transparency and calm
197
sea - Beaufort Sea state 1) for sightings of marine mammals and sea turtles during flyover
198
on northern coast of Alagoas.
199
200
The behavior of Antillean manatees, with little exposure at the water surface and its
201
predominantly solitary habits (unlike the other taxa studied) did not hamper detection due
202
to the high water transparency, which allowed the visualization of submerged individuals.
203
However, the sightings of some manatees and sea turtles became more confusing when
204
flying over areas located above reefs or in very turbid waters due to the cryptic brownish
205
coloration of these animals. In five of these cases, we performed the recount effort, two of
206
them being discarded.
207
The detection of manatees within four estuaries was not possible due to the high water
208
turbidity, the difficulty of flying over narrow, twisting channels (e.g. estuary of Barra de
20
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
209
Santo Antônio; Fig. 2) and abundant vegetation on the banks of the rivers. To validate the
210
efficiency of aerial detection under such conditions, a flyover was performed on the estuary
211
of the Tatuamunha River (09°12’83.00”S/35°16’11.29”W), where three manatees are kept
212
in natural captivity (1050 m²) and none were sighted from the airplane (Fig. 4). However,
213
manatees were sighted at the mouths of the Tatuamunha and Camaragibe Rivers
214
(09°18’30.37”S/35°23’42.19”W) (Fig. 2).
215
Figure 4 – Aerial photo of validation of viability of aerial survey of estuaries performed in
216
natural captivity of three Antillean manatees in estuary of Tatuamunha River, Alagoas;
217
Image reveals non-viability of visual detection due to high water turbidity.
218
219
All dolphins sighted belonged to the family Delphinidae, with only one group of seven
220
individuals at Peroba Beach (0858'17''S/3509'18''W) identified as S. guianensis. The social
221
structure of the delphinids was predominantly gregarious, with groups of three to seven
222
animals. Sea turtles, represented by the family Chellonidae, were the second most
223
abundant taxon (Table 1), with groups of up to four specimens detected.
21
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
224
The clinometer readings regarding the some sightings determined the following angles: 30,
225
40, 45, 50, 55 and 65. Considering the constant altitude of the flight (150 m) and the
226
largest angle (65), the scanning areas per researcher totalized 321.7 m, with 634.4 m of
227
area covered (Fig. 5).
228
Figure 5 – Schematic of strip transect sampling method from aircraft indicating constant
229
altitude, maximum sighting angle and length of base scanned (tread area) by each
230
observer.
231
232
Three small methodological adjustments were necessary: (1) reduction of the open angle
233
of the transects to 40° to increase the sampling area, (2) standardization of the transect
234
lines to 1.5 nautical miles from the coast, corresponding to 2778 km (isobaths of 10 to 20
235
m), due to the considerable variation in the continental shelf in the area, and (3)
236
replacement of the transects in estuaries with only a scan of the mouths of rivers, due the
237
transparency bad this water in comparison with the sea coast water.
238
239
240
22
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
241
DISCUSSION
242
This pilot aerial study on the northern coast of the state of Alagoas for detection of marine
243
megafauna attained satisfactory results regarding the flying and environmental conditions,
244
except in water turbid estuaries where the transparency of the water was crucial for the
245
successful detection of manatees. In contrast, COSTA (2006) reported methodological
246
inefficacy regarding the identification and quantification of manatees to the east of the state
247
of Ceará due to the turbidity of the sea water. In the present study, meteorological and
248
environmental variables exerted a positive influence on the sighting of the animals and such
249
favorable variables may be considered a priority to the feasibility of this type of survey in
250
the Brazilian northeast coast.
251
The methodological inefficacy regarding the identification of species of dolphins (uncertainly
252
of 65% sightings) and sea turtles, even in transparent waters, may be related to the agile
253
movements of the animals, at the water surface and the speed of the aircraft, which did not
254
allow ample time for the diagnosis of the specimens. The little experience of the observers
255
in aerial record type may also have influenced in the diagnosis of the species. The
256
uncertainty in the identification of delfinids is due to the fact that the species are
257
differentiated by slight variations in coloration, morphology and behavioral patterns
258
(JEFFERSON; LEATHERWOOD; WEBBER, 1993). The Guiana dolphin was identified due to
259
the grayish coloration of the dorsum and the triangular shape of the dorsal fin (JEFFERSON
260
et al., 1993).
261
Difficulties identifying sea turtles are also reported in previous studies, with the small size of
262
the animals the most aggravating factor (EPPERLY; BRAUN; CHESTER, 1995; WYNEKEN,
263
2001; ROOS et al., 2005). A size threshold of approximately 75 cm in carapace length has
264
been stipulated for optimal aerial detection (SHOOP; KENNEY, 1992). Moreover, fleeing
265
behavior was recorded due to the noise of the aircraft, characterized by ripples caused on
266
the surface of the water due to the rapid diving of the turtles. According to MCCLELLAN
267
(1996), helicopters are more indicated for the identification of species in aerial surveys due
268
to the lesser flight velocity. However, a comparative study found that the noise produced by
23
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
269
such aircraft scare marine animals off more than a single-engine high-wing plane
270
(RATHBUN, 1988), as the one used in the present study.
271
The essentially solitary habits and subtle exposure at the water surface (HARTMAN, 1979)
272
may exert a negative influence on the detection of manatees in turbid waters. Antillean
273
manatees are difficult to sight due to the fact that these animals spent a large amount of
274
time under water (REYNOLDS; POWELL 2002) and are therefore more easily detected when
275
in groups, although the precise count of individuals is more difficult (LANGTIMM et al.,
276
2011). Aerial surveys were used in Florida to estimate the quantity of Trichechus manatus
277
latirostris (HARLAN, 1824) in the region. This was done during periods of cold weather, as
278
the manatees gather in areas of warm water, which this facilitated counting the animals
279
(ACKERMAN, 1995; LEFEBVRE et al., 2001). In Brazil, the constant temperature of the
280
coastal waters turns this type of procedure unnecessary (LIMA et al., 2011).
281
Besides biological traits, degrees of turbidity and tide conditions may lead to detection
282
errors, especially with regard to T. m. manatus and sea turtles. At low tide, rocky outcrops
283
and reefs may be confused for these animals due to the similar color (ROOS et al., 2005).
284
Therefore, flyovers during the rising tide, when these formations are submerged, may
285
minimize this type of error. Moreover, the access of manatees to estuaries is facilitated,
286
thereby allowing a greater chance of sighting these animals. Aerial surveys within estuaries
287
are inefficacious due to frequent turns and circuitous flight, path required to sample the
288
irregular-shaped estuarine water bodies, and mainly to the turbidity of the water. This
289
irregular-shaped turns difficult to consistently maintain a formal transect protocol
290
(LANGTIMM et al., 2011). However, there is a considerable need to monitor species that use
291
these ecosystems, such as T. m. manatus (LIMA et al., 2011). The use of side-scan sonar in
292
nautical studies is favorable to the detection of manatees in this type of environment
293
(GONZALEZ-SOCOLOSKE; OLIVERA-GÓMEZ; FORD, 2009).
294
The corrected methodological parameters (reduction of the transect angle, constant zigzag
295
transects of 1.5 nautical miles, and transects restricted to the mouths of estuaries) will
296
minimize the limiting effects regarding the detection of marine mammals and sea turtles
297
related mainly to the morphological and behavioral characteristics of the species in contrast
24
ALVES, M. D. O.; BORGES, J. C. G.; ARAÚJO, M. E. Pilot aerial study of the marine
megafauna in northern coast Alagoas, Brazil.
298
to the conditions of the environment. Aerial surveys can also provide information for the
299
development of management, conservation and recovery programs directed at habitats of
300
ecological importance to the survival of marine mammals and sea turtles.
301
302
ACKNOWLEDGMENTS
303
The authors are grateful to the Fundação Mamíferos Aquáticos (FMA) and the Universidade
304
Federal de Pernambuco (UFPE) for the execution of the study; the Sponsor Petrobrás
305
through the Petrobrás Environmental Program; the Brazilian fostering agency Conselho
306
Nacional de Pesquisa e Desenvolvimento (CNPq) for the doctoral grant awarded to the first
307
author; to Centro Mamíferos Aquáticos (CMA) and especially to Iran Normande researcher,
308
for support and initial participation in the study; to the Instituto Baleia Jubarte for loaning
309
the clinometers; and the team at NVO aerial taxi for adapting the aircraft with the
310
implantation of bubble windows and for the logistic adjustments of the flyovers.
311
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Chetumal Bay, Mexico. Biological Conservation, v. 95, p. 67-75, 2000.
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PARENTE, C. L.; VERGARA-PARENTE, J. E.; LIMA, R. P. Strandings of Antillean Manatees,
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452
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454
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30
Capítulo 2* - Primeira estimativa de abundância de peixe-boi antilhano (Trichechus
manatus manatus) no Brasil utilizando levantamento aéreo.
Chapter 2* - First abundance estimate of the Antillean manatee (Trichechus manatus
manatus) in Brazil using aerial survey.
* Capítulo em formato de artigo e padronizado de acordo com as normas da revista
Endangered Species Research.
1
First abundance estimate of the Antillean manatee (Trichechus manatus manatus)
2
in Brazil using aerial survey.
3
4
Abundance of the Antillean manatee in Brazil
5
6
Maria Danise de Oliveira Alves1,2*, Maria Elisabeth de Araújo1, Miriam Marmontel3,
7
João Carlos Gomes Borges2,4, Alexandra Fernandes Costa5, Paul Gerhard Kinas6
8
1
9
Department of Oceanography, UFPE, Cidade Universitária, s/n, Recife-PE, 50670-
10
901, Brazil.
2“
11
Fundação Mamíferos Aquáticos”, 17 de agosto, Casa Forte, 2001, Recife-
12
Pernambuco, 52061-540, Brazil.
3“
13
Instituto de Desenvolvimento Sustentável Mamirauá” (IDSM), Estrada do Bexiga
14
15
2.584, Bairro Fonte Boa, Tefé-Amazonas, 69470-000, Brazil.
4
Graduate Program in Tropical Animal Sciences, UFRPE, Dom Manoel Medeiros, Dois
16
17
Irmãos, s/n, Recife-PE, 52171-900, Brazil.
5
Graduate Program in Aquatic Ecology and Fishery, UFPA, Cidade Universitária,
18
19
20
Guamá-Belém-Pará, 66075-110, Brazil.
6“
Instituto de Matemática Estatística e Física”, FURG, Avenida Itália km 8, Rio
Grande-RS, 93201-900, Brazil.
21
22
*Email: [email protected]
23
24
25
31
26
ABSTRACT
27
Aerial surveys were conducted over 2590.2 km2 of the northeastern Brazilian coast
28
between January and April 2010. The objective was to estimate the abundance of
29
Antillean manatees on a large-scale study and evaluate the efficacy of the method for
30
conservation purposes. Flights were conducted at 150 m altitude and 140 km h-1 speed,
31
using two independent observers. Strip transects were flown in a zigzag pattern. A total
32
of 67 individuals (on and off effort) were recorded in 55 sightings. On effort, the highest
33
manatee density was found in Piauí state. These results were used to estimate
34
abundance, using published records of occurrence of the species in the area as
35
correction factors for the perception bias of observers. We estimated the manatee
36
population of northeastern Brazil in 1146 individuals within a Bayesian framework and
37
a weakly informative prior distribution. The wide 95% posterior probability interval
38
associated to this estimate, ranging from 610 to 1955 individuals, indicates high
39
uncertainty. However, the corresponding posterior coefficient of variation of 29% is
40
acceptable for ecological studies of this nature. Large-scale studies in the region are
41
needed to understand the population trends over the years. However, the
42
implementation of studies in small spatial scale, in hotspot areas, is necessary to reduce
43
the coefficient of variation, and may allow improved techniques for monitoring the
44
species, associated to the species-specific characteristics. The study evidenced the
45
efficacy of aerial surveys as a tool applicable to the evaluation of the present
46
conservation status of the species, considered the most endangered aquatic mammal in
47
Brazil.
48
49
KEY WORDS: Antillean manatee . population . strip transect . aerial detection
50
32
51
INTRODUCTION
52
The West Indian manatee (Trichechus manatus) is one of the four extant species
53
within the mammalian order Sirenia, being divided into two subspecies: Trichechus
54
manatus latirostris (Harlan, 1824) (Florida manatee) and Trichechus manatus manatus
55
Linnaeus, 1758 (Antillean manatee) (Hatt 1934). This species inhabits fresh, brackish
56
and marine waters in the Wider Caribbean, from Florida to the northeastern coast of
57
South America, with Antillean manatee’s distribution on the east coast of Mexico,
58
Central America, northern and northeastern South America (Lefebvre et al. 2001). The
59
species is listed by the IUCN as “endangered”, in continuing decline, with severely
60
fragmented populations (Self-Sullivan & Mignucci-Giannoni 2008).
61
Publications on T. m. manatus population estimates are sparse, and always use T. m.
62
latirostris' as a comparative parameter. Scientific papers and personal communication
63
with specialists from half of the Antillean manatee range countries report the present
64
population estimate as less than 2500 mature individuals. These data suggest a decline
65
greater than 20% over the next two generations (estimated as 40 years for an
66
unexploited population) (Self-Sullivan & Mignucci-Giannoni 2008).
67
The population decline of the Antillean manatee in Brazil initiated with the predatory
68
hunts in the past, and has been intensified by the continuous degradation of coastal and
69
estuarine environments (Domning 1982; Parente et al. 2004, Borges et al. 2007, Luna et
70
al. 2008, Meirelles 2008, Lima et al. 2011). At present the T. m. manatus is considered
71
the most endangered aquatic mammal in Brazil (ICMBio 2011). Studies in the 1990's
72
estimated the number of Antillean manatees along the northern and northeastern coasts
73
of Brazil in 485 animals, distributed in a discontinuous pattern between the states of
74
Sergipe and Amapá (Luna et al. 2008). For the northeastern region alone two abundance
75
estimates have been produced: 278 manatees (Lima 1997) and 242 speciments (Lima et
33
76
al. 2011). The methodology used in those three studies took into account the traditional
77
knowledge by fishermen, based on the maximum number of live manatees sighted by
78
each interviewee. The total sum of these national estimates resulted higher than the
79
estimate published internationally (Self-Sullivan & Mignucci-Giannoni 2008), of only
80
200 animals. Both results presented innovative information to the understanding of
81
population trends of Antillean manatee in Brazil, albeit questionable in terms of
82
methodological and statistical parameters adopted.
83
Obtaining a measure of the abundance of sirenians is essential for their conservation,
84
and the method of aerial surveys is the most suitable for monitoring manatee and
85
dugong numbers (Olivera-Gómez & Mellink 2002, 2005, Preen 2004, Edwards et al.
86
2007, Langtimm et al. 2011). In Brazil, however, only one aerial survey has been
87
conducted, with the aim of evaluating the distribution of Antillean manatees at a small
88
geographic scale in the northeastern state of Ceará (Costa 2006). Furthermore, test
89
flights were conducted by "Fundação Mamíferos Aquáticos" in the 1990's, but with
90
unpublished results (Borges, pers. comm.).
91
Aerial methods for abundance estimates are susceptible to space variation
92
(availability bias - probability of an animal being available for detection, which may be
93
highly variable in extensive and heterogeneous environments, beyond diving behavior
94
of each species) and to imperfect detectability (perception bias - probability of an
95
animal being detected, assuming it is available for observation) (Pollock et al. 2006,
96
Katsanevakis et al. 2012).
97
The strip transect method is widely used in aerial studies of manatees and dugongs
98
(Marsh & Sinclair 1989, Lefebvre et al. 2001, Olivera-Gómez & Mellink 2002, Easton
99
et al. 2003, Lanyon 2003, Marsh et al. 2004, Hines et al. 2005, Langtimm et al. 2011).
100
The method is recognized as being easy to apply in the field, when compared to distance
34
101
sampling, which may record imprecise perpendicular angular distances, as those are
102
simultaneous to detection and counting of animals (Marsh 1995, Miller et al. 1998,
103
Pollock et al. 2006). In addition, smaller species with subtle exposure behavior on the
104
water surface, such as manatees when compared to large whales, make distance
105
sampling even less viable (Lefebvre et al. 1995).
106
The aim of this study was to apply the strip transect aerial methodology to estimate
107
abundance of Antillean manatees in a large-scale study along the northeastern coast of
108
Brazil, to evaluate the efficacy of aerial survey as a tool in the re-evaluation of the
109
conservation status of the critically endangered populations of T. m. manatus.
110
111
MATERIALS AND METHODS
112
Study area
113
The study ranged over six Brazilian states, covering roughly 44% of the 3400 km of
114
northeastern coast. The limits of the study area were the Canárias island on the Parnaíba
115
river mouth (Piauí state) to the north, and the São Francisco river mouth (Alagoas state)
116
to the south. A stretch of only 22 km of coastline was not surveyed, due to traffic
117
restrictions around the Recife international airport, capital of Pernambuco state (Fig. 1).
118
The continental shelf of northeastern Brazil ranges in width from 85 km in the north
119
to 40 km in the southern portion. Climate is tropical, with high temperatures (>24°C)
120
(Muehe & Garcez 2005). Diversity in the coastal and estuarine environments includes
121
beaches, dunes, coral reefs, mangrove forests and seagrass beds (Kempf et al. 1970,
122
Oliveira-Filho et al. 1983, Castro & Pires 2001), all of which are vulnerable to
123
anthropogenic actions, especially urban development, tourism and fisheries (Cunha
124
2005).
125
35
126
127
Fig. 1. Study area between the states of Piauí and Alagoas, northeastern Brazil (A).
128
Aerial transects in a zigzag pattern in the estuarine mouth Delta do Rio Parnaíba (B).
129
130
Aerial surveys
131
Aerial surveys were conducted using a single-engine high-wing Cessna 172 A
132
aircraft, to facilitate viewing the sea surface, and adapted with bubble windows at the
133
rear (Zerbini et al. 2011), allowing a wider viewing angle. The team was composed by
134
two independent observers (Langtimm et al. 2011), positioned by each of the side
135
windows, wearing polarized sunglasses to minimize perception bias; and a registrar, in
36
136
the front beside the pilot (Morales-Vela et al. 2000). Two observers were already
137
experienced in manatee observation; however all observers were trained during a test
138
flight (Alves et al. 2013a) to help reduce detection bias of animals. The registrar used a
139
global positioning system (GPS) to indicate all sighting points (latitude and longitude
140
positions), in addition to the GPS of the plane, which recorded the aerial routes. The
141
registrar also used nautical charts (1:300.000), two photographic cameras, and a
142
portable recorder to compile the field records.
143
Aerial sampling was performed using the strip transect method, a type of line
144
transect sampling which consists of a random sampling of a known fraction of the total
145
study area and assuming that all animals within the searched strip are detected and
146
counted (Jolly 1969). Transects were made in a zigzag pattern, perpendicular to the
147
coast (Morales-Vela et al. 2000, Hines et al. 2005) (Fig. 1), with an angle of turn of 40°,
148
as to better cover the area and to maximize the flying effort. The surveyed areas
149
extended from estuarine inlets (Fig. 1) (Langtimm et al. 2011), to the isobaths of 10 to
150
20 m. The flight was standardized with 150 m altitude and 140 km h-1 speed, minimum
151
values for flight safety, and within the range found in other aerial surveys (Morales-
152
Vela et al. 2000, Easton et al 2003, Olivera-Gómez & Mellink 2005, Costa 2006,
153
Langtimm et al. 2011). The widest sighting angle (approximately 65o) was determined
154
with a clinometer during a test flight, and resulted in an accurate area of 321.7 m per
155
observer (i.e. a total strip width 643.4 m) (Alves et al. 2013a). A variable effort recount
156
method (Lefebvre & Kochman, 1991) was applied in cases of doubtful sightings or
157
imprecise specimen counts, consisting of a circular flight around the sighting point out
158
to confirm identification (Lefebvre et al. 1995, Morales-Vela et al. 2000, Langtimm et
159
al. 2011); unconfirmed sightings were discarded. Calves corresponded to specimens
37
160
measuring up to 1/3 of the adult size (Hartman 1979). Two or more animals were
161
defined as a group (Morales-Vela et al. 2000).
162
Aerial surveys were conducted in dry season, period of mild winds and greater water
163
transparency, morning period to avoid glare and to take advantage of generally light
164
winds, and high tide when the animals have a better access to shallow foraging areas
165
(macroalgal banks and seagrass beds) and estuaries (Paludo & Langguth 2002, Lanyon
166
2003, Hines et al. 2005, Olivera-Gómez & Mellink 2005, Langtimm et al. 2011), and to
167
reduce the potentially confusing effect of reefs and algae sandstone substrates that
168
appear at low tide (Costa 2006). Flights were conducted when weather conditions were
169
excellent, with Beaufort Sea state 2 or less, and absence of rain or mist (Lanyon 2003,
170
Preen 2004).
171
According to water transparency conditions, manatee sighting classes were defined
172
as: 1 - excellent: manatees clearly visible, even when submerged; 2 - good: manatees
173
visible when close to the water surface; 3 - medium: manatees visible only if exposed a
174
small part of the body on water surface (eg.: rostrum or caudal fin); and 4 - poor:
175
manatees visible only if almost completely exposed on water surface. The classification
176
“terrible” corresponds to high water turbidity found inside estuaries, with impossibility
177
of recording under such conditions (Alves et al. 2013a). Therefore to minimize
178
availability bias, estuaries were excluded from sampling, despite representing an
179
environment widely used by the species (Lima et al. 2011).
180
Aerial surveys were carried out between January and April 2010. The total coverage
181
area was 2590.2 km2, calculated by strip transect width (643.4 m) and total linear
182
distance traveled in zigzag. Each flight lasted for less than three hours per day. The
183
effective effort exceeded 27 flight hours in 11 days.
184
38
185
Abundance estimate - structure data and statistical analysis
186
Antillean manatee distribution data and aerial route maps were produced using
187
ArcMap software (version 10.0), for later production of digital maps and statistical
188
analysis of manatees' abundance estimate.
189
For estimation of the manatees number a Bayesian approach was used. Description
190
of the statistical model used the following notation: i - region identifier index (i = 1, 2...
191
899), defined by sampling units of zig (coast - sea transect) and zag (sea - coast transect)
192
coverage in m2; Ai - total area of region i; ai - area tracked by the observers in region i
193
(ai < Ai); yi – number of manatees sighted on effort in area ai; zi – subjectively imputed
194
occurence probability for region i, based on a priori records of sightings or strandings
195
(Albuquerque & Marcovaldi 1982, Parente et al. 2004, Costa 2006, Alves 2007, Luna et
196
al. 2008, Meirelles 2008, Lima et al. 2011), or observed individuals off effort (Fig. 2,
197
Table 1).
198
199
Fig. 2. Figure representing parameters of statistical model used to analyze sightings of
200
manatees (manatee drawing): i – identifier index of sampling units (numbers); Ai – total
201
area (rectangular spotted polygon), and ai – area tracked by observers (wavy band).
202
39
203
Table 1. Criteria to determine occurrence probabilities (z values) relative to occurrence
204
of Antillean manatee in sampling units in northeastern Brazil.
zi Value
Definition of values according to sampling unit
“Aerial detection” of manatee on or off sampling effort.
1
0.8
“High probability” of manatee occurrence, according to recent
historical records and/or appropriate environmental features.
0.5
“Dubious probability” of manatee occurrence, according to past
historical records and/or absence of updated information.
0.2
“Low probability” of manatee occurrence, with absence of historical
records and/or inappropriate environmental features.
205
206
Latent variables and unknown model parameters were as follows: wi – latent variable
207
indicative of occurrence (wi = 1) or absence (wi = 0) of manatee in region i; p –
208
probability to detect a manatee in area ai at the time of sampling; µ – expected number
209
of manatee per unit of area (i.e. density); Ni – total number of manatee in region i.
∑
210
211
212
213
∑
, manatee abundance in the region covered by the study (i.e. in area
).
The hierarchical structure of the model starts by the Bernoulli distribution for the
occurrence of manatee in a given region i, with imputed probability
.
( )
214
215
The number of manatees in region i is modeled by a Poisson distribution with mean
conditional on manatee density (µ), area ( ) and occurrence (
(
).
)
216
Given the latent number of manatees ( ), the model to describe the number of
217
detected individuals is Binomial with detection probability p times the availability
218
probability
.
(
)
40
219
Parameters to be estimated from this model are p, µ and total abundance N. The
220
Bayesian estimation procedure (McCarthy 2007, Kinas & Andrade 2010) was chosen,
221
for two reasons: (a) convenience of using this procedure in the case of a hierarchical
222
model with a large number of latent variables and, consequently, a similarity function
223
very complex to obtain estimates of maximum similarity and their approximate standard
224
errors; (b) the possibility to incorporate informative prioris that reflect the already
225
available ecological knowledge and may compensate for the insufficient amount of data.
226
Extra-data information was incorporated in two ways: by means of the zi variable
227
that describes the probability of occurrence of manatees in the regions, and by means of
228
prioris distributions partially informative for p (probability of effective detection of
229
manatee) and μ (mean density of manatee per km2). These information proved to be
230
particularly useful in the study due to the reduced number of sightings, which rendered
231
the flight data, in isolation, little informative to estimate p and μ simultaneously. The
232
used prioris were:
(
( )
233
(
)
(
)
)
with N (a, b) indicating a Gaussian distribution with mean a and standard deviation b.
234
The posterior probability distributions were obtained by stochastic simulation using
235
the Monte Carlo method via Markov Chains (MCMC), with three chains in parallel and
236
retaining 3 x 5000 = 15000 final values. The program OpenBUGS (via R libraries
237
BRugs and R2WinBUGS) conducted the simulations (Thomas et al. 2006, R
238
Development Core Team 2008).
239
240
241
41
242
RESULTS
243
Sightings of Antillean manatee
244
The aerial methodology proved efficient for studies of population estimates of
245
Antillean manatee under conditions found in northeastern Brazil. Efforts to recount
246
manatees were necessary in four occasions only, with success in identification in three
247
of those. Thirty-six sightings and 41 individuals were recorded on effort, with only one
248
calf in Barreta beach (6° 6' S, 35° 4' W), Rio Grande do Norte state; 19 sightings and 26
249
specimens were recorded off record (i.e. off the transect area), also with only one calf in
250
Coqueirinho beach (7° 26' S, 34° 45' W), Paraíba state (Fig. 3).
251
Manatees occurred between the Miaí de Baixo beach (10° 14' S, 36° 12' W) in
252
Alagoas state, and the estuarine mouth Delta do Rio Parnaíba in Piauí state (2° 44' S,
253
41° 47 W). Despite the lack of sightings along large areas in the coasts of Pernambuco,
254
Rio Grande do Norte and Ceará states, aerial survey results expanded the species'
255
known area of distribution, which now includes the Iguape beach, Ceará (3° 54' S, 38°
256
17' W), and Miaí de Baixo beach, in the southernmost portion of Alagoas (Fig. 3).
257
258
259
260
261
42
262
263
Fig. 3. Manatee sightings between Piauí and Alagoas states, during on effort (manatee
264
drawings) and off effort (red circle) periods.
265
266
On effort manatee relative density was 0.24/km of coast, and 0.05/km2, considering
267
the distance of 10 and 20 m isobaths of approximately 5 km offshore. On effort, the
268
Antillean manatee density was at its highest in Piauí state, with five animals found in
269
the estuarine complex of the rivers Timonha/Ubatuba and Cardoso/Camurupim
270
(between 2° 54' S, 41° 22' W and 2° 53' S, 41° 29' W). The highest sighting numbers
271
and total manatee abundance on and off effort were obtained for Rio Grande do Norte
272
and Paraíba states, respectively (Table 2).
43
273
Table 2. Occurrence of manatees on and off effort, and the demographic density by
274
stretch of coast (DC = org/km) and area (DA* = org/km2) for each state.
Manatees on effort
States
Area
(shoreline)
Manatees off effort
Sightings Abundance Sightings Abundance
Demographic density
Coast
Area*
(org/km) (org/km2)
Piauí
57.44
5
6
0
0
0.1
0.0209
Ceará
531.18
5
5
2
2
0.01
0.0019
Rio Grande
do Norte
374.01
9
12
2
2
0.03
0.0064
123
8
8
8
11
0.06
0.013
Pernambuco
158.15
6
6
1
1
0.03
0.0076
Alagoas
226.88
3
4
6
10
0.01
0.0035
Total
1470.66
36
41
19
26
0.24
0.0533
Paraíba
275 *Demographic density by area calculated based on distance of 5 km from coast
276
277
The error source of availability bias was considerably limiting to animal detection,
278
due to the environmental variation along the extensive coastal area, associated to T. m.
279
manatus morphological and behavioral characteristics, such as predominantly solitary
280
habit (64.18% on and off effort), little exposure on the water surface, and cryptic
281
coloration in turbid estuarine waters and sandstone substrate.
282
Wind conditions during on effort manatee sightings were in accordance with
283
proposed parameters, in levels between 0 and 2, with 52.78% (n = 19) of sightings in
284
level 1. The sampled area was qualitatively characterized as "good" and "medium"
285
transparency, with type "poor" being described for turbid waters close to estuarine
286
mouths and “excellent” predominant between coasts with coral reef formation of the
287
southern Pernambuco and north of Alagoas states. Most of the 67 sighted manatees
44
288
were detected under "good" conditions (40.3%; n = 27), followed by "medium"
289
(26.86%; n = 18), "excellent" (20.9%; n = 14) and "poor" (11.94%; n = 8) (Fig. 4).
290
Fig. 4. Manatee sightings (black circles) under different scales of visibility, during aerial
291
surveys in northeastern Brazil: (1) Excellent – two manatees submerged in a seagrass
292
bed, Quitéria's beach (4° 40' S, 37° 18' W) in Ceará state (2); Good – one manatee close
293
to the water surface, Pirangi do Sul beach (5° 58' S, 35° 6' W) in Rio Grande do Norte
294
state; (3) Medium – two manatees, with one identified only because of the rostrum
295
emergence in the water (black arrow), Oiteiro beach (6° 51' S, 34° 53' W) in Paraíba
296
state; and (4) Poor – one manatee visible after almost total body exposure on water
297
surface, estuarine mouth in Guajú River (6° 29' S, 34° 57' W) in Rio Grande do Norte
298
state.
299
300
301
45
302
Abundance estimate
303
The logit distribution for p assumes a priori uncertainty for which the 5%, 50% and
304
95% quantiles correspond to p values of 0.020, 0.099 e 0.362, respectively. In addition,
305
the probability that p > 0.4 equals 0.0346, i.e. we consider this possibility small, albeit
306
possible. The a priori distribution of p follows the figure below (Fig. 5).
307
308
Fig. 5. A priori (dotted line) and posterior (continuous line) distribution for the
309
probability of p detection.
310
311
In a similar way, the natural logarithm for µ assumes a priori uncertainties for which
312
the 5%, 50% and 95% quantiles correspond to values of μ 0.018, 0.301 and 0.501,
313
respectively. Furthermore, the probability of μ > 0.6 equals 0.0137. The a priori
314
distribution of μ is represented in Figure 6.
46
315
316
Fig. 6. A priori (dotted line) and posterior (continuous line) distribution for the density
317
of individuals μ.
318
319
This a priori distribution, relatively informative for μ, corresponds to the statement
320
that the total manatee abundance in the study region is lower than 3400 individuals with
321
95% probability. Nevertheless, it leaves open (5%) the possibility of values above 3400
322
if the adjustment of the model to the data suggested so.
323
Manatee sightings occurred in only 52 sampling units of the 899 defined regions. In
324
18 of them, sightings occurred off effort (a) and therefore have values y = zero (but with
325
value z = 1) and summed 26 individuals, in 19 sightings. In the 34 regions where
326
sightings occurred "on effort", these summed 41 individuals, in 36 sighting events. The
327
remainder regions only had the value y = 0 (no sightings) (Table 3), qualified by the
328
occurrence probability (z) (Table 1).
329
330
331
332
47
333
Table 3. Distribution of 899 regions according to probability of manatee occurrence (z)
334
and number of sighted individuals "on effort" (Y).
335
Y
336
z
337
338
339
340
0
1
2
0.2
146
0
0
0.5
85
0
0
0.8
617
0
0
1.0
18
27
7
341
342
343
344
The posterior distribution for abundance N is represented by the histogram below
(Fig. 7).
345
346
Fig. 7. Posterior distribution of manatee abundance (N) in the study area.
48
347
In comparison with the a priori probability attributed to abundance, the a posteriori
348
probability that N be larger than 3400 is practically null. In other words, the 95%
349
quantile that inicially was 3400 is reduced a posteriori, to approximately half, or 1752.
350
The statistical summary of the marginal posterior distributions of the three parameters
351
of interest is shown below (Table 4).
352
353
Table 4. Statistical summaries of posterior distributions of main parameters (2.5% and
354
97.5% quantile delimit the 95% creditability intervals; "Mean" corresponds to the
355
specific estimate in the study).
Parameter
2.5%
Median
97.5%
Mean
SD
p
0.050
0.092
0.177
0.098
0.033
µ
0.165
0.298
0.528
0.309
0.090
N
610
1106
1955
1146
334.2
356
357
The estimated number of manatees inhabiting the study area is 1146 individuals.
358
Nevertheless, and despite the use of a prioris distribution, which are partially
359
informative, the results presented a considerable level of uncertainty, represented by the
360
posterior coefficient of variation of 29% and the 95% probability interval ranging from
361
610 to 1955 individuals.
362
363
DISCUSSION
364
Antillean manatee distribution
365
The data generated on Antillean manatee distribution in northeastern Brazil were
366
similar to historical records of the species' occurrence (Albuquerque & Marcovaldi
367
1982, Parente et al. 2004, Costa 2006, Alves 2007, Luna et al. 2008, Meirelles 2008,
368
Lima et al. 2011). However, the expansion of the area of use of the species could be
49
369
related, the implementation of conservation measures in the 1980s (Luna et al. op. cit.)
370
and the current translocation of captive specimens in the northern portion of the state of
371
Alagoas (Lima 2008).
372
High densities of dugongs, up to 7.25/km2 in Australia, have been recorded in
373
specific foraging areas, with several individuals sharing a limited space (Lanyon 2003).
374
The apparent discontinuity of sightings and the low relative density of manatees, of only
375
0.05/km2, may indicate the existence of reduced and fragmented populations along the
376
Brazilian northeastern coast (Albuquerque & Marcovaldi 1982, Lima et al. 2011, Alves
377
et al. 2013b), with an index lower than those found in other studies with sirenians,
378
which vary between 0.075 and 0.240/km2 (Preen et al. 1997, Morales-Vela & Olivera-
379
Gómez 1994, Olivera-Gómez & Mellink 2002, Preen 2004). The sightings discontinuity
380
in the states of Pernambuco, Rio Grande do Norte and Ceará may be related to the
381
natural lack of natural resources essential to the species such as abundant aquatic
382
vegetation but, mainly, to the degradation of coastal and estuarine habitats due to human
383
development (Lima et al. 2011, Alves et al. 2013b), causing the animals to search for
384
less impacted areas.
385
The greatest demographic density of this species found on the Piauí coast can be
386
directly linked to the presence of a collection of islands interspersed with estuaries and
387
preserved bays, within the Environmental Protection Area of the Parnaíba Delta
388
(IBAMA 1998). The estuarine complex of the rivers Timonha/Ubatuba and
389
Cardoso/Camurupim, where were sighted five animals, as well as the adjacent coastal
390
zone is considered to be an important niche for the species, with seagrass beds,
391
freshwater sources and excellent parenting locations (Choi et al. 2009). Recorded
392
sighting of only one animal, at approximately 40 km distance of the other five sightings,
393
was localized in Canárias Island estuarine mouth. This discontinuity of sightings could
50
394
be directly linked to the presence of the Luís Correia seaport (2° 51' S, 41° 38' W) in the
395
estuary of the Parnaíba River, with intense vessel traffic, rendering this area inaccessible
396
for animals. These human activities, associated to manatees' costal habit, potentiate
397
risks of collision and accidental captures, (Borges et al. 2007, Meirelles 2008, Alves et
398
al. 2013b), probably forcing animals to find new habitats (Reynolds & Szelistowski
399
1995, Alves 2007).
400
The susceptibility to errors in abundance estimates, common in aerial surveys, may
401
have influenced the few sighting records of this study. The great extension of coastal
402
area surveyed, with a wide variety of environments and sea states (e.g. coastal
403
morphology and water turbidity), associated to characteristics of the species (shy
404
behavior during exposure on water surface, cryptic morphology and solitary habit) may
405
have affected the detection probability by the observers, generating imperfect or
406
heterogeneous detection of individuals, defined by the variable proportion of animals
407
present in a given area, and yet not sighted (Katsanevakis et al. 2012).
408
The excellent transparency level of waters on the northern coast of Alagoas was
409
similar to that found by, Alves et al (2013a), highlighting the favorable conditions for
410
aerial detection of manatees in this area. However, the low manatee abundance under
411
"excellent" and "poor" conditions may suggest an underestimation in more turbid
412
waters: these situations do not provide the ideal conditions for detection of individuals,
413
and yet are associated to proximity with estuaries, habitats with high water turbidity it
414
impossible this detection (Alves et al. 2013a). The estuaries are highly favorable
415
environments to the occurrence of the species, for both feeding, reproduction and
416
resting (Olivera-Gómez & Mellink 2005, Lima et al. 2011), although many estuaries
417
find themselves silted (Alves et al. 2013b), making them inaccessible and causing
418
strandings, especially of calves (Parente et al. 2004, Meirelles 2008).
51
419
The water transparency is a key factor in abundance estimates (Marsh & Sinclair
420
1989, Ackerman 1995), and may negatively influence the availability bias when it is
421
very variable (Hines et al. 2005, Pollock et al. 2006). During periods of cold weather in
422
Florida, aerial surveys uncovered large groups of manatees in areas of warm and
423
transparent water, which facilitated the counting (Edwards et al. 2007). The detection of
424
aquatic fauna (especially those cryptic, shy species with essentially solitary habit) is
425
particularly hampered in turbid waters of estuaries, lakes and rivers (Reynolds & Powell
426
2002). In eastern Ceará, where water transparency categories ranged from "excellent" to
427
"regular", nautical monitoring of manatees was more effective than aerial surveys,
428
(Costa 2006). An alternative for sampling in turbid waters would be the use of nautical
429
surveys using side-scan sonar, allegedly efficient in acoustic detection of manatees in
430
limited and turbid waters of Mexico and Florida (Gonzalez-Socoloske et al. 2009,
431
Gonzalez-Sololoske & Olivera-Gómez 2012).
432
433
Antillean manatee abundance estimate
434
The abundance estimate of 1146 manatees along approximately 1500 km of coastline
435
suggests a reduced population index for an important large area of occurrence of T. m.
436
manatus in Brazil. Although this number is higher than the estimated abundance of
437
manatees between the states of Piauí and Sergipe, with only 242 (Lima et al. 2011) or
438
278 animals (Lima 1997), one cannot say that there was an increase in manatee
439
population, in the region from the 1990s until the present time, due to different
440
methodologies employed.
441
This result does not correspond to a precise estimate of the number of animals, but to an
442
estimate of a minimum abundance, which highlights the conservationist character of the
443
information. These data will represent a baseline for future studies of evaluation of
52
444
distribution and population trends of the species (Ackerman 1995, Lefebvre et al. 1995,
445
Miller et al. 1998, Olivera-Gómez & Mellink 2002, Katsanevakis et al. 2012),
446
suggesting the need of directing new efforts in the same area sampled and/or smaller
447
scale for improvement of the methodology.
448
The only aerial study conducted in the Brazilian northeast so far, in a restricted area
449
of only 50 km of coast in Ceará state, generated errors associated to the water turbidity
450
and difficulty of identification and counting of manatees (Costa 2006). These errors
451
were possibly increased, respectively, by the inappropriate sampling period (winter) and
452
the flight design (e.g. reduced sampling effort due to transect parallel to the coast, and
453
absence of bubble windows). Among the recommendations for improvement, Costa (op.
454
cit.) proposed the need of application of aerial methodologies in other areas, with the
455
aim of future systematic monitoring of the species, objective attained in the present
456
study.
457
Based on the ideal figure for the coefficient of variation less than 20% (Hines et al
458
2005, Marsh et al. 2005), the value of 29% suggest a considerable level of uncertainty
459
in the abundance estimate of manatees in this study. Nevertheless, values above the
460
ideal are commonly recorded in aerial surveys for sirenian estimates, related mainly to
461
monitoring habitats with turbid waters, such as Chetumal Bay, in Mexico, with
462
percentages 21-70.3% (Morales-Vela et al. 2000) and 34.4-65.5% (Olivera-Gómez &
463
Mellink 2002), in the Andaman coast, in Thailand, with 33.4% (Hines et al. 2005), and
464
in Porto Rico, with 55.8% (Powell et al. 1981). Large-scale studies in the region are
465
needed to understand the population trends over the years. However refinements of the
466
aerial methodology in small spatial scales are necessary to reduce the coefficient of
467
variation, in order to avoid sources of error of perception and availability biases (Marsh
468
& Sinclair 1989, Marsh 1995). Other methodologies must also be adapted for
53
469
population manatees estimates, such as nautical surveys using side-scan sonar
470
(Gonzalez-Socoloske et al. 2009, Gonzalez-Sololoske & Olivera-Gómez 2012). This
471
method is presently being used in Brazil in Amazonian (Trichechus inunguis)
472
(Marmontel pers. comm.) and Antillean (Choi pers. comm.) manatee research.
473
The implementation of distribution and abundance studies of Antillean manatee at
474
appropriate scales, in northeastern Brazil, is hereby recommended to allow the
475
implantation of efficient management strategies for the protection of the species,
476
notwithstanding logistic difficulties and high financial cost. The identification, at a local
477
scale, of manatee and dugong abundance hotspots areas is favorably used in population
478
surveys and analyses of conservation status, mainly through aerial surveys (Rajamani &
479
Marsh 2010, Lanyon 2003, Castelblanco-Martínez 2012). Based on the results of the
480
present study, we suggest as some of the main hotspots for future aerial surveys along
481
the Brazilian northeastern region: the coast of Piauí, the state which presents the largest
482
density of individuals; the easternmost portion of Ceará, an important area in terms of
483
manatee calf strandings (Parente et al. 2004, Meirelles 2008); areas along the
484
southwestern coast of Rio Grande do Norte state; the whole state of Paraíba, particularly
485
the Barra de Mamanguape Area of Environmental Protection, with a past record of up to
486
15 individuals (Albuquerque & Marcovaldi 1982), and traditional area of release area of
487
captive animals (Lima 2008); northernmost portion of Pernambuco, which contains
488
extensive seagrass beds (Magalhães & Cazuza 2005); and northern Alagoas, present
489
area of reintroduction of captive animals (Lima op. cit).
490
491
492
493
54
494
CONCLUSION AND IMPLICATIONS FOR CONSERVATION
495
The results of this survey highlight its importance for the conservation of this
496
endangered species, being an essential tool for future studies on large-scale in the
497
country, to the understanding of the population trends over the years. The
498
implementation of studies in small spatial scale may allow improved techniques for
499
monitoring the species, with better knowledge of their occurrence.
500
The statistical arrangement applied, using bibliographic data and sightings from
501
aerial surveys, was applied due to the difficulty of sampling a dispersed population over
502
a large area, rendering the analysis of abundance estimate susceptible to errors. In this
503
case, future efforts are needed, where individuals may be detected and counted. The
504
application of statistical and methodological models specific at the local level also will
505
allow, in the future, the compilation of data for the whole study region, according to
506
existing environmental particularities, refining the abundance estimates. This will
507
generate consistent population trends, with the identification of a probable population
508
decline or increase, according to conservation actions developed for the protection of
509
the species.
510
511
Acknowledgements
512
The authors would like to thank the Federal University of Pernambuco (UFPE) and
513
the “Fundação Mamíferos Aquáticos” (FMA) for supporting the survey; “Petrobras
514
Petróleo Brasileiro S.A.” through its “Programa Petrobras Ambiental” for sponsoring
515
the aerial surveys; “Conselho Nacional de Desenvolvimento Científico e Tecnológico”
516
(CNPq) for the doctoral scholarship granted to the first author; the “Centro Mamíferos
517
Aquáticos” (CMA) for initially supporting the research; and the NVO air taxi team for
55
518
adapting their plane to carry out the aerial survey and logistics of flights. This study is
519
part of the doctoral thesis of the first author.
520
521
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63
Capítulo 3*† - Pesquisa aérea de peixes-bois, golfinhos e tartarugas marinhas no
nordeste do Brasil: correlação com as feições costeiras e as atividades humanas.
Chapter
3*†
-
Aerial
survey
of
manatees,
dolphins
and
sea
turtles
off northeastern Brazil: correlations with coastal features and human activities.
* Capítulo em formato de artigo e padronizado de acordo com as normas da revista
Biological Conservation.
† Artigo aceito na revista Biological Conservation (Apêndice)
1
Aerial survey of manatees, dolphins and sea turtles
2
off northeastern Brazil: Correlations with coastal features and human activities.
3
4
Maria Danise de Oliveira Alvesa,b*, Ralf Schwambornc, João Carlos Gomes Borgesb,d,
5
Miriam Marmontele, Alexandra Fernandes Costaf, Carlos Augusto França Schettinia,
6
Maria Elisabeth de Araújoa.
7
a
8
Universitária, s/n, Recife-PE, 50670-901, Brazil. E-mail addresses:
9
[email protected], [email protected], [email protected]
10
Department of Oceanography, Federal University of Pernambuco (UFPE), Cidade
b“
Fundação Mamíferos Aquáticos” (FMA), 17 de agosto, Casa Forte, 2001, Recife-
11
Pernambuco, 52061-540, Brazil. [email protected]
12
c
13
Brazil. E-mail address: [email protected]
14
d
15
Pernambuco (UFRPE), Dom Manoel Medeiros, Dois Irmãos, s/n, Recife-PE, 52171-
16
900, Brazil.
17
Department of Zoology, UFPE, Cidade Universitária, s/n, Recife-PE, 50670-901,
Post-graduation Program in Tropical Animal Sciences, Federal Rural University of
e“
Instituto de Desenvolvimento Sustentável Mamirauá” (IDSM), Estrada do Bexiga
18
2.584, Bairro Fonte Boa, Tefé-Amazonas, 69470-000, Brazil. E-mail address:
19
[email protected]
20
f
21
(UFPA), Cidade Universitária, José Silveira Neto, Rua Augusto Corrêa 01, Guamá-
22
Belém-Pará, 66075-110, Brazil. E-mail address: [email protected]
Post-graduation Program in Aquatic Ecology and Fishery, Federal University of Pará
23
24
Corresponding author: Departamento de Oceanografia-UFPE, Cidade Universitária, s/n, Recife-PE,
25
50670-901, Brazil. Tel.: +55-81-96851342. E-mail address: [email protected] (Alves, M.D.O).
64
26
Abstract
27
The objective of the present study was to analyze the distribution of manatees, dolphins
28
and sea turtles off northeastern Brazil through aerial surveys, relating them to specific
29
habitats and human activities, with emphasis on marine protected areas (MPAs).
30
Surveys were conducted between January and April 2010 at 150 m altitude and 140 km
31
h-1, using two independent observers. Strip transects were flown in a zigzag pattern.
32
Transects covered 4026 km in more than 27 flight hours. A total of 36 sightings of
33
manatees (Trichechus manatus manatus, 41 individuals), 28 of dolphins (Delphinidae,
34
78 individuals, including 10 Sotalia guianensis) and 256 of sea turtles (Cheloniidae, 286
35
individuals) were recorded. Manatees and sea turtles displayed solitary habits, while
36
dolphins were commonly seen in groups. Manatees were positively correlated with sea
37
turtles, probably due to their preference for sheltered shallow habitats with favorable
38
conditions for foraging and resting. Furthermore, manatees showed a positive
39
relationship with mangrove estuaries, and medium-sized coastal cities probably due to
40
the intense urban development in many estuarine areas. Manatees and sea turtles were
41
also positively correlated with boats, showing a severe threat for these species. Density
42
of manatees was significantly higher within MPAs with preserved mangrove estuaries
43
than in non-protected areas, while dolphins and sea turtles were observed in high
44
densities MPAs with coral reefs. The elevated density of these organisms shows the
45
vital importance of protecting and adequately managing unique ecosystems to ensure a
46
sustainable future for the populations of severely threatened species.
47
48
Keywords: Manatees, Dolphins, Sea turtles, Aerial surveys, Northeastern Brazil.
49
50
65
51
1. Introduction
52
Marine mammals and sea turtles are considered key organisms for marine conservation
53
in several parts of the world (Chatwin, 2007). Many populations of these animals occur
54
in coastal areas that are intensively used by local people (Ojeda-Martínez et al., 2011),
55
which make them vulnerable or threatened by extinction (IUCN, 2012). Marine
56
protected areas (MPAs) are thus essential tools to ensure the conservation of these
57
organisms and their ecosystems (Hooker and Gerber, 2004). However, the efficiency of
58
MPAs should be based on thorough surveys (Ojeda-Martínez et al., 2011), which in
59
effect, are often incipient or too small-scaled spatial (Witt et al., 2009; Panigada et al.,
60
2011; Knip et al., 2012). Large-scale studies that quantitatively determine the
61
correlations between endangered species, such as manatees, dolphins and sea turtles,
62
coastal features and human activities are rare.
63
In northeast Brazilian waters, the most important threats to coastal biodiversity are
64
fisheries and intensive urban development, thus turning this region one of the most
65
vulnerable within South America (Chatwin, 2007). The most common marine
66
mammals in the coastal zone off northeastern Brazil are the Antillean manatee
67
(Trichechus manatus manatus) (Lima et al., 2011) and 19 species of cetaceans, among
68
which the Guiana dolphin (Sotalia guianensis) is the most frequent species (Alvite et
69
al., 2004). Also, this region occur five of the seven living species of sea turtles, the
70
loggerhead (Caretta caretta), hawksbill (Eretmochelys imbricata), olive ridley
71
(Lepidochelys olivacea), leatherback (Dermochelys coriacea), and the green turtle
72
(Chelonia mydas), the most common species in Brazil (Marcovaldi and Marcovaldi,
73
1999). Antillean manatee is the most endangered aquatic mammal in Brazil (ICMBio,
74
2011), being classified internationally as "endangered" as S. guianensis is listed as "data
66
75
deficient" (IUCN, 2012). All sea turtles mentioned are under threat, D. coriacea and E.
76
imbricata being classified as “critically endangered”, C. caretta and C. mydas as
77
“endangered” and L. olivacea as “vulnerable” (IUCN, 2012).
78
Aerial surveys are considered a standard technique to assess distribution, abundance and
79
habitat characteristics of marine mammals and sea turtles worldwide (e.g. Preen, 2004;
80
Edwards et al., 2007; Certain et al., 2008; Witt et al., 2009; Jean et al., 2010; Langtimm
81
et al., 2011). In Brazil, however, few studies have been based on aerial surveys (Secchi
82
et al., 2001; Andriolo et al., 2006, 2010; Danilewicz et al., 2010; Zerbini et al., 2010,
83
2011; Wedekin, 2011). In the northeastern coast, only one single aerial survey of
84
manatees was performed on a local scale off Ceará state (Costa, 2006).
85
The objective of the present study was to quantify and analyze the large-scale spatial
86
distribution of manatees, dolphins and sea turtles off northeastern Brazil, in relation to
87
habitat characteristics, current human activities, and the importance of MPAs for the
88
conservation of these animals.
89
90
2. Material and Methods
91
2.1. Study area
92
The northern limit of the study area was the mouth of the Parnaíba River Delta, around
93
Canárias Island (02°44'S, 41°47'W), Piauí State. The southern limit was the mouth of
94
the São Francisco River (10°30'S, 36°24'W), located in Alagoas State (Fig. 1).
95
67
96
97
Fig. 1. Map of the study area between the states of Piauí and Alagoas, northeastern
98
Brazil (A) showing the main Marine Protected Areas (DP - Delta do Rio Parnaíba, RC -
99
Recifes de Corais, BM - Barra do Rio Mamanguape, CC - Costa dos Corais) and coastal
100
cities (black squares). Inlet: Aerial transects in a zigzag pattern in the marine protected
101
area Delta do Rio Parnaíba (B).
102
103
The northeastern coast of Brazil extends for approximately 3400 km and displays
104
variety of environments such as beaches, dunes, cliffs, coral reefs, mangrove estuaries,
105
and seagrass beds, each being governed by specific dynamics and anthropogenic
106
vulnerabilities (Cunha, 2005; Muehe and Garcez, 2005). The continental shelf is 85 km
107
wide in the north and narrows to 40 km in the southern part. Climate is tropical, with
68
108
high temperatures and salinities, and low concentrations of nutrients, except for
109
estuarine areas, where primary productivity and biomass are high (Muehe and Garcez,
110
2005).
111
There are four relevant Marine Protected Areas (MPAs) in this region, each with its
112
specific conservation targets: "Delta do Rio Parnaíba" (manatees, mangroves, beaches,
113
sand banks, estuaries, coastal grasslands, marshes, dunes, lakes and lagoons), "Recifes
114
de Corais" (defined around the “Parrachos de Maracajaú” offshore coral reefs), "Barra
115
do Rio Mamanguape" (manatees, mangroves, lagoons, sand banks) and "Costa dos
116
Corais", Brazil's largest MPA (manatees, coral and sandstone reefs, estuarine
117
mangroves) (Figs. 1 and 2). Their function is to protect and preserve natural resources
118
and to promote sustainable development (FAO, 2011).
119
120
2.2. Aerial surveys
121
Aerial surveys were accomplished after a pilot study (Alves et al. 2013), using a single-
122
engine Cessna 172 A aircraft with a high-wing design to facilitate viewing the sea
123
surface. It was adapted with bubble windows at the rear (Zerbini et al., 2010, 2011),
124
allowing for a wider viewing angle. Sampling was performed using the strip transect
125
method, assuming that all animals within the strip (a band of fixed width on each side of
126
the transect line) were detected and counted (Jolly, 1969). This method has been widely
127
applied for marine mammals and sea turtles (Cardona et al., 2005; Certain et al., 2008;
128
Witt et al., 2009; Langtimm et al., 2011; Katsanevakis et al., 2012).
129
A total 899 lines transects were made in a zigzag pattern, with an angle of turn of 40°,
130
as to better cover the area and to maximize the flying effort (Secchi et al., 2001;
131
Cardona et al., 2005; Andriolo et al., 2006, 2010). The surveyed areas extended from
69
132
estuarine inlets, especially aiming at sightings of manatees, to the isobaths of 10–20 m
133
(Fig. 1). The flight was standardized with 150 m altitude and 140 km h-1 speed, which is
134
within the range found in other aerial surveys (Morales-Vela et al., 2000; Olivera-
135
Gómez and Mellink, 2005; Roos et al., 2005; Costa, 2006; Langtimm et al., 2011). The
136
widest sighting angle (approximately 65º) was determined with a clinometer during a
137
test flight, and resulted in a sampled width of 321.7 m per observer (i.e., the total strip
138
width equals 643.4 m) (Alves et al., 2013). Sea conditions were Beaufort Sea state 2 or
139
less (Certain et al., 2008), characterized by flat or calm sea, and conditions of visibility
140
and water transparency between "excellent" and "average". Aerial surveys were
141
conducted during the dry season, between January and April 2010, in the morning
142
period and at high tide, when the animals have a better access to shallow foraging areas
143
such as macroalgal banks and seagrass beds (Paludo and Langguth, 2002; Olivera-
144
Gómez and Mellink, 2005), and to reduce the potentially confusing effect of reefs and
145
algae sandstone substrates that appear at low tide (Costa, 2006; Alves et al., 2013).
146
Observations were performed by two independent observers, located at each of the side
147
windows to minimize perception bias (Langtimm et al., 2011), and who were wearing
148
polarized sunglasses to minimize the effect of glare on the water surface and accentuate
149
the color gradient. A registrar, in the front beside the pilot, used a GPS to indicate
150
sighting points, in addition to the GPS of the plane, which recorded the route. The
151
registrar also used two photographic cameras, a portable recorder, and nautical charts to
152
compile the field records. Each flight lasted for less than 3 h per day.
153
All identifications were based on morphological and characteristic behavioral
154
diagnostics. Calves corresponded to specimens measuring up to 1/3 of the adult size
155
(Hartman, 1979). Two or more animals were defined as a group (Morales-Vela et al.,
70
156
2000). In cases of doubtful sightings or imprecise counts, a circular flight around the
157
sighting point was carried out to confirm identification (Morales-Vela et al., 2000;
158
Langtimm et al., 2011).
159
Approximately 1500 km of coastline were flown over in six Brazilian states, totaling
160
4026 km along the zigzag path (Fig. 1). The total coverage area was 2590.2 km2,
161
calculated as the zigzag path multiplied by the strip width (643.4 m). The effective
162
effort exceeded 27 flight hours in 11 days. A stretch of only 22 km coastline was not
163
surveyed, due to traffic restrictions around the Recife international airport (Fig. 1).
164
165
2.3. Data analysis
166
Sighting data were transferred to GIS using the Arcmap software (version 9.2) and
167
received identification numbers and coordinates. The data were plotted on nautical
168
charts (1:300.000) to obtain isobaths and maximal depths for each sighting (with tide at
169
0.0 m).
170
A descriptive analysis of the large-scale distribution patterns of marine mammals and
171
sea turtles was carried out in the different areas. The results were also used to perform
172
statistical analyses of potential relationships between the sightings of these animals,
173
human activities, and coastline features. For this purpose, the coastline under
174
investigation was divided into 294 segments of 5 km length. For each segment, seven
175
ecological and human parameters were examined. During flights, the following
176
information of occurrence records was obtained for each segment: (1) animal
177
abundance, (2) coastal zone occupation patterns (shrimp farms, salt works and ports),
178
and (3) fishing and tourism activities (trawling boats, motor boats, sail boats and rowing
179
boats). Based on cartographic and bibliographic analysis, the following were diagnosed:
71
180
(4) MPAs ("Delta do Rio Parnaíba", "Recifes de Corais", "Barra do Rio Mamanguape"
181
and “Costa dos Corais"), (5) Reefs (Northern Beach Rocks, Offshore Reef Patches,
182
Coastal Reef Lines) (Castro and Pires, 2001), (6) Estuarine mouths (complex,
183
mangrove, partially obstructed sandy barrier/small: 0.01–0.05 km, intermediate: 0.06–
184
0.1 km, large: above 0.1 km), and (7) coastal urban centers (small < 180 km2, medium-
185
sized: 180–840 km2, large > 840 km2 (IBGE, 2007).
186
Spearman rank correlation analysis (Zar, 1996) was used to test for significant
187
correlations between human activities, coastline features, MPAs, and animal abundance
188
per segment. This method of correlation analysis was chosen due to the non-linearity of
189
relationships and non-normality and heteroscedascity of most distributions. All analyses
190
were performed using the “R” language and environment at α = 0.05 (R Development
191
Core Team, 2009, version 2.9).
192
193
3. Results
194
3.1. Distribution of sightings
195
A total of 320 sightings of marine mammals and sea turtles were recorded during the
196
surveys. Of these, 36 were sightings of Antillean manatees (41 individuals), 28 were
197
sightings of dolphins (Delphinidae, 78 individuals), with 10 individuals identified as S.
198
guianensis, and 256 were sightings of sea turtles (Cheloniidae, 286 individuals) (Fig. 2
199
and Table 1). Although it was generally possible to see head, carapace and fins of turtles
200
on the surface, this was not sufficient for identification at species level. Fish were also
201
spotted occasionally, including 22 sightings of individual flying fish, seven unidentified
202
large schools, seven rays and two sharks.
72
203
Fig. 2. Spatial distribution of manatees, dolphins and sea turtles between the states of
204
Piauí and Alagoas, northeastern Brazil. Marine protected areas are indicated as gray
205
rectangles (DP: Delta do Rio Parnaíba, RC: Recifes de Corais, BM: Barra do Rio
206
Mamanguape, CC: Costa dos Corais). White rectangle: area with scarce sightings. A
207
single sighting of manatee mother and calf is highlighted in a circle, and specimens of
208
Sotalia guianensis in light blue color. Dotted lines: state borders.
209
210
Table 1. Summary of the sightings of manatees, dolphins and sea turtles during aerial
211
surveys in northeastern Brazil. N = number.
212
Manatees
Dolphins
Sea Turtles
213
Individuals
41
78
286
214
Sightings
36
28
256
Mean N / sighting
1.1
2.8
1.1
Maximum N / sighting
2
8
2
Positive segments*
29
24
127
217
Positive segments (%)*
10
8
43
218
Maximum N / segment*
3
10
10
215
216
219
*The coastline was divided into 294 segments of 5 km in length. Positive segments are those where sightings occurred.
73
220
Marine mammals and sea turtles were recorded throughout the study area, except along
221
approximately 130 km of coastline around the western portion of the state of Rio
222
Grande do Norte (Potiguar Basin), where only a single sea turtle sighting occurred (Fig.
223
2).
224
Manatees and sea turtles were most frequently observed as solitary animals (86.1% and
225
88.3%, respectively), or as groups of two adults. A pair of manatee mother and calf was
226
sighted only once, at Barreta beach (06°06'S, 35°04'W, Rio Grande do Norte). Dolphins
227
were generally found in groups (64.3%) composed of two to eight individuals (mean:
228
4.4 individuals per group) (Fig. 2, Table 1).
229
Sightings of all three taxa were concentrated within 2–10 m depth (Fig. 3). Manatees
230
were clearly concentrated in shallower areas, being most frequently sighted within 6–8
231
m depth, reaching a maximum local depth of 14.8 m. Regarding the distance from the
232
coast, manatees were also clearly concentrated in areas closest to shore, being most
233
frequently sighted at distances that ranged from only 0.01 to 3.9 km from the coast, with
234
a continuous decrease in frequency toward offshore areas. Accordingly, this species
235
showed the lowest mean distance from the coast, with only 1.2 km, as compared to
236
2.1 km for dolphins and for sea turtles. Dolphins showed maximum frequency at the 8–
237
10 m isobath, and three sightings occurred within the 16–18 m isobaths. Dolphins
238
showed a more offshore distribution (0.1–4.4 km from the coast), with higher
239
frequencies in the central part of the surveyed area, at 1.5–2.0 km from the coast.
240
Guiana dolphins were recorded between 2.1 and 9.2 m depth and between 1.6 and 3.2
241
km from the coast. The highest maximum values of depth and distance from the coast
242
were recorded for sea turtles, with 18.5 m and 5 km, respectively, with high frequencies
243
throughout the surveyed area (Figs. 2 and 3).
74
244
245
Fig. 3. Frequency histograms of depth (m) and distance from shore (km) at the sighting
246
locations for manatees (a, b), dolphins (c, d), and sea turtles (e, f) in northeastern Brazil.
247
Data are based on 27 hours of aerial surveys carried out along the northeastern Brazilian
248
coast from the states of Piauí to Alagoas.
249
250
Spearman rank correlation analysis showed that manatees were positively correlated
251
with sea turtles (p = 0.032, Table 2), while dolphins were not correlated with any of
252
these groups.
253
254
255
256
75
257
Table 2. Results of Spearman correlation analysis of sightings of manatees, dolphins,
258
sea turtles, selected coastal features and human activities, based on 27 hours of aerial
259
surveys in northeastern Brazil. Values given in the table are “p” values of the analyses
260
based on N = 294 coastal segments of 5 km in length.
Spearman correlation
Manatees
Dolphins
Sea Turtles
Manatees
-
n.s.
n.s.
Dolphins
n.s.
-
n.s.
0.032
n.s.
-
Northern Beach Rocks
0.0089
n.s.
0.0041
Offshore Reef Patches
n.s.
n.s.
0.0012
Coastal Reef Lines
n.s.
n.s.
n.s.
Estuaries (all)
n.s.
n.s.
n.s.
Small
n.s.
n.s.
n.s.
Medium
n.s.
n.s.
n.s.
Large
n.s.
0.027
n.s.
Complex
n.s.
n.s.
n.s.
Mangrove
0.027
0.023
n.s.
n.s.
n.s.
n.s.
Shrimp farms
n.s.
n.s.
n.s.
Salt works
n.s.
n.s.
n.s.
Ports
n.s.
n.s.
n.s.
Cities (all)
n.s.
n.s.
n.s.
Small
n.s.
n.s.
n.s.
0.034
n.s.
n.s.
n.s.
n.s.
n.s.
Boats (all)
n.s.
n.s.
0.030
Trawling
n.s.
n.s.
n.s.
0.011
n.s.
0.0017
Sail
n.s.
n.s.
n.s.
Rowing
n.s.
n.s.
n.s.
Sea Turtles
Reefs
Estuarine mouths
Sandy barrier
Land Use
Medium
Large
Fishing and tourism boats
Motor
261
“n.s.”: not significant at α = 0.05.
262
76
263
3.2. Correlations of coastal features and human activities
264
Spearman rank correlation analysis detected several significant correlations of coastline
265
features and human activities with the density of manatees, dolphins and sea turtles
266
(Table 2). A significant positive correlation of manatee sightings with reef habitats was
267
detected for “Northern Beach Rocks” (p = 0.0089). For sea turtles, sightings were also
268
positively correlated with “Northern Beach Rocks” (p = 0.0041) and “Offshore Reef
269
Patches” (p = 0.0012). A significant positive correlation (p = 0.027) was detected
270
between the density of open, mangrove-lined estuaries and manatee sightings. Other
271
estuarine types such as partially obstructed sand bar (barrier) estuaries or seasonally
272
obstructed sand bar estuaries, which are both typical of coasts with sandy beaches, sand
273
bars, sand banks, dunes, strong wave action and wind-driven currents, showed no
274
correlation with the density of manatees. Dolphin sightings were positively correlated
275
with large estuaries (p = 0.027) and mangroves (p = 0.023) (Table 2).
276
Manatee sightings were positively correlated with the presence of medium-sized cities
277
(p = 0.034) and motor boats (p = 0.011). Sea turtles were positively correlated with the
278
total number of fishing boats (p = 0.030) and with motorized boats (p = 0.0017). Shrimp
279
farms, salt works and ports did not show any positive or negative correlations with any
280
animals (Table 2).
281
282
3.3. Marine protected areas (MPAs)
283
Significant positive correlations with MPAs were detected for manatees, dolphins and
284
sea turtles, and varied considerably between taxonomic groups and areas (Fig. 4 and
285
Table 3). When considering all four MPAs and comparing sightings in these areas to
286
areas outside MPAs, manatees were the only group to show significantly higher density
77
287
within MPAs (Table 3). The average density of manatees within MPAs was 0.3
288
individuals per 5 km-segment (18 individuals along 310 km coastline), three times
289
larger than in areas outside MPAs (0.1 individuals per 5 km-segment, 23 individuals
290
along 1160 km coastline). This positive relationship was confirmed by Spearman
291
correlation analysis (p = 0.001).
292
When considering individual MPAs, manatees showed significantly higher density in
293
two estuarine MPAs (“Delta do Rio Parnaíba” and “Barra do Rio Mamanguape”) than
294
outside, with six and five manatees, respectively. Dolphins showed significantly higher
295
density within the “Costa dos Corais” MPA (24 dolphins), while sea turtles showed
296
significantly higher density within the “Recifes de Corais” MPA (41 sea turtles) (Fig. 4
297
and Table 3).
298
299
Fig. 4. Density of manatees (left), dolphins (center) and sea turtles (right) in marine
300
protected areas in northeastern Brazil (DP: Delta do Rio Parnaíba, RC: Recifes de
301
Corais, BM: Barra do Rio Mamanguape, CC: Costa dos Corais, Outside: areas outside
302
marine protected areas). Data are based on 27 hours of aerial surveys from the states of
303
Piauí to Alagoas. N = 294 coastal segments of 5 km length.
304
78
305
27 hours of aerial surveys. N = 294 coastal segments of 5 km length. Values given in the table are total number of organisms (N) and
Table 3. Marine Protected Areas (MPAs) in northeastern Brazil and total sightings of manatees, dolphins and sea turtles. Data are based on
Spearman correlation
3 / 0.2
6 / 0.4
2 / 0.3
0 / 0.0
4 / 0.3
22 / 0.8
8 / 1.3
41/ 2.9
12 / 0.8
0.001
n.s.
0.0007
n.s.
0.004
n.s.
0.024
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
0.0008
n.s.
Manatees Dolphins Sea Turtles Manatees Dolphins Sea Turtles
N / Density per segment
306
Main Habitat
density (N per km coastline).
Area
(km² / segment)
5 / 0.8
24 / 0.9
83 / 1.3
Extensive
4 / 0.2
30 / 0.5
203 / 0.9
Recifes de Corais
Barra do Rio
Mamanguape
0.15 / 6
“n.s.“: not significant at α= 0.05.
Lines
Coastal Reef
Lines
Coastal Reef
Patches
Offshore Reef
Mangroves
4.14 / 26
18 / 0.3
48 / 0.2
3.14 / 16
Costa dos Corais
Total: 9.23 / 62
23 / 0.1
Parnaíba
All MPAs
Total: - / 232
1.8 / 14
Outside MPAs
Delta do Rio
MPAs
307
308
309
310
311
312
313
314
315
316
317
79
318
4. Discussion
319
The data generated by the hitherto largest effort to quantify and correlate the
320
distribution of manatees, dolphins and sea turtles in Brazil yielded important new
321
insights into the situation of conservation these groups.
322
This study revealed a wide distribution of manatees, dolphins and sea turtles, except for
323
a single area (the Potiguar Basin), probably due to specific hydrographic features and
324
anthropogenic factors in this area. The present data showed that some species were
325
associated with each other and with coastal features, such as estuaries and reefs. The
326
important role of MPAs was corroborated by the high densities of these animals. One
327
alarming finding was the association of manatees and sea turtles with motorized fishing
328
boats and coastal cities, which is a relevant conservation issue.
329
330
4.1. Spatial distribution
331
Manatees, dolphins and sea turtles occurred more or less continuously along the study
332
area. The only extensive area with virtually no sightings of animals was inserted in
333
Potiguar Basin area, located at the northwestern coast of Rio Grande do Norte state.
334
This region presents extremely harsh conditions due to the high energy of winds, waves
335
and tides, with strong alongshore currents in westerly direction (Silva and Amaro,
336
2008). It is also considered one of the most oligotrophic regions of Brazil and has the
337
lowest estuarine influence of the entire coastline, with virtually no freshwater input
338
(Júnior et al., 2010). Furthermore, intensive resource exploration and coastal
339
degradation have persisted for many decades due to the activities of the offshore oil
340
industry, salt works and shrimp farming (Silva and Amaro, 2008), as observed during
341
the survey. Seismic surveys associated with the offshore industry may cause severe
80
342
physiological and behavioral changes in several organisms, especially in marine
343
mammals (McCauley et al., 2000; Early, 2001). However, the present study and earlier
344
assessments (Parente et al., 2006; Parente and Araújo, 2011) are still insufficient to
345
evaluate the influence of offshore activities on the distribution and behavior of marine
346
mammals and sea turtles in northeastern Brazil. The distribution of manatees, that
347
forage on macrophytes and seagrass beds and are known to actively seek freshwater to
348
drink, seems to be fundamentally determined by the availability of freshwater and food
349
sources, and shelter in estuaries for reproduction (Hartman, 1979; Reynolds et al.,
350
2009). However, the extreme harshness of the dynamic coastline, the scarcity or
351
absence of freshwater sources and foods, the scarce and inaccessible sand bar estuaries,
352
the absence of any shelter provided by barrier reefs and the intense human exploration
353
may together explain the absence of manatees in the Potiguar Basin. This area and the
354
eastern portion of the state of Ceará show the largest numbers of cases of manatee
355
strandings, especially neonates, probably related to these factors (Parente et al., 2004;
356
Meirelles, 2008; Lima et al., 2011).
357
The coexistence of manatees and sea turtles found in this study has been recorded in
358
various other locations worldwide (Fertl and Fulling, 2007). This positive relationship is
359
a function of the ecological requirements of both taxa, which may share common shelter
360
and coastal foraging areas. Herbivory is a common trait among sirenians and C. mydas,
361
feeding on seagrass beds and macroalgae (Hartman, 1979; Borges et al., 2008; López-
362
Mendilaharsu et al., 2008; Guebert-Bartholo et al., 2011). There is a correlation of both
363
taxa and fishing boats, both being concentrated close to shore, in the same, productive
364
areas. This proximity implies a high risk of collision, accidental capture and habitat
365
destruction, mainly by shrimp trawlers (Borges et al., 2007; Meirelles, 2008; Eguchi et
81
366
al., 2010; Guebert-Bartholo et al., 2011). In Florida, most of the reported mortalities and
367
serious mutilations of manatees (T. m. latirostris) are due to collisions with motor boats
368
(Nowacek et al., 2004; Rommel et al., 2007). In northeastern Brazil, previous reports
369
indicate that the interaction of T. m. manatus with motor boat traffic represents a direct
370
threat for this species, causing lesions and deaths (Borges et al., 2007; Meirelles, 2008).
371
In San Diego Bay, an intensively urbanized coastal area, frequent strandings of green
372
turtles have been reported, probably related to collisions with motor boats (Eguchi et al.,
373
2010).
374
375
4.1.1. Antillean manatee
376
Studies on the distribution of manatees in Brazil have been conducted since the 80s,
377
based on information from fishermen and stranding data (Parente et al., 2004; Luna et
378
al., 2008; Lima et al., 2011). Only one single study in the eastern part of Ceará state
379
used an aerial survey, however with difficulties associated to the observation of these
380
animals in turbid waters during the rainy season and flight logistics (Costa, 2006).
381
Conversely, the aerial methodology used in this study was very favorable for the
382
detection of manatees, highlighting its importance for the conservation of this
383
endangered species.
384
The detection of some manatees has been hampered due to the following factors: (1)
385
solitary habit, (2) barely visible exposure on the surface, and (3) cryptic brownish color
386
surrounded by turbid waters near estuaries. These limitations may make counting and
387
identification inaccurate (Edwards et al., 2007), one alternative being the use of a side-
388
scan sonar (Gonzalez-Socoloske et al., 2009). During periods of cold weather, aerial
389
surveys conducted in Florida uncovered large groups of manatees in areas of warm and
82
390
transparent water, which facilitated the counting (Edwards et al., 2007). In the study
391
area, the almost constant temperature of coastal waters prevents this type of
392
phenomenon (Lima et al., 2011).
393
The social structure of manatees, predominantly solitary or in couples, was also found
394
in other studies in this region (Borobia and Lodi, 1992; Paludo and Langguth, 2002;
395
Costa, 2006). The presence of calves on Barreta beach, Rio Grande do Norte state, was
396
also recorded by other researchers (Oliveira et al., 1990; Paludo, 1998), suggesting the
397
existence of a nursery area. The mating period of manatees in northeastern Brazil is the
398
dry season, from October to May (Paludo, 1998; Parente et al., 2004; Meirelles, 2008;
399
Lima et al., 2011). The observation of a single calf only within the reproductive season
400
(March) during the aerial survey may be considered worrisome for the conservation of
401
this species, which is threatened by the destruction and degradation of its estuaries
402
(Parente et al., 2004; Meirelles, 2008). Furthermore, these few records may be due to
403
lack of sampling within the estuaries, which are ecosystems using for reproduction and
404
parental care of manatees (Hartman, 1979; Lima et al., 2011), or detection difficulty
405
related smaller size.
406
The presence of manatees in shallow coastal waters, generally with less than 12 m
407
depth, seems to be related to the availability of food sources (Hartman, 1979; Olivera-
408
Gómez and Mellink, 2005; Rodas-Trejo et al., 2008; Langtimm et al., 2011).
409
Furthermore, these are often shallow sheltered sites that allow animals to spend less
410
energy in respiratory intervals (Smethurst and Nietschmann, 1999; Bacchus et al.,
411
2009). The access to shallow foraging areas at high tide only introduces additional
412
variability to the depth range of manatees. In previous studies conducted in northeastern
413
Brazil with observations from shore or on boats, water depth of manatee sightings
83
414
varied between only 0.4 and 5.6 m (Borobia and Lodi, 1992; Paludo and Langguth,
415
2002; Costa, 2006), which is much shallower than the range observed in our study
416
(most frequently within 6–8 m, reaching 14.8 m). This difference is probably due to the
417
more efficient coverage of deeper waters in this aerial survey as compared to earlier
418
studies. The most common seagrass in this region, Halodule wrightii, which is
419
considered one of the main food sources for this species (Borges et al., 2008; Lima et
420
al., 2011), is found from the intertidal zone down to 10 m depth (Laborel-Deguen,
421
1963).
422
Furthermore, the occurrence of manatees near well-preserved mangrove estuaries
423
located in the northern part of the study area reflects the use of these types of habitats
424
for breeding and foraging (Olivera-Gómez and Mellink, 2005; Rodas-Trejo et al., 2008;
425
Lima et al., 2011). In many other estuaries surveyed in this study, the visible
426
deforestation of mangrove vegetation due to the expansion of shrimp farms, salt works,
427
and urbanization has caused the closing of estuaries with sand bars, hampering the
428
access by manatees (Lima et al., 2011).
429
The positive correlation between manatees and medium-sized cities highlights the
430
intense human occupation of the coastal zone around estuarine and sheltered areas that
431
are important for this species. The attractiveness of bays and estuaries for human
432
populations in Brazil resulted in a long process of intense urban development, fisheries,
433
ports, industries and recreational activities in these areas, which are major threats for
434
coastal ecosystems (Cunha, 2005) and many endangered species.
435
436
437
84
438
4.1.2. Dolphins
439
Even under ideal conditions of water transparency and swimming in groups, the
440
identification of dolphins was difficult due to their quick movements in opposition to
441
the speed of the aircraft. The small morphological variations between some cetaceans
442
make aerial identification difficult (Preen, 2004). S. guianensis was diagnosed by the
443
morphology of the rostrum and melon, pink-gray coloration and its triangular dorsal fin
444
(Flores, 2002).
445
Groups of two to eight Guiana dolphins found in this study are commonly observed in
446
northeastern Brazil (Araújo et al., 2001, 2008), while groups of this species may reach
447
150 specimens in the southern region (Flores, 2002), where waters are more productive
448
due to seasonal upwelling (Muehe and Garcez, 2005). This explains the tendency of
449
large groups to inhabit the southern and southeastern region, and small groups to occur
450
in the northeastern region (Araújo et al., 2008).
451
The higher frequency of dolphins in deep waters, reaching a depth of 17.1 m and at a
452
distance of up to 4.4 km from the coast in the present study, is similar to findings of
453
previous studies on Guiana dolphins in Brazil, with up to 16 m depth and four km from
454
the coast (Bazzalo et al., 2008; Wedekin et al., 2010). Previous studies showed that the
455
bathymetry is important for the distributions of dolphins, mainly due to the depth-
456
related distribution of prey (Baumgartner et al., 2001; Certain et al., 2008). This may
457
reflect their search for food, corroborated by the migration of fish to deeper areas and
458
away from the coast due to environmental perturbations in nearshore reef ecosystems in
459
northeastern Brazil (Frédou and Ferreira, 2005). The search of these animals for more
460
offshore areas may suggest a strategy to find favorable foraging areas, and possibly to
461
avoid the intense coastal artisanal fishing activity recorded in this study. Accidental
85
462
capture in fishing nets is a main threat for Guiana dolphins in Ceará state, cetacean
463
species with highest (62%) incidence of strandings (Meirelles et al., 2009). This species
464
and bottlenose dolphins (Tursiops truncatus) have foraging as a determinant factor for
465
habitat choice (Hastie et al., 2004; Wedekin et al., 2010).
466
The occurrence of dolphins close to estuaries may indicate the search for food sources
467
that are associated to these important nurseries for crustaceans and fish, both for
468
resident species and for marine migratory species (Blaber, 2000). In Brazil, S.
469
guianensis frequently occurs in estuarine areas and their surroundings (Flores, 2002;
470
Araújo et al., 2008), suggesting that many unidentified specimens are probably of this
471
species.
472
473
4.1.3. Sea turtles
474
Sea turtles were the most abundant taxon in this study. This is the first aerial survey of
475
sea turtles carried out in Brazil. This methodology has been shown to provide important
476
abundance estimates of sea turtle populations, especially in foraging or nesting grounds
477
(Epperly et al., 1995; Cardona et al., 2005; Roos et al., 2005; Witt et al., 2009).
478
Individuals from the family Cheloniidae have been identified by the greenish-brown
479
shell coloration, that is distinct from Dermochelyidae, which have a black color and
480
very prominent ridges. The detection of the specimens, even in moderate visibility
481
conditions, occurred through the total body exposure and turbulence at the water surface
482
caused by the fins during the dive, which could reveal the number of animals
483
(McClellan, 1996). However, flight altitude and speed, and escape behavior caused by
484
the noise of the aircraft, made the identification at species level difficult, as observed in
485
other studies (Shoop and Kenney, 1992; Epperly et al., 1995, McClellan, 1996). The
86
486
smaller size of sea turtles in relation to other taxa studied also contributed as a limiting
487
factor for identification to species level. Previous studies based on aerial surveys
488
suggested a minimum size of 30 (Epperly et al., 1995) to 75 cm (Shoop and Kenney,
489
1992) carapace width for a specific diagnosis of sea turtles. Conversely, in the present
490
study, identification to species level was not possible even for large-sized specimens.
491
The high number of solitary sea turtles sighted could indicate that the areas studied did
492
not include major breeding grounds, since mating occurs in large groups in shallow
493
waters (Hirth, 1980). In Brazil, green turtles, for example, may be sighted in groups
494
during the reproductive period from September to March, which includes the study
495
period. This species uses oceanic islands for mating, being rarely sighted in large groups
496
along the continental northeastern coast of Brazil. The northeastern coast harbors 12 of
497
the 19 main breeding areas for sea turtles in country (Marcovaldi and Marcovaldi,
498
1999). However, none is included in the study area, although nesting areas along the
499
coast have been recorded. Aerial and snorkel census techniques for estimating green
500
turtle abundance in foraging areas identified small groups of 4–5 individuals, that
501
apparently were randomly distributed (Roos et al., 2005). It is therefore likely that the
502
study area is mainly used for feeding and resting.
503
In this study, varying depths (0.9–18.5 m) and distances from the coast (from the
504
coastline up to 5 km) occupied by sea turtles showed the diversity of existing habitats.
505
Their spatial distribution can be influenced by physical and biological parameters, and
506
depth distribution is closely related to their feeding, breeding and resting behavior
507
(Griffin and Griffin, 2003; Roos et al., 2005; Witt et al., 2010). In a previous study in
508
Brazil, green turtles were sighted during scuba dives feeding at 6 m depth (Guebert-
509
Bartholo et al., 2011), and swimming in areas with vegetation at 10 m depth and up to
87
510
10 km distant from the coast (Parente et al., 2006). These numbers are within the range
511
recorded in this study, suggesting the occurrence of important foraging areas in
512
northeastern Brazil.
513
The positive correlation of sea turtles with reef formations such as Northern Beach
514
Rocks and Offshore Reef Patches, as observed by the high density of individuals in the
515
MPA “Recifes de Coral" may be intimately related to the search for shallow sheltered
516
areas and for areas with abundant macroalgae that grow on sandstone substrates.
517
Likewise, an aerial survey carried out in Western Australia revealed a higher density of
518
sea turtles in reef areas (Preen et al., 1997). In a study conducted in the South-West
519
Indian Ocean, the distribution of these animals close to coral reefs and on the outer reef
520
slopes was explained by the availability of shelter and food (Jean et al., 2010), similarly
521
to the findings of the present study.
522
523
4.2. Marine protected areas (MPAs)
524
The high density of manatees in the MPAs "Delta do Rio Parnaíba” and "Barra do Rio
525
Mamanguape" highlights the importance of these areas for the protection of this species
526
and its habitats. These areas are mainly composed of a complex deltaic environment
527
with well-preserved mangroves ("Delta do Rio Parnaíba”) or estuarine mangroves with
528
adjacent coastal reef lines ("Barra do Rio Mamanguape"), allowing for the occurrence
529
of groups of manatees in sheltered, well-preserved areas and an open access to upstream
530
environments for reproduction and resting (Borobia and Lodi, 1992; Lima et al., 2011).
531
In the Persian Gulf, areas with high densities of dugongs and sea turtles were related to
532
habitats that are rich in seagrass beds and coral reefs, and were chosen for the
533
establishment of MPAs (Preen, 2004).
88
534
The occurrence of dolphins and sea turtles in MPAs characterized by linear coastal reef
535
formations can ensure sheltered areas for foraging and resting. The MPA “Recifes de
536
Coral”, with high numbers of sea turtle sightings, has coastal and offshore reefs, as well
537
as seagrass beds and banks of macroalgae, which likely represent food sources for these
538
animals (Guebert-Bartholo et al., 2011). In the MPA "Costa dos Corais", the
539
configuration of a large-scale barrier reef may allow for higher food availability and
540
facilitate fish capture strategies by dolphins. The use of specific foraging techniques is
541
commonplace for some species of delphinids, such as the bottlenose dolphin, that adapt
542
its distribution patterns towards habitats that are favorable for prey capture (Hastie et
543
al., 2004; Torres and Read, 2009). In Brazil, Guiana dolphins feed preferentially in
544
bays, barrier reefs and estuaries, where they can direct fish schools to shallower waters
545
(Araújo et al., 2001; Rossi-Santos and Flores, 2009). Such areas are widely found in the
546
MPA "Costa dos Corais" (FAO, 2011).
547
It is noteworthy that there is a captive manatee reintroduction program within the MPA
548
"Costa dos Corais", located in the northern part of the state of Alagoas. This very
549
successful program has possibly provided an increase of the manatee population in this
550
area (ICMBio, 2011). However, proximity and easy access of human populations to reef
551
areas found in the study can directly affect the biological communities (Castro and
552
Pires, 2001). Habitat loss and the degradation of feeding areas for sea turtles are a
553
potential cause of population decline (López-Mendilaharsu et al., 2008; Guebert-
554
Bartholo et al., 2011) and the presence of motor boat traffic and trawling can cause
555
behavioral changes in dolphins (Constantine et al., 2004; Wedekin et al., 2010; Carrera
556
et al., 2008).
89
557
The results of the present study cannot be used to test whether the existence of MPAs
558
increases the density of endangered species in these areas, as in other studies (Witt et
559
al., 2009; Panigada et al., 2011; Knip et al., 2012). All MPAs were delineated around
560
special coastal features, such as outstandingly large or exceptionally well-preserved
561
estuaries and barrier reefs, which create favorable and essential habitats for these and
562
many other species. Rather than proving the effect of MPAs, the elevated density of
563
these organisms shows the vital importance of protecting and adequately managing such
564
unique ecosystems to ensure a sustainable future for the populations of severely
565
threatened species.
566
567
5. Conclusions
568
The spatial distributions of manatees, dolphins and sea turtles show the different types
569
of behavior of these species and the variety of ecosystems along the coast, with a
570
preference for well-preserved foraging and resting habitats.
571
In northeastern Brazil, aerial monitoring in areas of occurrence of marine mammals and
572
sea turtles, that are susceptible to habitat loss, can encourage the development of
573
management, environmental conservation and recovery programs. The diagnosis and
574
monitoring of ecosystems are essential for the survival of marine biodiversity,
575
highlighting the role of MPAs for the protection of ecosystems and species.
576
577
578
579
580
90
581
Acknowledgments
582
The authors would like to thank the Federal University of Pernambuco (UFPE) and the
583
“Fundação Mamíferos Aquáticos” (FMA) for supporting the survey; “Petrobras
584
Petróleo Brasileiro S.A.” through its “Programa Petrobras Ambiental” for sponsoring
585
the aerial surveys; “Conselho Nacional de Desenvolvimento Científico e Tecnológico”
586
(CNPq) for the doctoral scholarship granted to the first author; the “Centro Mamíferos
587
Aquáticos”(CMA) for initially supporting the research; PhD. Paul Gerhard Kinas for
588
methodological support; and the NVO air taxi team for adapting their plane to carry out
589
the aerial survey and logistics of flights. This study is part of the doctoral thesis of the
590
first author.
591
592
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593
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594
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102
Capítulo 4* - Distribuição do peixe-boi marinho em relação às angiospermas marinhas
no nordeste do Brasil.
Chapter 4* - Distribution of Antillean manatee in relation to seagrass in northeastern
Brazil.
* Capítulo em formato de artigo e padronizado de acordo com as normas da revista
Aquatic Conservation: Marine and Freshwater Ecosystems.
1
Distribution of Antillean manatee in relation to seagrass in northeastern Brazil
2
3
MARIA DANISE DE OLIVEIRA ALVESa,b*, MARIA ELISA PITANGAa,c, MARIA
4
ELISABETH DE ARAÚJOa, SIMONE RABELO DA CUNHAd, KARINE MATOS
5
MAGALHÃESc
6
7
8
a
9
Department of Oceanography, Universidade Federal de Pernambuco, Recife,
10
Pernambuco, Brazil.
b
11
c
12
13
14
15
Fundação Mamíferos Aquáticos, Recife, Pernambuco, Brazil.
Department of Biology, Universidade Federal Rural de Pernambuco, Recife,
Pernambuco, Brazil.
d
Centro Acadêmico de Vitória, Universidade Federal de Pernambuco, Bela Vista,
Pernambuco, Brazil.
16
17
18
19
20
21
22
23
24
*Correspondence to: MDO. Alve, Department of Oceanography, Universidade Federal
25
de Pernambuco, Recife, Pernambuco, Brazil.
26
E-mail: [email protected]
103
27
ABSTRACT
28
1. Seagrass is one of the main food items in the diet of the Antillean manatee.
29
2. The aim of the present study was to relate the spatial distribution pattern of seagrass
30
with the occurrence of the Antillean manatee in northeastern Brazil and characterize
31
potential foraging grounds for the species.
32
3. The identification of areas with seagrass was based on in situ observations, data from
33
the literature and personal information from the researchers and the local fishermen.
34
Data on the occurrence of Antillean manatees consisted of aerial sightings, cases of
35
stranding and information from fishermen.
36
4. Seagrass was recorded at 41 beaches, wich is 69% greater than the number of records
37
described in the literature. The species identified were Halodule wrightii, which was the
38
most frequent, Halophila decipiens and Ruppia maritima. The distance from shore and
39
depth of the coastal habitats and estuarine with seagrass were similar to the spatial
40
distribution described by literature for the Antillean manatee
41
5. Despite the 27 records of occurrence of both seagrass and manatees at the same sites,
42
the correlation analysis of the two factors was not significative. This lack of significant
43
correlation may be related to the reduction in the foraging grounds and/or the generalist
44
habit of manatees, which feeds on different types of vegetation, especially macroalgae,
45
throughout its variable home range.
46
6. The present findings emphasize the importance of directing efforts toward reducing
47
additional losses of seagrass beds and serve as a useful tool for the drafting of regional
48
management plans to prevent the further decline of these ecosystems, which are
49
potential foraging grounds for the Antillean manatee.
50
KEY WORDS: seagrass; manatees; occurrences; food resources; habitats; Brazil
104
51
INTRODUCTION
52
The Antillean manatee, Trichechus manatus manatus Linneaus 1758, is a herbivorous
53
aquatic mammal (Hartman, 1979) that inhabits, rivers, estuaries and shallow coastal
54
waters from the eastern coast of Mexico to the northeastern portion of South America
55
(Lefebvre et al., 2001). The presence of fresh water and an abundance of aquatic
56
vegetation, especially seagrass, are important environmental characteristics influencing
57
of occurrence of these animals (Morales-Vela et al., 2000; Paludo and Langguth, 2002;
58
Olivera-Gómez and Mellink, 2005; Costa, 2006; LaCommare et al., 2008).
59
In Brazil, T. m. manatus exhibits heterogeneous distribution along the northern and
60
northeastern regions of the country (Luna et al., 2008; Lima et al., 2011; Alves et al.,
61
2013). The history of hunting practiced in the past (Oliveira et al., 1990) and the
62
significant reduction current in coastal habitats and estuaries, which have traditionally
63
been used by the species for feeding, breeding and resting grounds (Parente et al., 2004;
64
Meirelles, 2008; Alves et al., 2013), has led to a population decline, making the
65
Antillean manatee the most endangered aquatic mammal in Brazil (ICMBio, 2011).
66
In terms of diet, the Antillean manatee is an opportunistic, generalist herbivore that
67
feeds on a variety of algae, seagrass and freshwater macrophytes (Hartman, 1979;
68
Smith, 1993). The main seagrasses consumed by this manatee are turtle seagrass
69
(Thalassia testudinum Banks ex König 1805), manatee seagrass (Syringodium filiforme
70
Kützing in Hohenacker 1860), widgeon grass (Ruppia maritima Linneaus 1753), three
71
species of the genus Halophila (H. engelmannii Ascherson in Neumayer 1875, H.
72
johnsonii Eiseman 1980 and H. decipiens Ostenfeld 1902) and shoal grass (Halodule
73
wrightii Ascherson 1868) (Provancha and Hall, 1991; Lefebvre et al., 2000; Reich and
74
Worthy, 2006; Castelblanco-Martínez et al., 2009; Alves-Stanley et al., 2010), the latter
105
75
of which is considered the most consumed by populations of the Antillean manatee in
76
Brazil (Banks and Albuquerque-Neto, 1985; Costa, 2006; Borges et al., 2008; Lima et
77
al., 2011).
78
Seagrass is represented by approximately 60 species worldwide, distributed among
79
13 genera (Short et al., 2001). Despite the low degree of taxonomic diversity, seagrass
80
plays an important ecological role in coastal environments (Heck and Valentine, 2006;
81
Marques & Creed, 2008; Pereira et al. 2010). In the Brazilian coast are recorded R.
82
maritima, H. decipiens, Halophila baillonis Ascherson ex Dickie in JD Hooker 1874,
83
Halodule emarginata Hartog, 1970 and H. wrightii, the latter of which is the most
84
widely distributed and best studied (Short et al., 2007).
85
The general distribution and composition of seagrass beds in Brazil have been
86
documented in only two studies (Den Hartog, 1972; Oliveira-Filho et al., 1983), with a
87
more recent bibliographic review (Marques and Creed, 2008). In the northeastern
88
region, studies have been restricted to small areas (Vieira, 2006; Silva, 2010; Silva et
89
al., 2012), and most of them were carried out in the state of Pernambuco (Laborel-
90
Deguen, 1963; Magalhães and Alves, 2002; Magalhães and Cazuza, 2005; Reis, 2007).
91
Seagrass are restricted to shallow coastal waters and estuaries, and so has historically
92
been endangered by intensive activities of urbanization and fishing worldwide, making
93
them vulnerable to extinction (Duarte, 2002; Ceccherelli et al., 2007; Freeman et al.,
94
2008; Short et al., 2011; Pitanga et al., 2012).
95
Knowledge on the spatial distribution of manatees based on the presence of food
96
resources is essential to the establishment of local and regional conservation strategies
97
aimed to insure the protection of the species and of its habitats (Olivera-Gómez and
98
Mellink, 2005; Alves-Stanley et al., 2010; Semeyn et al., 2011). Studies on the presence
106
99
of T. m. manatus and its foraging grounds are rare in Brazil and have been limited to the
100
monitoring of native animals in restricted areas (Paludo and Langguth, 2002; Costa,
101
2006) or specimens reintroduced into the natural environment (Lima, 2008).
102
Due to the lack of data on the distribution of seagrass and the large-scale association
103
between this ecosystem and the spatial distribution of manatees, the aim of the present
104
study was to relate the spatial distribution pattern of seagrass to the presence of the
105
Antillean manatee in northeastern Brazil. The results will allow mapping the current
106
areas of occurrence of seagrass in part of this region of the country and allow the
107
establishment of priority areas for the protection of such ecosystems. This is the first
108
survey on the spatial distribution of possible foraging grounds of the Antillean manatee
109
in Brazil.
110
111
METHODS
112
Study region
113
The study area was located between the states of Rio Grande do Norte and Alagoas,
114
covering approximately 932 km of the 3400 km of coastline throughout northeastern
115
Brazil (Figure 1). This region is characterized by a variety of ecosystems, including
116
beaches, dunes, coral reefs, mangroves and estuaries. The area is defined by two
117
seasons (dry and rainy), high temperatures (>26°C), high salinity and a low
118
concentration of nutrients, except in estuarine areas, in which high primary productivity
119
and biomass are found (Andrade and Lins, 2005; Muehe and Garcez, 2005).
120
107
121
122
Figure 1. Study area with demarcation of sampling units (70 km) for analysis of the
123
spatial distribution of seagrass between the states of Rio Grande do Norte and Alagoas
124
along the northeastern coast of Brazil.
125
126
Seagrass in northeastern Brazil is represented by five species (Oliveira-Filho et al.,
127
1983; Marques and Creed, 2008) and corresponds to more than 70% of the national
128
coverage, which is estimated at 200 km2 (Freire et al., 2008). In the region, the
129
Antillean manatee was estimated at less than 300 animals, basing fisherman information
130
(Lima et al., 2011), and 1146 specimens in recent study of the aerial survey (Alves et
131
al., unpublished).
108
132
Seagrass sampling
133
The identification of potential foraging areas of the Antillean manatee in northeastern
134
Brazil (characterized by the presence/absence of seagrass) was based on 33 records
135
available in the literature (Laborel-Deguen, 1963; Den Hartog, 1972; Oliveira-Filho et
136
al., 1983; Magalhães and Cazuza, 2005; Vieira, 2006; Reis, 2007; Silva, 2010; Silva et
137
al., 2012) (Figure 2B), personal information from specialists in each state as well as 92
138
interviews with local fishermen. In exceptional cases of an absence of such information,
139
beaches with records of the occurrence of Antillean manatees were selected for field
140
investigations. Bibliographic data on the occurrence of seagrass in non-visited areas
141
were used to detail information on the distribution of this aquatic vegetation. The in situ
142
mapping for the confirmation of areas of occurrence of seagrass beds was performed
143
between April 2011 and December 2012, with intensive search for samples stranded in
144
the mid littoral zone at low tide (≤ 0.4 m).
145
For the identification of the species, samples were preferably taken from the central
146
region of the seagrass bed. The depth of the areas of seagrass beds was measured using
147
a portable digital echo sounder to determine free diving (depths ≤ 60 cm) or scuba
148
diving (depths > 70 cm) for the collection of samples. Stranded plants were sampled
149
only when no seagrass beds were found. The species were identified based on
150
descriptions by Oliveira-Filho et al. (1983).
151
Records of the occurrence of T. m. manatus were defined by 30 aerial sightings
152
(Alves et al., unpublished data), 32 stranded specimens (Parente et al., 2004; Oliveira et
153
al., 1990) and 62 interviews with fishermen (Lima et al., 2011), totaling 124 records.
154
155
109
156
Data analysis
157
The records of the occurrence of seagrass were georeferenced and the data transferred to
158
the GPS TrackMaker PRO (version 4.8) Geographic Information System, and each
159
geographic coordinate received an identification code by species. Manatee records were
160
georeferenced using Google Earth 2013 and the data then entered in the ArcMap
161
program (version 10.0) for the construction of a map of Antillean manatee distribution
162
versus vegetal distribution.
163
For the analysis of the spatial distribution patterns of seagrass and the Antillean
164
manatee, the study area was divided into 12 sectors (sampling units), each one with
165
approximately 70 km of coastline (Figure 1). This distance was based on the mean
166
distances recorded between sites of fidelity (home range) of the Antillean manatees and
167
areas of reintroduction in Brazil (Lima, 2008). Only one site (located between sectors 2
168
and 3, to the northeast of the state of Rio Grande do Norte) was not sampled due to the
169
absence of records of seagrass. Furthermore, were also analyzed sectors of smaller size
170
corresponding to 5, 10, 20 and 40 km. At each one these sectors bibliographic and
171
current records of seagrass and manatee were counted.
172
Two cluster analyses were performed to investigate the similarity among sectors. The
173
first was based on bibliographic and current records of seagrass. The second was based
174
on manatee occurrence determined by aerial sightings, stranding data and information
175
from fisherman. The Bray-Curtis index was used as the similarity measure and the
176
group average was used for the cluster mode. The analyses were performed using
177
Primer 6.0 (Clarke and Gorlye, 2006).
178
Spearman rank correlation analysis (Zar, 1996) was used to relate records of seagrass
179
and manatees at each sector (5, 10, 20, 40 and 70 km), as data presence/absence. This
110
180
method of correlation analysis was chosen due to the non-linearity of relationships and
181
non-normality and heteroscedascity of most records. All analyses were performed using
182
the “R” language and environment, considering α = 0.05 (R Development Core Team
183
2009, version 2.9).
184
185
RESULTS
186
Spatial distribution of seagrass
187
Seagrass was recorded in 41 of the 53 beaches mapped. Among these, 32 were seagrass
188
beds and nine were fragments plants. The following species were found: H. wrightii (n
189
= 35), H. decipiens (n = 1) and R. maritima (n = 1). Moreover, Halodule wrightii and
190
Halophila decipiens were found coexisting in the same seagrass bed (n = 4) (Figure 2).
191
H. wrightii was found predominantly in marine habitats (48.57%), whereas H. decipiens
192
and R. maritima were found exclusively in estuaries and coastal lagoon, respectively.
193
The most cases of Halodule wrightii and Halophila decipiens coexistence was in marine
194
environments (75%). The distance of the seagrass beds from the coastline ranged from 0
195
to 7.6 km (mean: 1.28 km). Depths at low tide ranged from 0 to 10.2 m (mean: 1.28 m).
196
The localization of more distant and deeper seagrass beds was only possible due to
197
information acquired from local fishermen.
198
The spatial distribution of seagrass in the present study broadens information found
199
in the literature on the occurrence of the species, with H. wrightii the most common and
200
most widely distributed. The major “hot spots” for the occurrence of seagrass were
201
sectors 5, 6 and 7 using current information and sectors 7 and 8 using bibliographic
202
information (Figure 2).
203
111
204
Figure 2. Distribution of seagrass in present study (A) and based on data from the
205
literature (B) (Laborel-Deguen, 1963; Den Hartog, 1972; Oliveira-Filho et al., 1983;
206
Magalhães and Cazuza, 2005; Vieira, 2006; Reis, 2007; Silva, 2010; Silva et al., 2012).
207
The details show the areas with the greatest numbers of these plants.
208
209
Based on the occurrence of seagrass was possible to identify two groups of sites
210
(similarity of 40%). Sector 12 was not grouped. The isolation of this sector was due to
211
the absence of seagrass (confirmed in both the literature and present study). Sectors 7
212
and 8 were united by a greater number of bibliographic records of seagrass, with
213
similarity greater than 60%. The remaining sectors were grouped (similarity around
214
50%) due to the small amount or absence of bibliographic records of seagrass records.
215
One hundred percent similarity was found between sectors 3 and 4 as well as between
216
sectors 1 and 11 (Figure 3).
112
217
218
Figure 3. Bray-Curtis dendogram (A) and graph (B) of occurrence of seagrass in
219
sampling sectors based on data from the literature and the present study.
220
221
Spatial distribution of Antillean manatee versus seagrass
222
In the analysis of the spatial distribution of manatees and seagrass, no significant
223
correlations were found in any of the combinations tested, all sizes of sectors proposed,
224
including the individual analysis between the Antillean manatees and “hot spot” sectors
225
regarding the occurrence of seagrass. However, a total of 27 beaches had joint records
226
of occurrence of manatees and seagrass. Aerial sightings, which were considered the
227
most current data on the presence of T. m. manatus in the study area, occurred in
228
40.74% of the beaches with records of seagrass. Likewise, information from fishermen,
229
which constituted the oldest records of the occurrence of Antillean manatees, occurred
113
230
in 66.66% of the beaches with seagrass. The occurrence of both seagrass and stranded
231
manatees was recorded on 29.63% of the beaches (Figure 4).
232
233
Figure 4. Spatial distribution of records of occurrence of seagrass in the study area
234
based on data from the literature (A) and the present study (B) as well as the occurrence
235
of manatees based on aerial sightings (A, B – airplane), stranding (A, B – cross) and
236
information from fishermen (A, B – fisherman).
114
237
The clusters of sectors 2 and 12 had approximately 65% similarity regarding the
238
occurrence of Antillean manatees due to the few records of this species and seagrass
239
(Figure 5). Sector 8 was isolated due to the absence of manatees, which is contrary to
240
the result for seagrass (Figure 4). The largest cluster, with similarity indices greater than
241
60%, encompasses areas with the greatest records of occurrence manatees. The cluster
242
formed by sectors 1 and 11 is distinguished by the absence of aerial sightings. Stranded
243
manatees occurred with greater frequency in sectors 5 and 6 (Figure 5), which also
244
exhibited current occurrences of seagrass (Figure 3).
245
246
Figure 5. Bray-Curtis dendogram (A) and graph (B) of occurrence of manatees in
247
sampling sectors based on aerial sightings, stranding and information from fisherman.
248
249
115
250
DISCUSSION
251
The present study updates information on the distribution seagrass beds in northeastern
252
Brazil and is the first study to relate the occurrence of these plants to the Antillean
253
manatee in the country. The mapping of seagrass increases the number of beaches with
254
records of these plants by 69% in comparison to data found during previous surveys
255
carried out in the region (Laborel-Deguen, 1963; Den Hartog, 1972; Oliveira-Filho et
256
al., 1983; Magalhães and Cazuza, 2005; Vieira, 2006; Reis, 2007; Silva, 2010; Silva et
257
al., 2012), demonstrating a greater knowledge of the distribution of seagrasses in this
258
part of northeastern Brazil.
259
Despite the increase in the number of records seagrass, was not observed a statistic
260
correlation between occurrence these plants and the manatees. This lack of correlation
261
may be associated with the reduction in these foraging grounds due to countless human
262
activities impactful in their habitats and/or the manatees’ generalist habit of herbivory
263
due to their possibly broad home range.
264
Most studies addressing the dependence of the manatees on seagrass beds in Brazil
265
are restricted to information from specific sites and therefore classify the feeding
266
preferences of this species in a qualitatively suggestive manner (Banks and
267
Albuquerque-Neto, 1985; Lima, 2008; Costa, 2006). However, two studies stand out for
268
direct indication of the diet of T. m. manatus in northeastern Brazil. In the first study,
269
according to fishermen who hunted the species, the main food found in the intestinal
270
tract of manatees killed were species Halodule sp. and Halophila sp. (Lima, 1997). In
271
the other study, the diet of the Antillean manatee based on fecal and stomach samples
272
collected in northeastern Brazil demonstrates that these mammals consume a diversity
273
of food items, with a preference for macroalgae (Borges et al., 2008). This last may
116
274
explain the lack of a direct correlation between T. m. manatus and seagrass beds in the
275
present study. Moreover, large home ranges are suggested for reintroduced manatees
276
specimens in northeastern Brazil (Lima, 2008), which could explain both the variety of
277
food resources used by native animals as well as the low degree of dependence on local
278
seagrass beds.
279
280
Characterization of seagrass habitats
281
The lack of previous information on the occurrence of seagrass, the extensive coastline
282
and turbid coastal waters limited the localization and detailed characterization of
283
seagrass habitats in the present study. Seagrass beds can be mapped using a range of
284
approaches from in situ observations to remote sensing (McKenzie, 2003). Sampling
285
can vary on a scale ranging from meters to kilometers and may include aerial
286
photographs and satellite images (McKenzie et al., 2001). In small areas with turbid
287
waters, methods involving underwater monitoring with video cameras may overcome
288
the difficulty in spotting seagrass beds (Adulyanukosol and Poovachiranon, 2006)
289
However, for large areas, as in the present study large scale, seagrass bed identification
290
studies are first needed, followed by more detailed studies on a smaller geographic scale
291
adjusted to each type of environment.
292
The species of seagrass identified in the present study (Halodule wrightii, Halophila
293
decipiens and R. maritima) represent the three genera of the five species of seagrass
294
found along the coast of Brazil (Oliveira-Filho et al., 1983). The present findings are in
295
agreement with those reported in previous studies, which describe H. wrightii as the
296
species with the widest distribution in the northeastern region, followed by H. decipiens
297
(Laborel-Deguen, 1963; Olivieira-Filho et al., 1983; Magalhães and Alves, 2002). The
117
298
coexistence of two or more species in the same seagrass bed, as occurred with Halodule
299
wrightii and Halophila decipiens in the present study, seems to be a common pattern in
300
seagrass occurrence (Hemminga and Duarte, 2000). However this definition was
301
contrary the past studies in the Paraíba e Pernambuco states, where Halophila decipiens
302
completely eliminates Halodule wrightii when both grow in one place (Laborel-Deguen,
303
1963). This proves the importance of this study re-evaluating the occurrence patterns of
304
seagrasses in northeastern Brazil.
305
In Brazil, the distribution of seagrass of these genera was previously described
306
exclusively for the marine environment (Oliveira-Filho et al., 1983). Recently, however,
307
shoal grass has been described in estuarine environments in the state of Pernambuco
308
(northeastern region of the country) (Reis, 2007). The presence of Halodule wrightii
309
and Halophila decipiens within or near the estuaries mapped in the present study offers
310
further evidence of the diversity of environments occupied by these species (Short et al.,
311
2007), which may also be exploited by the Antillean manatee. The type of habitat in
312
which R. maritima was found (coastal lagoon complex) is common to species of this
313
genus, which develop in calm waters with low salinity, as found in mangroves, estuaries
314
and coastal lagoons (Creed, 2000; Short et al., 2007).
315
316
Distribution of manatees versus seagrass
317
The use of coastal habitats and estuaries is also characteristic of the spatial distribution
318
of the manatees for feeding throughout the world (Olivera-Gómez and Mellink, 2005;
319
Lima, 2008; Rodas-Trejo et al., 2008; Lima et al., 2011). The greater number of
320
occurrences of these mammals in estuaries with preserved mangroves in northeastern
321
Brazil (Alves et al., unpublished data) suggests greater use of these habitats for foraging
118
322
activities. In such ecosystems, the availability of food items is considerably broader due
323
to the additional provision of freshwater macrophytes, which make up part of the diet of
324
the Antillean manatee in the region (Borges et al., 2008). The opportunistic, generalist
325
habits of herbivory of T. m. manatus (Hartman, 1979) lead to an increase in the spatial
326
area of use and reduces the dependence of the species on seagrass beds. Sheltered areas
327
in the interior of estuaries ensure the protection of these mammals and their food
328
resources. Therefore, the diversified use of food items seems to be mainly associated
329
with the type of resources available. For example, manatees in the northern portion of
330
the Gulf of Mexico feed mainly on submerged and floating vegetation (Hartman, 1979;
331
Smith, 1993), whereas manatees in South America and on the northern coast of the state
332
of Florida (USA) commonly consume mangrove vegetation (Smethurst and
333
Nietschmann, 1999; Borges et al., 2008).
334
The greater number of records of seagrass in shallows coastal waters along the
335
northeastern coast of Brazil (mean depth: 1.28 m) may be related to the shape and
336
distance of the reefs in relation to the coastline. Reefs offer shelter from strong winds
337
and currents and lower depths assist in the protection of seagrass from hydrodynamics,
338
as reported for other locations (Laborel-Deguen, 1963; Kempf, 1970; Koch, 2001). In
339
the state of Rio Grande do Norte, which has the widest continental shelf among the
340
states mapped herein, the semi-arid climate and low degree of influence from estuaries
341
with regard to nutrient content (Muehe and Garcez, 2005) make the coastal environment
342
in this state less productive. Thus, the presence of offshore reef patches (Castro and
343
Pires, 2001) likely allows the occurrence of seagrasss beds at greater distances from the
344
shore (5.5 km to 7.6 km) and at greater depths (3 to 10.20 m), as reported by Silva
345
(2010), by offering shelter and adequate water transparency, which are necessary to the
119
346
survival of these plants. The maximum depths of occurrence of H. wrightii, H. decipiens
347
and species of the genus Ruppia can reach 10 m (Laborel-Deguen, 1963), 85 m (Den
348
Hartog, 1970) and 3 m (Creed, 2000), respectively.
349
The presence of the Antillean manatees at depths of 14.8 m and between 0.4 and 3.9
350
km from shore in northeastern Brazil (Borobia and Lodi, 1992; Paludo and Langguth,
351
2002; Costa, 2006; Alves, unpublished data) is similar to the patterns of occurrence of
352
seagrass in the present study. In the state of Florida (USA), all species of seagrass are
353
found at depths used by manatees during foraging activities (Smith, 1993). The
354
localization of food resources is essential to the determination of the distribution of
355
manatees (Hartman, 1979; Lefebvre et al., 2000; Olivera-Gómez and Mellink, 2005;
356
Rodas-Trejo et al., 2008; Langtimm et al., 2011).
357
The simultaneous records of occurrence of manatees and seagrass at 27 of the
358
beaches studies herein (66% of beaches with seagrass) suggest the spatial use of these
359
ecosystems, despite the lack of a significant correlation between them. It is possible that
360
the occurrence of the Antillean manatee is more influenced by other characteristics of
361
seagrass beds, such as extension and area of coverage as well as the density and biomass
362
of the plants. However, this type of assessment requires an intensive effort on the local
363
scale, which is unviable when working on a spatial scale as large as that used in the
364
present study.
365
Another explanation for the lack of a correlation between the records of occurrence
366
of seagrass and the Antillean manatee may be the potentially broad home range of these
367
mammals. Although only conducted with captive animals that were reintroduced into
368
the wild, studies on the home range of the Antillean manatee on the coast of
369
northeastern Brazil report considerable diversity in the size of the area exploited by the
120
370
different specimens observed (Lima, 2008). Some animals remain restricted to small
371
home ranges, whereas others can travel as many as hundreds of kilometers in a few
372
days, using resources in a broad geographic area (Lima op. cit.). This variable behavior
373
in terms of the area use has been described for manatees in the state of Florida (USA),
374
suggesting that long-distance migration allows the use of habitats that are favorable to
375
foraging (Deutsch et al., 2003). Considering observations of specimens that have been
376
reintroduced into the wild, native animals are also thought to exhibit this variable
377
behavior in terms of the extension of area use and it would therefore be natural not to
378
observe records of the simultaneous occurrence of seagrass and the Antillean manatee.
379
The bibliographic data on the occurrence of seagrass serve as a comparative
380
parameter in the assessment of the current state of conservation of seagrass beds.
381
Itamaracá Island beach on the northern coast of the state of Pernambuco (sector 7)
382
exemplifies this. The area in question has been described as one of the beaches with the
383
greatest indices of H. wrightii biomass and density on the coast of Brazil (Kempf, 1970;
384
Magalhães and Eskinazi-Leça, 2000; Magalhães and Alves, 2002). In the present study,
385
however, this site was characterized by only small patches of seagrass beds. The impact
386
of urban development, boat traffic, shellfish extraction and beach seine fishing activities
387
may have contributed to this reduction (Pitanga et al., 2012). However, it is likely that
388
local extraction of approximately 20 tons per year of shoal grass for the feeding of
389
Antillean manatees maintained in captivity at the Aquatic Mammal Center [Centro
390
Mamíferos Aquáticos] beginning in the 1960s (Banks and Albuquerque-Neto, 1985;
391
Magalhães and Alves, 2002) is a relevant factor and should be studied in details. In
392
order to minimize the damage to these ecosystems, a seagrass collection protocol was
393
created in northeastern Brazil (Pitanga et al., in press), which has led to the interruption
121
394
of plant collection when seagrass abundance is low. As this area is considered an
395
important habitat for the Antillean manatee, with records of occurrence based on
396
information from fishermen (Lima et al., 2011) as well aerial sightings (Alves et al.,
397
unpublished data), the reduction in seagrass coverage may compromise directly the
398
foraging activities of this species. To support the conservation and further research in
399
the area, worldwide studies on feeding ecology of manatees and dugongs, based on both
400
aerial and nautical surveys, demonstrates that these animals are most frequent registered
401
in areas with a greater abundance of seagrass (Provancha and Hall, 1991; Lefebvre et
402
al., 2000; LaCommare et al., 2008; Semeyn et al., 2011).
403
Among the species of seagrass identified in the present study, only R. maritima is not
404
included in the diet of T. m. manatus in northeastern Brazil. However, according to
405
fishermen and researchers of the Aquatic Mammal Center, this species is currently
406
collected and offered to manatees in captivity in the northern portion of the state of
407
Alagoas (sector 9) and serves as a potential food resource for manatees that have been
408
reintroduced into the wild in the area. The consumption of this species is described for
409
manatees in Chetumal Bay (Gulf of Mexico) (Castelblanco-Martínez et al., 2009) and
410
the state of Florida (USA) (Hartman, 1979; Reich and Worthy, 2006).
411
In the literature, the largest numbers of records of seagrass occurred in sectors 7 and
412
8, where studies have been carried out since the 1960s (Laborel-Deguen, 1963).
413
Regarding the records in the current mapping, seagrass was identified in all sectors
414
(except sector 12), with sector 6 standing out due to the greater number of records.
415
These results indicate that sectors 6, 7 and 8 are the most important regarding the
416
abundance of seagrass in the study area. Moreover, the findings underscore the
417
importance of the state of Pernambuco to the execution of studies on seagrass over the
122
418
years (Kempf, 1970; Reis, 2007; Freire et al., 2008) as well as the need to increase
419
efforts in previously unexplored areas, such as sites in the states of Alagoas and Paraíba,
420
which had a high number of current records of seagrass.
421
On the coast of the states of Paraíba and Pernambuco (sectors 5 to 8), the high
422
number of records of occurrence of both seagrass and the Antillean manatee indicate
423
that this region is favorable to the survival of the species studied. These areas are
424
characterized by a narrow continental shelf (Muehe and Garcez, 2005), reefs parallel to
425
the shoreline (Castro and Pires, 2001) and a high degree of connectivity among coastal
426
ecosystems (Pereira et al., 2010; Silva-Falcão et al., 2012), which makes this region
427
rich in species diversity and protected from extreme oceanographic action.
428
429
CONCLUSION
430
The lack of a correlation between the records of occurrence of seagrass and the
431
Antillean manatee may be associated to the reduction in these potential foraging
432
grounds and/or the generalist habit of herbivory on the part of the Antillean manatee,
433
with allows it to consume different types of food resources throughout its variable home
434
range. Despite the lack of a significant correlation, the present findings emphasizes the
435
importance of directing efforts toward reducing additional losses of seagrass beds in
436
northeastern Brazil, especially in areas with the simultaneous occurrence of the
437
Antillean manatee. Therefore, seagrass beds should be considered potential foraging
438
grounds for this species, which justifies the efforts of future studies on these plants and
439
as habitats for the release of captive manatees in northeastern Brazil. The mapping of
440
areas of occurrence of seagrass beds is useful to the drafting of regional management
123
441
plans and specific legislation to prevent the further decline of these ecosystems, which
442
are important ecosystems for manatees throughout the world.
443
444
ACKNOWLEDGMENTS
445
The authors would like to thank the Universidade Federal de Pernambuco (UFPE) and
446
the Fundação Mamíferos Aquáticos (FMA) for supporting the survey; the Fundação
447
Grupo o Boticário for sponsoring the survey; the Conselho Nacional de
448
Desenvolvimento Científico e Tecnológico (CNPq) for the doctoral scholarship granted
449
to the first author; the many fisherman and researchers (Cláudio Macedo, Marcos
450
Vinícius, Daniel Lippi, Helen Barros, Janson Joab, Viviane Melo, Caroline Feitosa,
451
João Borges, Iran Normande, George Miranda, Natália Carla and others) who helped in
452
the search for seagrass habitats in northeastern Brazil. This study is part of the doctoral
453
thesis of the first author.
454
455
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Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
Considerações finais
O conhecimento sobre o padrão de distribuição espacial da megafauna marinha
costeira e a abundância de espécies criticamente ameaçadas de extinção, como o
peixe-boi marinho, é fundamental para o estabelecimento de diretrizes de gestão e
manejo dos principais ecossistemas funcionais aos animais. Essas pesquisas são
consideradas prioritárias e urgentes pelos planos de ação de mamíferos aquáticos e
tartarugas marinhas do Brasil.
As considerações aqui apresentadas sobre a distribuição espacial, a abundância e
a caracterização dos habitats de ocorrência da megafauna marinha, na costa nordeste
do Brasil, representam o primeiro passo para se compreender o padrão de distribuição
e uso de habitats das espécies por meio de metodologia aérea, além de quantificar as
ações antropogênicas negativas à manutenção do equilíbrio ecológico.
O emprego de levantamento aéreo piloto no norte de Alagoas, para avaliar a
viabilidade dessa ferramenta em estudos de distribuição e estimativa populacional da
megafauna no nordeste do Brasil, foi considerado satisfatório pelo número de peixesbois, golfinhos e tartarugas observados e pelas condições ambientais favoráveis ao
monitoramento, como elevada transparência da água e ventos amenos. No entanto, a
elevada turbidez da água no interior dos estuários limitou a detecção dos animais,
sendo esses ecossistemas retirados das futuras amostragens.
A quantificação e a análise em larga escala geográfica da distribuição espacial de
peixes-bois, golfinhos e tartarugas, entre os estados do Piauí e Alagoas, evidenciaram a
importância dos habitats costeiros e estuarinos e das atividades humanas para a
ocorrência das espécies. Os estuários preservados e os recifes costeiros, analisados
133
Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
neste estudo, foram considerados ecossistemas de extrema importância na
distribuição da megafauna, por serem propícios à reprodução, alimentação e descanso
de diversos táxons, principalmente dos peixes-bois marinhos. No entanto, destacou-se
a exploração desses habitats para atividades humanas diversas, como o
desenvolvimento urbano e as atividades de pesca, que podem levar a redução de suas
funcionalidades ecológicas de modo drástico, com a subsequente fragmentação dos
habitats de ocorrência das espécies. A intensidade dos impactos antropogênicos
costeiros vem, ao longo dos anos, acarretando a degradação ambiental de habitats
essenciais à sobrevivência de diversas espécies da megafauna, consideradas
organismos-chave para a conservação marinha. Ressaltou-se a importância das Áreas
Marinhas Protegidas na conservação da megafauna, evidenciando a importância da
criação de novos habitats protegidos para as espécies vulneráveis às ações humanas.
A abundância de peixes-bois ao longo da costa nordeste do Brasil, com pouco mais
de 1000 indivíduos, representou os primeiros dados de tamanho populacional de T. m.
manatus em distribuição mais ao sul da América, utilizando a ferramenta padrão de
monitoramento aéreo. O arranjo estatístico adotado, com a incorporação de dados
bibliográficos e avistagens aéreas dentro e fora do esforço amostral, foi necessário
devido à provável dispersão das populações em uma grande extensão costeira,
podendo induzir a erros de subestimativa de abundância. Por isso, é fundamental que
novos estudos sejam realizados em áreas consideradas hot spots de abundância dos
peixes-bois, para que haja um refinamento nas estimativas futuras.
Em particular, a não correlação dos registros de ocorrência das angiospermas
marinhas com os peixes-bois sugere que as prováveis reduções desses habitats de
134
Habitats da megafauna marinha na costa nordeste do Brasil, com ênfase em peixes-bois.
forrageio possam interferir no padrão de distribuição da espécie. Além disso, o hábito
herbívoro generalista dos animais, com a utilização de uma extensa e variável área de
vida, propicia o acesso a diferentes fontes alimentares, não havendo, portanto, uma
dependência direta dos animais com as plantas. O mapeamento das áreas de
ocorrência das angiospermas marinhas é uma ferramenta útil para auxiliar na
elaboração de planos regionais de gestão e legislação específica, visando o manejo e à
prevenção do declínio desses ecossistemas, considerados fundamentais aos peixesbois em todo o mundo.
135
APÊNDICE
136
Biological Conservation 161 (2013) 91–100
Contents lists available at SciVerse ScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Aerial survey of manatees, dolphins and sea turtles off northeastern
Brazil: Correlations with coastal features and human activities
Maria Danise de Oliveira Alves a,b,⇑, Ralf Schwamborn c, João Carlos Gomes Borges b,d, Miriam Marmontel e,
Alexandra Fernandes Costa f, Carlos Augusto França Schettini a, Maria Elisabeth de Araújo a
a
Department of Oceanography, Federal University of Pernambuco (UFPE), Cidade Universitária, s/n, Recife-PE 50670-901, Brazil
‘‘Fundação Mamíferos Aquáticos’’ (FMA), 17 de agosto, Casa Forte, 2001, Recife-PE 52061-540, Brazil
Department of Zoology, UFPE, Cidade Universitária, s/n, Recife-PE 50670-901, Brazil
d
Post-graduation Program in Tropical Animal Sciences, Federal Rural University of Pernambuco (UFRPE), Dom Manoel Medeiros, Dois Irmãos, s/n, Recife-PE 52171-900, Brazil
e
‘‘Instituto de Desenvolvimento Sustentável Mamirauá’’ (IDSM), Estrada do Bexiga 2.584, Bairro Fonte Boa, Tefé-Amazonas 69470-000, Brazil
f
Post-graduation Program in Aquatic Ecology and Fishery, Federal University of Pará (UFPA), Cidade Universitária, José Silveira Neto, Rua Augusto Corrêa 01,
Guamá-Belém-Pará 66075-110, Brazil
b
c
a r t i c l e
i n f o
Article history:
Received 7 August 2012
Received in revised form 27 November 2012
Accepted 24 February 2013
Keywords:
Manatees
Dolphins
Sea turtles
Aerial surveys
Northeastern Brazil
a b s t r a c t
The objective of the present study was to analyze the distribution of manatees, dolphins and sea turtles
off northeastern Brazil through aerial surveys, relating them to specific habitats and human activities,
with emphasis on marine protected areas (MPAs). Surveys were conducted between January and April
2010 at 150 m altitude and 140 km h1, using two independent observers. Strip transects were flown
in a zigzag pattern. Transects covered 4026 km in more than 27 flight hours. A total of 36 sightings of
manatees (Trichechus manatus manatus, 41 individuals), 28 of dolphins (Delphinidae, 78 individuals,
including 10 Sotalia guianensis) and 256 of sea turtles (Cheloniidae, 286 individuals) were recorded. Manatees and sea turtles displayed solitary habits, while dolphins were commonly seen in groups. Manatees
were positively correlated with sea turtles, probably due to their preference for sheltered shallow habitats with favorable conditions for foraging and resting. Furthermore, manatees showed a positive relationship with mangrove estuaries, and medium-sized coastal cities probably due to the intense urban
development in many estuarine areas. Manatees and sea turtles were also positively correlated with
boats, showing a severe threat for these species. Density of manatees was significantly higher within
MPAs with preserved mangrove estuaries than in non-protected areas, while dolphins and sea turtles
were observed in high densities MPAs with coral reefs. The elevated density of these organisms shows
the vital importance of protecting and adequately managing unique ecosystems to ensure a sustainable
future for the populations of severely threatened species.
Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction
Marine mammals and sea turtles are considered key organisms
for marine conservation in several parts of the world (Chatwin,
2007). Many populations of these animals occur in coastal areas
that are intensively used by local people (Ojeda-Martínez et al.,
2011), which make them vulnerable or threatened by extinction
(IUCN, 2012). Marine protected areas (MPAs) are thus essential
tools to ensure the conservation of these organisms and their
⇑ Corresponding author at: Department of Oceanography, Federal University of
Pernambuco (UFPE), Cidade Universitária, s/n, Recife-PE 50670-901, Brazil. Tel.: +55
81 96851342.
E-mail addresses: [email protected] (M.D.d.O. Alves), [email protected]
(R. Schwamborn), [email protected] (J.C.G. Borges), marmontel@
mamiraua.org.br (M. Marmontel), [email protected] (A.F. Costa),
[email protected] (C.A.F. Schettini), [email protected] (M.E.d. Araújo).
0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biocon.2013.02.015
ecosystems (Hooker and Gerber, 2004). However, the efficiency
of MPAs should be based on thorough surveys (Ojeda-Martínez
et al., 2011), which in effect, are often incipient or too small-scaled
spatial (Witt et al., 2009; Panigada et al., 2011; Knip et al., 2012).
Large-scale studies that quantitatively determine the correlations
between endangered species, such as manatees, dolphins and sea
turtles, coastal features and human activities are rare.
In northeast Brazilian waters, the most important threats to
coastal biodiversity are fisheries and intensive urban development,
thus turning this region one of the most vulnerable within South
America (Chatwin, 2007). The most common marine mammals in
the coastal zone off northeastern Brazil are the Antillean manatee
(Trichechus manatus manatus) (Lima et al., 2011) and 19 species of
cetaceans, among which the Guiana dolphin (Sotalia guianensis) is
the most frequent species (Alvite et al., 2004). Also, this region
occur five of the seven living species of sea turtles, the loggerhead
(Caretta caretta), hawksbill (Eretmochelys imbricata), olive ridley
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M.D.d.O. Alves et al. / Biological Conservation 161 (2013) 91–100
(Lepidochelys olivacea), leatherback (Dermochelys coriacea), and the
green turtle (Chelonia mydas), the most common species in Brazil
(Marcovaldi and Marcovaldi, 1999). Antillean manatee is the most
endangered aquatic mammal in Brazil (ICMBio, 2011), being classified internationally as ‘‘endangered’’ as S. guianensis is listed as
‘‘data deficient’’ (IUCN, 2012). All sea turtles mentioned are under
threat, D. coriacea and E. imbricata being classified as ‘‘critically
endangered’’, C. caretta and C. mydas as ‘‘endangered’’ and L.
olivacea as ‘‘vulnerable’’ (IUCN, 2012).
Aerial surveys are considered a standard technique to assess
distribution, abundance and habitat characteristics of marine
mammals and sea turtles worldwide (e.g. Preen, 2004; Edwards
et al., 2007; Certain et al., 2008; Witt et al., 2009; Jean et al.,
2010; Langtimm et al., 2011). In Brazil, however, few studies have
been based on aerial surveys (Secchi et al., 2001; Andriolo et al.,
2006, 2010; Danilewicz et al., 2010; Zerbini et al., 2010, 2011;
Wedekin, 2011). In the northeastern coast, only one single aerial
survey of manatees was performed on a local scale off Ceará state
(Costa, 2006).
The objective of the present study was to quantify and analyze
the large-scale spatial distribution of manatees, dolphins and sea
turtles off northeastern Brazil, in relation to habitat characteristics,
current human activities, and the importance of MPAs for the conservation of these animals.
2. Materials and methods
2.1. Study area
The northern limit of the study area was the mouth of the Parnaíba River Delta, around Canárias Island (02°440 S, 41°470 W), Piauí
State. The southern limit was the mouth of the São Francisco River
(10°300 S, 36°240 W), located in Alagoas State (Fig. 1).
The northeastern coast of Brazil extends for approximately
3400 km and displays variety of environments such as beaches,
dunes, cliffs, coral reefs, mangrove estuaries, and seagrass beds,
each being governed by specific dynamics and anthropogenic vulnerabilities (Cunha, 2005; Muehe and Garcez, 2005). The continental shelf is 85 km wide in the north and narrows to 40 km in the
southern part. Climate is tropical, with high temperatures and
salinities, and low concentrations of nutrients, except for estuarine
areas, where primary productivity and biomass are high (Muehe
and Garcez, 2005).
There are four relevant Marine Protected Areas (MPAs) in this
region, each with its specific conservation targets: ‘‘Delta do Rio
Parnaíba’’ (manatees, mangroves, beaches, sand banks, estuaries,
coastal grasslands, marshes, dunes, lakes and lagoons), ‘‘Recifes
de Corais’’ (defined around the ‘‘Parrachos de Maracajaú’’ offshore
coral reefs), ‘‘Barra do Rio Mamanguape’’ (manatees, mangroves,
Fig. 1. Map of the study area between the states of Piauí and Alagoas, northeastern Brazil (a) showing the main Marine protected areas (DP – Delta do Rio Parnaíba, RC –
Recifes de Corais, BM – Barra do Rio Mamanguape, CC – Costa dos Corais) and coastal cities (black squares). Inlet: Aerial transects in a zigzag pattern in the marine protected
area Delta do Rio Parnaíba (b).
M.D.d.O. Alves et al. / Biological Conservation 161 (2013) 91–100
93
Fig. 2. Spatial distribution of manatees, dolphins and sea turtles between the states of Piauí and Alagoas, northeastern Brazil. Marine protected areas are indicated as gray
rectangles (DP: Delta do Rio Parnaíba, RC: Recifes de Corais, BM: Barra do Rio Mamanguape, CC: Costa dos Corais). White rectangle: area with scarce sightings. A single
sighting of manatee mother and calf is highlighted in a circle, and specimens of Sotalia guianensis in light blue color. Dotted lines: state borders. (For interpretation of the
references to color in this figure legend, the reader is referred to the web version of this article.)
lagoons, sand banks) and ‘‘Costa dos Corais’’, Brazil’s largest MPA
(manatees, coral and sandstone reefs, estuarine mangroves) (Figs. 1
and 2). Their function is to protect and preserve natural resources
and to promote sustainable development (FAO, 2011).
2.2. Aerial surveys
Aerial surveys were accomplished after a pilot study (Alves
et al., 2013), using a single-engine Cessna 172 A aircraft with a
high-wing design to facilitate viewing the sea surface. It was
adapted with bubble windows at the rear (Zerbini et al., 2010,
2011), allowing for a wider viewing angle. Sampling was performed using the strip transect method, assuming that all animals
within the strip (a band of fixed width on each side of the transect
line) were detected and counted (Jolly, 1969). This method has
been widely applied for marine mammals and sea turtles (Cardona
et al., 2005; Certain et al., 2008; Witt et al., 2009; Langtimm et al.,
2011; Katsanevakis et al., 2012).
A total 899 lines transects were made in a zigzag pattern, with
an angle of turn of 40°, as to better cover the area and to maximize
the flying effort (Secchi et al., 2001; Cardona et al., 2005; Andriolo
et al., 2006, 2010). The surveyed areas extended from estuarine inlets, especially aiming at sightings of manatees, to the isobaths of
10–20 m (Fig. 1). The flight was standardized with 150 m altitude
and 140 km h1 speed, which is within the range found in other
aerial surveys (Morales-Vela et al., 2000; Olivera-Gómez and Mellink, 2005; Roos et al., 2005; Costa, 2006; Langtimm et al., 2011).
The widest sighting angle (approximately 65°) was determined
with a clinometer during a test flight, and resulted in a sampled
width of 321.7 m per observer (i.e., the total strip width equals
643.4 m) (Alves et al., 2013). Sea conditions were Beaufort Sea
state 2 or less (Certain et al., 2008), characterized by flat or calm
sea, and conditions of visibility and water transparency between
‘‘excellent’’ and ‘‘average’’. Aerial surveys were conducted during
the dry season, between January and April 2010, in the morning
period and at high tide, when the animals have a better access to
shallow foraging areas such as macroalgal banks and seagrass beds
(Paludo and Langguth, 2002; Olivera-Gómez and Mellink, 2005),
and to reduce the potentially confusing effect of reefs and algae
sandstone substrates that appear at low tide (Costa, 2006; Alves
et al., 2013).
Observations were performed by two independent observers, located at each of the side windows to minimize perception bias
(Langtimm et al., 2011), and who were wearing polarized sunglasses
to minimize the effect of glare on the water surface and accentuate
the color gradient. A registrar, in the front beside the pilot, used a
GPS to indicate sighting points, in addition to the GPS of the plane,
which recorded the route. The registrar also used two photographic
cameras, a portable recorder, and nautical charts to compile the field
records. Each flight lasted for less than 3 h per day.
All identifications were based on morphological and characteristic behavioral diagnostics. Calves corresponded to specimens
measuring up to 1/3 of the adult size (Hartman, 1979). Two or
more animals were defined as a group (Morales-Vela et al.,
2000). In cases of doubtful sightings or imprecise counts, a circular
flight around the sighting point was carried out to confirm identification (Morales-Vela et al., 2000; Langtimm et al., 2011).
Approximately 1500 km of coastline were flown over in six Brazilian states, totaling 4026 km along the zigzag path (Fig. 1). The
total coverage area was 2590.2 km2, calculated as the zigzag path
multiplied by the strip width (643.4 m). The effective effort exceeded 27 flight hours in 11 days. A stretch of only 22 km coastline
was not surveyed, due to traffic restrictions around the Recife
international airport (Fig. 1).
2.3. Data analysis
Sighting data were transferred to GIS using the Arcmap software (version 9.2) and received identification numbers and coordinates. The data were plotted on nautical charts (1:300.000) to
obtain isobaths and maximal depths for each sighting (with tide
at 0.0 m).
A descriptive analysis of the large-scale distribution patterns of
marine mammals and sea turtles was carried out in the different
areas. The results were also used to perform statistical analyses
of potential relationships between the sightings of these animals,
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M.D.d.O. Alves et al. / Biological Conservation 161 (2013) 91–100
Table 1
Summary of the sightings of manatees, dolphins and sea turtles during aerial surveys
in northeastern Brazil.
Individuals
Sightings
Mean N/sighting
Maximum N/sighting
Positive segmentsa
Positive segments (%)a
Maximum N/segmenta
Manatees
Dolphins
Sea turtles
41
36
1.1
2
29
10
3
78
28
2.8
8
24
8
10
286
256
1.1
2
127
43
10
a
The coastline was divided into 294 segments of 5 km in length. Positive segments are those where sightings occurred.
(6) Estuarine mouths (complex, mangrove, partially obstructed sandy barrier/small: 0.01–0.05 km, intermediate: 0.06–0.1 km, large:
above 0.1 km), and (7) coastal urban centers (small < 180 km2, medium-sized: 180–840 km2, large > 840 km2) (IBGE, 2007).
Spearman rank correlation analysis (Zar, 1996) was used to test
for significant correlations between human activities, coastline features, MPAs, and animal abundance per segment. This method of
correlation analysis was chosen due to the non-linearity of relationships and non-normality and heteroscedascity of most distributions.
All analyses were performed using the ‘‘R’’ language and environment at a = 0.05 (R Development Core Team, 2009, version 2.9).
3. Results
human activities, and coastline features. For this purpose, the coastline under investigation was divided into 294 segments of 5 km
length. For each segment, seven ecological and human parameters
were examined. During flights, the following information of occurrence records was obtained for each segment: (1) animal abundance,
(2) coastal zone occupation patterns (shrimp farms, salt works and
ports), and (3) fishing and tourism activities (trawling boats, motor
boats, sail boats, and rowing boats). Based on cartographic and
bibliographic analysis, the following were diagnosed: (4) MPAs
(‘‘Delta do Rio Parnaíba’’, ‘‘Recifes de Corais’’, ‘‘Barra do Rio Mamanguape’’ and ‘‘Costa dos Corais’’), (5) Reefs (Northern Beach Rocks,
Offshore Reef Patches, Coastal Reef Lines) (Castro and Pires, 2001),
3.1. Distribution of sightings
A total of 320 sightings of marine mammals and sea turtles
were recorded during the surveys. Of these, 36 were sightings of
Antillean manatees (41 individuals), 28 were sightings of dolphins
(Delphinidae, 78 individuals), with 10 individuals identified as S.
guianensis, and 256 were sightings of sea turtles (Cheloniidae,
286 individuals) (Fig. 2 and Table 1). Although it was generally possible to see head, carapace and fins of turtles on the surface, this
was not sufficient for identification at species level. Fish were also
spotted occasionally, including 22 sightings of individual flying
fish, seven unidentified large schools, seven rays and two sharks.
Fig. 3. Frequency histograms of depth (m) and distance from shore (km) at the sighting locations for manatees (a and b), dolphins (c and d), and sea turtles (e and f) in
northeastern Brazil. Data are based on 27 h of aerial surveys carried out along the northeastern Brazilian coast from the states of Piauí to Alagoas.
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M.D.d.O. Alves et al. / Biological Conservation 161 (2013) 91–100
Marine mammals and sea turtles were recorded throughout the
study area, except along approximately 130 km of coastline around
the western portion of the state of Rio Grande do Norte (Potiguar
Basin), where only a single sea turtle sighting occurred (Fig. 2).
Manatees and sea turtles were most frequently observed as solitary animals (86.1% and 88.3%, respectively), or as groups of two
adults. A pair of manatee mother and calf was sighted only once,
at Barreta beach (06°060 S, 35°040 W, Rio Grande do Norte). Dolphins
were generally found in groups (64.3%) composed of two to eight
individuals (mean: 4.4 individuals per group) (Fig. 2 and Table 1).
Sightings of all three taxa were concentrated within 2–10 m
depth (Fig. 3). Manatees were clearly concentrated in shallower
areas, being most frequently sighted within 6–8 m depth, reaching
a maximum local depth of 14.8 m. Regarding the distance from the
coast, manatees were also clearly concentrated in areas closest to
shore, being most frequently sighted at distances that ranged from
only 0.01 to 3.9 km from the coast, with a continuous decrease in
frequency toward offshore areas. Accordingly, this species showed
the lowest mean distance from the coast, with only 1.2 km, as compared to 2.1 km for dolphins and for sea turtles. Dolphins showed
maximum frequency at the 8–10 m isobath, and three sightings occurred within the 16–18 m isobaths. Dolphins showed a more offshore distribution (0.1–4.4 km from the coast), with higher
frequencies in the central part of the surveyed area, at 1.5–
2.0 km from the coast. Guiana dolphins were recorded between
2.1 and 9.2 m depth and between 1.6 and 3.2 km from the coast.
The highest maximum values of depth and distance from the coast
were recorded for sea turtles, with 18.5 m and 5 km, respectively,
with high frequencies throughout the surveyed area (Figs. 2 and 3).
Spearman rank correlation analysis showed that manatees were
positively correlated with sea turtles (p = 0.032, Table 2), while
dolphins were not correlated with any of these groups.
Table 2
Results of Spearman correlation analysis of sightings of manatees, dolphins, sea
turtles, selected coastal features and human activities, based on 27 h of aerial surveys
in northeastern Brazil. Values given in the table are ‘‘p’’ values of the analyses based
on N = 294 coastal segments of 5 km in length.
3.2. Correlations of coastal features and human activities
n.s.: not significant at a = 0.05.
Spearman rank correlation analysis detected several significant
correlations of coastline features and human activities with the
density of manatees, dolphins and sea turtles (Table 2). A significant positive correlation of manatee sightings with reef habitats
was detected for ‘‘Northern Beach Rocks’’ (p = 0.0089). For sea turtles, sightings were also positively correlated with ‘‘Northern
Beach Rocks’’ (p = 0.0041) and ‘‘Offshore Reef Patches’’
(p = 0.0012). A significant positive correlation (p = 0.027) was detected between the density of open, mangrove-lined estuaries
and manatee sightings. Other estuarine types such as partially obstructed sand bar (barrier) estuaries or seasonally obstructed sand
bar estuaries, which are both typical of coasts with sandy beaches,
sand bars, sand banks, dunes, strong wave action and wind-driven
currents, showed no correlation with the density of manatees. Dolphin sightings were positively correlated with large estuaries
(p = 0.027) and mangroves (p = 0.023) (Table 2).
Manatee sightings were positively correlated with the presence
of medium-sized cities (p = 0.034) and motor boats (p = 0.011). Sea
turtles were positively correlated with the total number of fishing
boats (p = 0.030) and with motorized boats (p = 0.0017). Shrimp
farms, salt works and ports did not show any positive or negative
correlations with any animals (Table 2).
3.3. Marine protected areas (MPAs)
Significant positive correlations with MPAs were detected for
manatees, dolphins and sea turtles, and varied considerably between taxonomic groups and areas (Fig. 4 and Table 3). When considering all four MPAs and comparing sightings in these areas to
areas outside MPAs, manatees were the only group to show significantly higher density within MPAs (Table 3). The average density
Spearman correlation
Manatees
Dolphins
Sea turtles
Manatees
Dolphins
Sea turtles
–
n.s.
0.032
n.s.
–
n.s.
n.s.
n.s.
–
Reefs
Northern Beach Rocks
Offshore Reef Patches
Coastal Reef Lines
0.0089
n.s.
n.s.
n.s.
n.s.
n.s.
0.0041
0.0012
n.s.
Estuarine mouths
Estuaries (all)
Small
Medium
Large
Complex
Mangrove
Sandy barrier
n.s.
n.s.
n.s.
n.s.
n.s.
0.027
n.s.
n.s.
n.s.
n.s.
0.027
n.s.
0.023
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
Land use
Shrimp farms
Salt works
Ports
Cities (all)
Small
Medium
Large
n.s.
n.s.
n.s.
n.s.
n.s.
0.034
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
Fishing and tourism boats
Boats (all)
Trawling
Motor
Sail
Rowing
n.s.
n.s.
0.011
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
0.030
n.s.
0.0017
n.s.
n.s.
of manatees within MPAs was 0.3 individuals per 5 km-segment
(18 individuals along 310 km coastline), three times larger than
in areas outside MPAs (0.1 individuals per 5 km-segment, 23 individuals along 1160 km coastline). This positive relationship was
confirmed by Spearman correlation analysis (p = 0.001).
When considering individual MPAs, manatees showed significantly higher density in two estuarine MPAs (‘‘Delta do Rio Parnaíba’’ and ‘‘Barra do Rio Mamanguape’’) than outside, with six
and five manatees, respectively. Dolphins showed significantly
higher density within the ‘‘Costa dos Corais’’ MPA (24 dolphins),
while sea turtles showed significantly higher density within the
‘‘Recifes de Corais’’ MPA (41 sea turtles) (Fig. 4 and Table 3).
4. Discussion
The data generated by the hitherto largest effort to quantify and
correlate the distribution of manatees, dolphins and sea turtles in
northeast Brazil yielded important new insights into the situation
of these taxon’s.
This study revealed a wide distribution of manatees, dolphins
and sea turtles, except for a single area (the Potiguar Basin), probably due to specific hydrographic features and anthropogenic factors in this area. The present data showed that some species
were associated with each other and with coastal features, such
as estuaries and reefs. The important role of MPAs was corroborated by the high densities of these animals. One alarming finding
was the association of manatees and sea turtles with motorized
fishing boats and coastal cities, which is a relevant conservation
issue.
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M.D.d.O. Alves et al. / Biological Conservation 161 (2013) 91–100
Fig. 4. Density of manatees (left), dolphins (center) and sea turtles (right) in marine protected areas in northeastern Brazil (DP: Delta do Rio Parnaíba, RC: Recifes de Corais,
BM: Barra do Rio Mamanguape, CC: Costa dos Corais, Outside: areas outside marine protected areas). Data are based on 27 h of aerial surveys from the states of Piauí to
Alagoas. N = 294 coastal segments of 5 km length.
Table 3
Marine protected areas (MPAs) in northeastern Brazil and total sightings of manatees, dolphins and sea turtles. Data are based on 27 h of aerial surveys. N = 294 coastal segments
of 5 km length. Values given in the table are total number of organisms (N) and density (N per km coastline).
MPAs
Delta do Rio Parnaíba
Recifes de Corais
Barra do Rio Mamanguape
Costa dos Corais
All MPAs
Outside MPAs
Area (km2/segment)
3.14/16
1.8/14
0.15/6
4.14/26
Total: 9.23/62
Total: /232
Main habitat
Extensive Mangroves
Offshore Reef Patches
Coastal Reef Lines
Coastal Reef Lines
N/Density per segment
Spearman correlation
Manatees
Dolphins
Sea turtles
Manatees
Dolphins
Sea turtles
6/0.4
3/0.2
5/0.8
4/0.2
18/0.3
23/0.1
4/0.3
0/0.0
2/0.3
24/0.9
30/0.5
48/0.2
12/0.8
41/2.9
8/1.3
22/0.8
83/1.3
203/0.9
0.004
n.s.
0.0007
n.s.
0.001
n.s.
n.s.
n.s.
0.024
n.s.
n.s.
0.0008
n.s.
n.s.
n.s.
n.s: not significant at a = 0.05.
4.1. Spatial distribution
Manatees, dolphins and sea turtles occurred more or less continuously along the study area. The only extensive area with virtually no sightings of animals was the Potiguar Basin, located at the
northwestern coast of Rio Grande do Norte state. This region presents extremely harsh conditions due to the high energy of winds,
waves and tides, with strong alongshore currents in westerly direction (Silva and Amaro, 2008). It is also considered one of the most
oligotrophic regions of Brazil and has the lowest estuarine influence of the entire coastline, with virtually no freshwater input
(Júnior et al., 2010). Furthermore, intensive resource exploration
and coastal degradation have persisted for many decades due to
the activities of the offshore oil industry, salt works and shrimp
farming (Silva and Amaro, 2008), as observed during the survey.
Seismic surveys associated with the offshore industry may cause
severe physiological and behavioral changes in several organisms,
especially in marine mammals (McCauley et al., 2000; Early, 2001).
However, the present study and earlier assessments (Parente et al.,
2006; Parente and Araújo, 2011) are still insufficient to evaluate
the influence of offshore activities on the distribution and behavior
of marine mammals and sea turtles in northeastern Brazil. The distribution of manatees, that forage on macrophytes and seagrass
beds and are known to actively seek freshwater to drink, seems
to be fundamentally determined by the availability of freshwater
and food sources, and shelter in estuaries for reproduction (Hartman, 1979; Reynolds et al., 2009). However, the extreme harshness
of the dynamic coastline, the scarcity or absence of freshwater
sources and foods, the scarce and inaccessible sand bar estuaries,
the absence of any shelter provided by barrier reefs and the intense
human exploration may together explain the absence of manatees
in the Potiguar Basin. This area and the eastern portion of the state
of Ceará show the largest numbers of cases of manatee strandings,
especially neonates, probably related to these factors (Parente
et al., 2004; Meirelles, 2008; Lima et al., 2011).
The coexistence of manatees and sea turtles found in this study
has been recorded in various other locations worldwide (Fertl and
Fulling, 2007). This positive relationship is a function of the ecological requirements of both taxa, which may share common shelter
and coastal foraging areas. Herbivory is a common trait among
sirenians and C. mydas, feeding on seagrass beds and macroalgae
(Hartman, 1979; Borges et al., 2008; López-Mendilaharsu et al.,
2008; Guebert-Bartholo et al., 2011). There is a correlation of both
taxa and fishing boats, both being concentrated close to shore, in
the same, productive areas. This proximity implies a high risk of
collision, accidental capture and habitat destruction, mainly by
shrimp trawlers (Borges et al., 2007; Meirelles, 2008; Eguchi
et al., 2010; Guebert-Bartholo et al., 2011). In Florida, most
of the reported mortalities and serious mutilations of manatees
(T. m. latirostris) are due to collisions with motor boats (Nowacek
et al., 2004; Rommel et al., 2007). In northeastern Brazil, previous
reports indicate that the interaction of T. m. manatus with motor
boat traffic represents a direct threat for this species, causing lesions and deaths (Borges et al., 2007; Meirelles, 2008). In San Diego
Bay, an intensively urbanized coastal area, frequent strandings of
green turtles have been reported, probably related to collisions
with motor boats (Eguchi et al., 2010).
4.1.1. Antillean manatee
Studies on the distribution of manatees in Brazil have been conducted since the 80s, based on information from fishermen and
stranding data (Parente et al., 2004; Luna et al., 2008; Lima et al.,
2011). Only one single study in the eastern part of Ceará state used
an aerial survey, however with difficulties associated to the observation of these animals in turbid waters during the rainy season and
flight logistics (Costa, 2006). Conversely, the aerial methodology
M.D.d.O. Alves et al. / Biological Conservation 161 (2013) 91–100
used in this study was very favorable for the detection of manatees,
highlighting its importance for the conservation of this endangered
species.
The detection of some manatees has been hampered due to the
following factors: (1) solitary habit, (2) barely visible exposure on
the surface, and (3) cryptic brownish color surrounded by turbid
waters near estuaries. These limitations may make counting and
identification inaccurate (Edwards et al., 2007), one alternative
being the use of a side-scan sonar (Gonzalez-Socoloske et al.,
2009). During periods of cold weather, aerial surveys conducted in
Florida uncovered large groups of manatees in areas of warm and
transparent water, which facilitated the counting (Edwards et al.,
2007). In the study area, the almost constant temperature of coastal
waters prevents this type of phenomenon (Lima et al., 2011).
The social structure of manatees, predominantly solitary or in
couples, was also found in other studies in this region (Borobia
and Lodi, 1992; Paludo and Langguth, 2002; Costa, 2006). The presence of calves on Barreta beach, Rio Grande do Norte state, was also
recorded by other researchers (Oliveira et al., 1990; Paludo, 1998),
suggesting the existence of a nursery area. The mating period of
manatees in northeastern Brazil is the dry season, from October to
May (Paludo, 1998; Parente et al., 2004; Meirelles, 2008; Lima
et al., 2011). The observation of a single calf only within the reproductive season (March) during the aerial survey may be considered
worrisome for the conservation of this species, which is threatened
by the destruction and degradation of its estuaries (Parente et al.,
2004; Meirelles, 2008). Furthermore, these few records may be
due to lack of sampling within the estuaries, which are ecosystems
using for reproduction and parental care of manatees (Hartman,
1979; Lima et al., 2011), or detection difficulty related smaller size.
The presence of manatees in shallow coastal waters, generally
with less than 12 m depth, seems to be related to the availability
of food sources (Hartman, 1979; Olivera-Gómez and Mellink,
2005; Rodas-Trejo et al., 2008; Langtimm et al., 2011). Furthermore,
these are often shallow sheltered sites that allow animals to spend
less energy in respiratory intervals (Smethurst and Nietschmann,
1999; Bacchus et al., 2009). The access to shallow foraging areas at
high tide only introduces additional variability to the depth range
of manatees. In previous studies conducted in northeastern Brazil
with observations from shore or on boats, water depth of manatee
sightings varied between only 0.4 and 5.6 m (Borobia and Lodi,
1992; Paludo and Langguth, 2002; Costa, 2006), which is much shallower than the range observed in our study (most frequently within
6–8 m, reaching 14.8 m). This difference is probably due to the more
efficient coverage of deeper waters in this aerial survey as compared
to earlier studies. The most common seagrass in this region, Halodule wrightii, which is considered one of the main food sources for
this species (Borges et al., 2008; Lima et al., 2011), is found from
the intertidal zone down to 10 m depth (Laborel-Deguen, 1963).
Furthermore, the occurrence of manatees near well-preserved
mangrove estuaries located in the northern part of the study area
reflects the use of these types of habitats for breeding and foraging
(Olivera-Gómez and Mellink, 2005; Rodas-Trejo et al., 2008; Lima
et al., 2011). In many other estuaries surveyed in this study, the
visible deforestation of mangrove vegetation due to the expansion
of shrimp farms, salt works, and urbanization has caused the closing of estuaries with sand bars, hampering the access by manatees
(Lima et al., 2011).
The positive correlation between manatees and medium-sized
cities highlights the intense human occupation of the coastal zone
around estuarine and sheltered areas that are important for this species. The attractiveness of bays and estuaries for human populations
in Brazil resulted in a long process of intense urban development,
fisheries, ports, industries and recreational activities in these areas,
which are major threats for coastal ecosystems (Cunha, 2005) and
many endangered species.
97
4.1.2. Dolphins
Even under ideal conditions of water transparency and swimming in groups, the identification of dolphins was difficult due to
their quick movements in opposition to the speed of the aircraft.
The small morphological variations between some cetaceans make
aerial identification difficult (Preen, 2004). S. guianensis was diagnosed by the morphology of the rostrum and melon, pink–gray coloration and its triangular dorsal fin (Flores, 2002).
Groups of two to eight Guiana dolphins found in this study are
commonly observed in northeastern Brazil (Araújo et al., 2001,
2008), while groups of this species may reach 150 specimens in
the southern region (Flores, 2002), where waters are more productive due to seasonal upwelling (Muehe and Garcez, 2005). This explains the tendency of large groups to inhabit the southern and
southeastern region, and small groups to occur in the northeastern
region (Araújo et al., 2008).
The higher frequency of dolphins in deep waters, reaching a
depth of 17.1 m and at a distance of up to 4.4 km from the coast
in the present study, is similar to findings of previous studies on
Guiana dolphins in Brazil, with up to 16 m depth and four km from
the coast (Bazzalo et al., 2008; Wedekin et al., 2010). Previous
studies showed that the bathymetry is important for the distributions of dolphins, mainly due to the depth-related distribution of
prey (Baumgartner et al., 2001; Certain et al., 2008). This may reflect their search for food, corroborated by the migration of fish
to deeper areas and away from the coast due to environmental perturbations in nearshore reef ecosystems in northeastern Brazil
(Frédou and Ferreira, 2005). The search of these animals for more
offshore areas may suggest a strategy to find favorable foraging
areas, and possibly to avoid the intense coastal artisanal fishing
activity recorded in this study. Accidental capture in fishing nets
is a main threat for Guiana dolphins in Ceará state, cetacean species with highest (62%) incidence of strandings (Meirelles et al.,
2009). This species and bottlenose dolphins (Tursiops truncatus)
have foraging as a determinant factor for habitat choice (Hastie
et al., 2004; Wedekin et al., 2010).
The occurrence of dolphins close to estuaries may indicate the
search for food sources that are associated to these important nurseries for crustaceans and fish, both for resident species and for
marine migratory species (Blaber, 2000). In Brazil, S. guianensis frequently occurs in estuarine areas and their surroundings (Flores,
2002; Araújo et al., 2008), suggesting that many unidentified specimens are probably of this species.
4.1.3. Sea turtles
Sea turtles were the most abundant taxon in this study. This is
the first aerial survey of sea turtles carried out in Brazil. This methodology has been shown to provide important abundance estimates of sea turtle populations, especially in foraging or nesting
grounds (Epperly et al., 1995; Cardona et al., 2005; Roos et al.,
2005; Witt et al., 2009).
Individuals from the family Cheloniidae have been identified by
the greenish-brown shell coloration, that is distinct from Dermochelyidae, which have a black color and very prominent ridges. The
detection of the specimens, even in moderate visibility conditions,
occurred through the total body exposure and turbulence at the
water surface caused by the fins during the dive, which could reveal
the number of animals (McClellan, 1996). However, flight altitude
and speed, and escape behavior caused by the noise of the aircraft,
made the identification at species level difficult, as observed in other
studies (Shoop and Kenney, 1992; Epperly et al., 1995; McClellan,
1996). The smaller size of sea turtles in relation to other taxa studied
also contributed as a limiting factor for identification to species
level. Previous studies based on aerial surveys suggested a minimum
size of 30 (Epperly et al., 1995) to 75 cm (Shoop and Kenney, 1992)
carapace width for a specific diagnosis of sea turtles. Conversely,
98
M.D.d.O. Alves et al. / Biological Conservation 161 (2013) 91–100
in the present study, identification to species level was not possible
even for large-sized specimens.
The high number of solitary sea turtles sighted could indicate
that the areas studied did not include major breeding grounds,
since mating occurs in large groups in shallow waters (Hirth,
1980). In Brazil, green turtles, for example, may be sighted in
groups during the reproductive period from September to March,
which includes the study period. This species uses oceanic islands
for mating, being rarely sighted in large groups along the continental northeastern coast of Brazil. The northeastern coast harbors 12
of the 19 main breeding areas for sea turtles in country (Marcovaldi and Marcovaldi, 1999). However, none is included in the study
area, although nesting areas along the coast have been recorded.
Aerial and snorkel census techniques for estimating green turtle
abundance in foraging areas identified small groups of 4–5 individuals, that apparently were randomly distributed (Roos et al., 2005).
It is therefore likely that the study area is mainly used for feeding
and resting.
In this study, varying depths (0.9–18.5 m) and distances from
the coast (from the coastline up to 5 km) occupied by sea turtles
showed the diversity of existing habitats. Their spatial distribution
can be influenced by physical and biological parameters, and depth
distribution is closely related to their feeding, breeding and resting
behavior (Griffin and Griffin, 2003; Roos et al., 2005; Witt et al.,
2010). In a previous study in Brazil, green turtles were sighted during scuba dives feeding at 6 m depth (Guebert-Bartholo et al.,
2011), and swimming in areas with vegetation at 10 m depth
and up to 10 km distant from the coast (Parente et al., 2006). These
numbers are within the range recorded in this study, suggesting
the occurrence of important foraging areas in northeastern Brazil.
The positive correlation of sea turtles with reef formations such
as Northern Beach Rocks and Offshore Reef Patches, as observed by
the high density of individuals in the MPA ‘‘Recifes de Coral’’ may
be intimately related to the search for shallow sheltered areas and
for areas with abundant macroalgae that grow on sandstone substrates. Likewise, an aerial survey carried out in Western Australia
revealed a higher density of sea turtles in reef areas (Preen et al.,
1997). In a study conducted in the South-West Indian Ocean, the
distribution of these animals close to coral reefs and on the outer
reef slopes was explained by the availability of shelter and food
(Jean et al., 2010), similarly to the findings of the present study.
4.2. Marine protected areas (MPAs)
The high density of manatees in the MPAs ‘‘Delta do Rio Parnaíba’’ and ‘‘Barra do Rio Mamanguape’’ highlights the importance
of these areas for the protection of this species and its habitats.
These areas are mainly composed of a complex deltaic environment with well-preserved mangroves (‘‘Delta do Rio Parnaíba’’)
or estuarine mangroves with adjacent coastal reef lines (‘‘Barra
do Rio Mamanguape’’), allowing for the occurrence of groups of
manatees in sheltered, well-preserved areas and an open access
to upstream environments for reproduction and resting (Borobia
and Lodi, 1992; Lima et al., 2011). In the Persian Gulf, areas with
high densities of dugongs and sea turtles were related to habitats
that are rich in seagrass beds and coral reefs, and were chosen
for the establishment of MPAs (Preen, 2004).
The occurrence of dolphins and sea turtles in MPAs characterized by linear coastal reef formations can ensure sheltered areas
for foraging and resting. The MPA ‘‘Recifes de Coral’’, with high
numbers of sea turtle sightings, has coastal and offshore reefs, as
well as seagrass beds and banks of macroalgae, which likely represent food sources for these animals (Guebert-Bartholo et al., 2011).
In the MPA ‘‘Costa dos Corais’’, the configuration of a large-scale
barrier reef may allow for higher food availability and facilitate fish
capture strategies by dolphins. The use of specific foraging
techniques is commonplace for some species of delphinids, such
as the bottlenose dolphin, that adapt its distribution patterns towards habitats that are favorable for prey capture (Hastie et al.,
2004; Torres and Read, 2009). In Brazil, Guiana dolphins feed preferentially in bays, barrier reefs and estuaries, where they can direct
fish schools to shallower waters (Araújo et al., 2001; Rossi-Santos
and Flores, 2009). Such areas are widely found in the MPA ‘‘Costa
dos Corais’’ (FAO, 2011).
It is noteworthy that there is a captive manatee reintroduction
program within the MPA ‘‘Costa dos Corais’’, located in the northern part of the state of Alagoas. This very successful program has
possibly provided an increase of the manatee population in this
area (ICMBio, 2011). However, proximity and easy access of human
populations to reef areas found in the study can directly affect the
biological communities (Castro and Pires, 2001). Habitat loss and
the degradation of feeding areas for sea turtles are a potential
cause of population decline (López-Mendilaharsu et al., 2008; Guebert-Bartholo et al., 2011) and the presence of motor boat traffic
and trawling can cause behavioral changes in dolphins (Constantine et al., 2004; Wedekin et al., 2010; Carrera et al., 2008).
The results of the present study cannot be used to test whether
the existence of MPAs increases the density of endangered species
in these areas, as in other studies (Witt et al., 2009; Panigada et al.,
2011; Knip et al., 2012). All MPAs were delineated around special
coastal features, such as outstandingly large or exceptionally
well-preserved estuaries and barrier reefs, which create favorable
and essential habitats for these and many other species. Rather
than proving the effect of MPAs, the elevated density of these
organisms shows the vital importance of protecting and adequately managing such unique ecosystems to ensure a sustainable
future for the populations of severely threatened species.
5. Conclusions
The spatial distributions of manatees, dolphins and sea turtles
show the different types of behavior of these species and the variety of ecosystems along the coast, with a preference for well-preserved foraging and resting habitats.
In northeastern Brazil, aerial monitoring in areas of occurrence
of marine mammals and sea turtles, that are susceptible to habitat
loss, can encourage the development of management, environmental conservation and recovery programs. The diagnosis and monitoring of ecosystems are essential for the survival of marine
biodiversity, highlighting the role of MPAs for the protection of
ecosystems and species.
Acknowledgments
The authors would like to thank the Federal University of Pernambuco (UFPE) and the ‘‘Fundação Mamíferos Aquáticos’’ (FMA)
for supporting the survey; ‘‘Petrobras Petróleo Brasileiro S.A.’’
through its ‘‘Programa Petrobras Ambiental’’ for sponsoring the
aerial surveys; ‘‘Conselho Nacional de Desenvolvimento Científico
e Tecnológico’’ (CNPq) for the doctoral scholarship granted to the
first author; the ‘‘Centro Mamíferos Aquáticos’’(CMA) for initially
supporting the research; PhD. Paul Gerhard Kinas for methodological support; and the NVO air taxi team for adapting their plane to
carry out the aerial survey and logistics of flights. This study is part
of the doctoral thesis of the first author.
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