Ecomorfologia, performance alimentar e bioerosão de budiões da

Transcrição

UNIVERSIDADE ESTADUAL DE SANTA CRUZ
PÓS-GRADUAÇÃO EM ECOLOGIA E
CONSERVAÇÃO DA BIODIVERSIDADE
Nicole Tiburcio Lellys
subfamília Scarinae (Actinopterygii: Labridae) no Banco dos Abrolhos, Bahia
Ilhéus, Bahia
2014
ii
Dissertação apresentada à
Universidade Estadual de Santa Cruz
para obtenção do título de Mestre em
Ecologia e Conservação da Biodiversidade
Área de concentração: Ecologia
Orientador: Prof. Dr. Rodrigo Leão de Moura
Coorientador: Prof. Dr. Fernando Zaniolo Gibran (UFABC)
Ilhéus, Bahia
2014
iii
L541
Lellys, Nicole Tiburcio.
Ecomorfologia, performance alimentar e bioerosão de burdiões
da subfamília scarinae (Actinopterygii : Labridae) no Banco dos
Abrolhos, Bahia / Nicole Tiburcio Lellys. – Ilhéus : UESC, 2014.
Xii, 58f. : il.
Orientador : Rodrigo Leão de Moura.
Coorientador : Fernando Zaniolo Gibran.
Dissertação (mestrado) – Universidade Estadual de Santa
Cruz. Programa de Pós-graduação em Ecologia e Conservação,
da Biodiversidade
Inclui referências.
1. Peixes recifais – Alimentação - Abrolhos, Arquipélogo de.
2.Ecossistemas recifais – Abrolhos, Arquipélogo de. (BA). 3.
Peixes – Espécies. I. Moura, Rodrigo Leão de. II. Gibran, FerNando Zaniolo. III. Título.
CDD – 639.32
iv
NICOLE TIBURCIO LELLYS
Comissão examinadora:
__________________________
Profª Drª Roberta Martini Bonaldo
(USP)
__________________________
Prof. Dr. Ronaldo Bastos Francini-Filho
(UFPB)
__________________________
Prof. Dr. Rodrigo Leão de Moura
(Orientador – UESC)
v
AGRADECIMENTOS
Muitas pessoas e instituições foram essenciais para a concepção e realização desse
trabalho e deixo aqui a minha profunda gratidão em forma de palavras.
Agradeço à CAPES pela bolsa de mestrado.
A Conservação Internacional do Brasil pelo financiamento do projeto “Subsídios para
conservação do budião-azul, Scarus trispinosus Valenciennes, 1840, no maior complexo
coralíneo do Atlântico Sul”.
Agradeço ao Prof. Dr. Rodrigo Leão de Moura pela orientação, dedicação, confiança,
amizade e pela oportunidade tão desejada por mim de trabalhar em Abrolhos e me
envolver com um grupo multidisciplinar que se empenha pela conservação dessa
belíssima e diversa região.
Ao Prof. Dr. Fernando Zaniolo Gibran pela valiosa coorientação, atenção e ensinamentos.
Ao Prof. Dr. Ronaldo Francini-Filho pela parceria, amizade, aprendizados e insights recifais,
e pelas contribuições como membro avaliador da dissertação.
À Dr. Roberta Martini Bonaldo pelas enriquecedoras contribuições como avaliadora da
dissertação, e por toda atenção e inspiração.
À Coral Fortunato e Fernanda Cervi pela participação nas coletas dos budiões e todo
importante apoio em Caravelas. À Jemilli e Clarinha pela ajuda no Laboratório de
Oceanografia Geológica da UESC.
A toda equipe do Projeto Rede Abrolhos/SISBIOTA pelas valiosas ajudas e experiências
vivenciadas nas expedições à Abrolhos. Agradeço especialmente a Leila, Diego Bola, Ericka
Guigui, Melina, Cynthia, Tiago Tigrão, Jomar, Arthur, Linda, Pedro, Guilherme, Patrícia,
Aline, Daniel, Rafael... É imensurável como nossas saídas de campo foram enriquecedoras.
A toda tripulação do Titan, Horizonte Aberto, Sanuk e Boto Cinza pelo incrível e incansável
apoio (atenção apoio apoio!) e pelos tantos aprendizados em alto mar. Agradeço
especialmente a Zá, Maurício Mau Mau e Carlinhos, aprendi muito com vocês.
vi
A toda equipe da Conservação Internacional da Base Marinha de Caravelas, pelo
fundamental apoio. Especialmente a Eduardo Camargo, Danilo Araújo e Renata Pereira.
Ao Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade,
especialmente à Deborah Faria, Fernanda Gaioto, Eliana Cazetta e Leandro Loguercio pelo
empenho e dedicação ao programa, que inspiram a fazermos o que acreditamos; e a Iky e
Amábile pelo apoio e carinhosa atenção de sempre.
À Universidade Estadual de Santa Cruz pela infraestrutura e pessoal, em nome do Prof. Gil
Marcelo Reuss e Prof. Ana Amélia do Laboratório de Oceanografia Geológica, e a Tiago,
Gerson e Osmar, pelas tantas ajudas nos laboratórios e equipamentos.
À minha turma de mestrado, Let, Mari, Iara, Lais, Leiza e Vini, pelas vivências, sufocos e
alegrias compartilhadas, que se estendem a outros amigos do PPGECB, SAT e ZOO.
À Olivença e toda equipe que me acolheu e tanto acrescentou na temporada de
mestrado, muito especial conhecer e ter vocês como família, Renatinha, Narita, Nani,
Suzane, Milena, Paul, Sassá, Tiagão, Siamens, João, Caio, Lucas, Ju, Gastón, Kena, Vini e
vários outros queridos da eco-surf-comunidade.
À Gab, minha incrível companhia diária, pelo amor, ajuda, paciência, força e tanto mais.
À minha amada família, mainha, painho, Marcel e Lara, o apoio e carinho de vocês
refletem em tudo que eu faço e em quem eu sou. Muita gratidão, respeito e amor.
À Pernambuco por me fazer valorizar ainda mais o que está longe e me fortalecer. À Bahia
por tudo que aprendo em suas terras e águas. À Abrolhos por me permitir mergulhar no
seu incrível mundo recifal. Aos budiões pelo privilégio da conexão e conhecimentos. À
Floresta de Iroko por me acalmar e encaminhar. E à natureza e todos os seus devas, por
me fazerem parte dela.
vii
“Não somos metades que se encaixam,
somos inteiros que se completam.”
Fabricio Carpinejar
viii
RESUMO
Os budiões (Perciformes: Labridae) formam um grupo diverso em ambientes recifais e
podem representar a maior parte da biomassa de peixes nesses sistemas. Alimentam-se
principalmente de algas e detritos e também podem incluir corais em suas dietas. As
espécies são geralmente divididas em três grupos funcionais (podadores, raspadores e
escavadores), com diversificação na morfologia bucal relacionada às diferentes formas de
forrageio. Os budiões são considerados um grupo funcional crítico em ecossistemas
recifais, atuando como controladores das macroalgas e como bioerosores. O objetivo
deste trabalho foi comparar, do ponto de vista ecomorfológico, três espécies de budiões,
Scarus trispinosus, Scarus zelindae e Sparisoma amplum, com ênfase na ecomorfologia,
performance alimentar e bioerosão exercida por Sc. trispinosus, a maior espécie de budião
e o peixe recifal mais abundante em Abrolhos, região que concentra os maiores recifes
coralíneos do Atlântico Sul. A pré-maxila, o dentário e configuração da boca discriminaram
as três espécies e as diferentes categorias de tamanho de Sc. trispinosus. O aparato bucal
mais fraco e móvel de Sc. zelindae e de indivíduos menores das demais espécies indicaram
que estes são predominantemente raspadores. Por outro lado, indivíduos maiores de Sc.
trispinosus e Sp. amplum, com aparato bucal robusto e articulações simples, são
predominantemente escavadores. Em Sc. trispinosus foi evidenciada uma forte relação
entre o tamanho dos indivíduos, sua taxa de alimentação e o volume de substrato
removido pelas mordidas, demonstrando um aumento progressivo em sua capacidade de
escavação. Dependendo principalmente da frequência de consumo dos diferentes itens
alimentares e de suas abundâncias relativas, as espécies terão papéis diferentes no
sistema recifal. Em Abrolhos, por exemplo, a bioerosão é exercida apenas por indivíduos
grandes de duas espécies de budiões (Sc. trispinosus e Sp. amplum). Para Sc. trispinosus, a
principal delas, o volume de substrato recifal removido por indivíduos foi estimado em
206,94 cm³ por dia e 75.534,14 cm³ por ano. O cenário de sobrepesca, em intensificação,
pode levar a reestruturações impactantes no funcionamento do ecossistema recifal,
especialmente em sistemas com baixa diversidade e reduzida redundância funcional, tais
como os recifes do Atlântico Sul. A supressão das maiores classes de tamanho, um dos
primeiros efeitos da pesca, pode acarretar em tais reestruturações, com consequências
ainda mal compreendidas.
Palavras chave: ambientes recifais, herbivoria, morfologia funcional.
ix
ABSTRACT
Parrotfishes (Perciformes: Labridae) form a diverse group in reef environments, and
represent the majority of fish biomass in many ecosystems. They feed mainly on algae
and detritus, but also include corals in their diet. The species are generally divided into
three functional groups (grazer, scrapers and excavators), with diversification in mouth
morphology related to different forms of foraging. Parrotfish are considered a critical
functional group in reef ecosystems, acting as controllers of macroalgae and contributing
to bioerosion. The objectives of this study were to compare the ecomorphology of three
species of parrotfish, Scarus trispinosus, Scarus zelindae and Sparisoma amplum, with an
emphasis on eco-morphology, feeding performance and bioerosion of Sc. trispinosus, the
largest species of parrotfish and the most abundant in the Abrolhos Bank, a region with
the highest coral reef diversity of the Southern Atlantic Ocean. Premaxilla, dentary and
mouth configurations distinguish the three species and the different size categories of Sc.
trispinosus. The weakest and most mobile oral apparatus of Sc. zelindae and the smaller
individuals from the other species can be predominantly classified as scrapers.
Contrastingly, individuals from the large category of Sc. trispinosus and Sp. amplum
exhibit a robust oral jaw apparatus with simple joints and are predominantly classified as
excavators. In Sc. trispinosus, a strong relationship was found between the size of the
individuals, their feeding rate and volume of substrate removed from the bites, showing a
progressive increase in their ability to excavate. Depending on the frequency of
consumption of different food items, as well as the means of obtaining food and their
relative abundances, species will have different roles in the reef system. In Abrolhos,
bioerosion is exercised only by large individuals of the two parrotfish species (Sc.
trispinosus and Sp. amplum). For Sc. trispinosus, the principal specie, the volume of reef
substrate removed per individual per day was estimated to be 206.94 cm³ and erosion
rates of 75,534.14 cm³ per year. The scenario of overfishing is intensifying and can lead to
profound restructuring in the functioning of reef ecosystems, especially in systems with
low diversity and low functional redundancy, such as South Atlantic reefs. The removal of
the largest size classes of these species, one of the first effects of overfishing, may result
in such restructurings, with consequences still poorly understood.
Key words: coral reefs, herbivory, jaw morphology.
x
LISTA DE TABELAS
Table 1. Eigenvalues, variance, eigenvectors and r values extracted for the two Principal
Components of the ordination with the morphometric and osteological attributes of the
three species (Scarus trispinosus, Sc. zelindae and Sparisoma amplum)…………………..…….15
Table 2. One-way ANOVA for ecomorphological attributes for Scarus trispinosus, Sc.
zelindae and Sparisoma amplum in the two size categories…..........................………..……..18
Table 3. Mean for the morphometric attributes and osteological attributes calculated for
small and large category of Sc. trispinosus, Sc. zelindae and Sp. amplum...................……..19
Components of the ordination with the morphometric and osteological attributes of the
six size categories of Sc. trispinosus……………………………………………………............………..……..22
Table 5. One-way ANOVA for the 11 ecomorphological attributes of the six size categories
of Scarus trispinosus..…………….…..............…………………………………....................…….…..……..25
Table 6. Mean values of the morphometric and osteological attributes of Scarus
trispinosus…………………….……............………..……..…………………………………............………..……..26
Table 7. Feeding rates, proportion of significant bites, bite volume and daily feeding rates
for each size-category of Sc. trispinosus studied in the Abrolhos Bank, Brazil..………..……..27
Table 8. One-way ANOVA performed on feeding rates, proportion of significant bites, bite
volume and feeding periods comparing the six size categories of Sc. trispinosus…....……..27
Table 9. Parameters used for estimating bioerosion rates of Sc. trispinosus.……..…...……..29
xi
LISTA DE FIGURAS
Figura 1. Indivíduos adultos (40-60 cm) das três espécies de budiões estudadas: Scarus
trispinosus, Scarus zelindae e Sparisoma amplum...……………………………………...........….........4
Figure 1. Map of the study region showing the Abrolhos National Marine Park boundaries
and sampling sites…………………………………………………………………...........………………………….…11
Figure 2. Distribution of the three parrotfish species and sizes in a two-dimensional
morphospace based on scores from the first two principal components from
morphometric attributes.................................…......................……........….........……..………..16
Figure 3. Distribution of the three parrotfish species and sizes in a two-dimensional
morphospace based on scores from the first two principal components from osteological
attributes ……..………………………………………………………………………………………………………………..18
Figure 4. Premaxilla and dentary of Scarus trispinosus, Sc. zelindae and Sparisoma
amplum………….………….………….………….………….………….………….………….………….………………….21
Figure 5. Maxilla and articular of Scarus trispinosus, Sc. zelindae and Sparisoma
amplum…………….….………….………….………….………….………….………….………….………….…………..21
Figure 6. Distribution of the six size classes of Scarus trispinosus in a two-dimensional
morphospace, based on scores from the first two morphometric principal component
axes................................................................................................................……….............23
Figure 7. Distribution of the six size classes of Scarus trispinosus individuals in a twodimensional morphospace, based on scores from the first two osteological principal
component axes.........................................................................................……...................24
xii
Figure 8. Feeding rates of Sc. trispinosus throughout the Diurnal period...........................28
Figura 9. Daily feeding of Sc. trispinosus with a quadratic polynomial trend line fitted to
the data.………......................................................................................................................28
xiii
SUMÁRIO
RESUMO..............................................................................................................................viii
ABSTRACT............................................................................................................................ix
LISTA DE TABELAS.................................................................................................................x
LISTA DE FIGURAS.................................................................................................................xi
INTRODUÇÃO GERAL.............................................................................................................1
ARTIGO:
ECOMORPHOLOGY,
FEEDING
PERFORMANCE
AND
BIOEROSION
OF
PARROTFISHES (LABRIDAE: SCARINAE) IN EASTERN BRAZIL..................................................6
CONCLUSÕES.......................................................................................................................49
REFERÊNCIAS BIBLIOGRÁFICAS...........................................................................................51
1
INTRODUÇÃO GERAL
Os budiões (Labridae: Scarinae) representam um dos mais importantes grupos funcionais
em ambientes recifais tropicais e subtropicais (STREELMAN et al., 2002). São peixes de
médio a grande porte de coloração vistosa, e possuem dentes fundidos com pré-maxila e
dentário caracteristicamente em forma de bico de papagaio, o que lhes permite obter
alimento aderido a substratos duros (BELLWOOD; CHOAT, 1990). O budiões se alimentam
principalmente de algas filamentosas e calcárias incrustantes associadas a rochas e corais
(BELLWOOD; CHOAT, 1990; CHOAT, 1991; BRUGGEMANN et al., 1994a). Algumas espécies
de budiões são consideradas herbívoro-detritívoras ou detritívoras, pelo fato da maior
parte de suas dietas incluir considerável quantidade de detritos (CROSSMAN et al., 2001;
WILSON et al., 2003). Os recifes coralíneos são ambientes cuja estrutura é moldada por
interações dinâmicas entre processos de construção e desgaste, tais como a calcificação
de corais e algas e a erosão por agentes físicos e biológicos. Os budiões participam
ativamente deste processo e são importantes agentes bioerosivos nos sistemas recifais
(BELLWOOD et al., 2003).
Hunte,W. &Wittenberg, M. Effects of eutrophication and sedimentation on juvenile corals.
II. Settlement. Mar. Biol. 114, 625–631 (1992).
47. Steneck, R. S., in 6th International Coral Reef Symposium (eds Choat, J. H. C. et al.) Vol.
1 37–49 (6th International Coral Reef Symposium Executive Committee, Townsville, 1988).
48.
Os budiões podem ser categorizados do ponto de vista funcional em três grupos,
podadores, raspadores e escavadores, em função de sua morfologia e hábitos alimentares
(BELLWOOD; CHOAT, 1990; STREELMAN et al., 2002). Os budiões podadores se alimentam
de algas epilíticas e turf (i.e. associações entre diferentes tipos de microalgas, detritos e
micro-organismos) que recobrem o substrato, mordendo-o superficialmente, sem causar
impacto à matriz calcária do recife (BELLWOOD; CHOAT, 1990; HUGHES, 1994) Os
raspadores, além de retirarem a cobertura do substrato ao se alimentar, chegam a raspar
levemente a matriz calcária, abrindo espaço para o recrutamento de organismos
2
incrustantes (BELLWOOD; CHOAT, 1990; BRUGGEMANN et al., 1994b; 1996). Já os budiões
escavadores possuem mordidas mais fortes, sendo capazes de remover pedaços
consideráveis da matriz calcária, sendo reconhecidos como os principais agentes
bioerosivos dos recifes (BELLWOOD; CHOAT, 1990; BELLWOOD et al., 2003). Os budiões
raspadores e escavadores contribuem para o recrutamento de corais e algas calcárias
incrustantes ao promoverem a abertura de novos espaços para recolonizações e
subsequentes sucessões ecológicas, como observado no Atlântico (e.g. LEWIS, 1986;
BRUGGEMANN, 1995), Pacífico (e.g. BELLWOOD, 1995a, b, 1996) e Índico (e.g.
LETOURNEUR, 1996). Desta forma, a intensa atividade alimentar dos budiões atua no
controle “descendente” (top-down) na cadeia alimentar, interferindo no balanço
competitivo entre algas frondosas, corais e algas calcárias incrustantes, sendo
fundamentais para a resiliência e saúde dos recifes com corais (BELLWOOD; CHOAT, 1990;
HUGHES, 1994; BELLWOOD et al., 2004; HOEGH-GULDBERG et al., 2007; BONALDO et al.,
2014).
Embora os budiões escavadores possuam maior força no aparato bucal para retirar
pedaços do substrato, eles não deixam marcas visíveis em todas as investidas contra o
substrato (BRUGGEMANN et al., 1996), pois estas marcas dependem da dureza do
substrato e da investida do budião. Quantificar a proporção de mordidas que deixam
marcas evidentes na matriz calcária (i.e. são significativas para a bioerosão) e mensurar o
volume retirado por tais investidas permite compreender melhor o impacto desses
escavadores no saldo de crescimento e desgaste dos recifes coralíneos. O potencial de
escavação do substrato varia também de acordo com a espécie e o tamanho dos budiões,
e estes aspectos irão influenciar o grau de bioerosão causada pelas suas populações e
como elas atuam na manutenção de ambientes recifais coralíneos (BELLWOOD; CHOAT,
1990; BRUGGEMANN et al., 1996; BONALDO; BELLWOOD, 2008).
Durante o crescimento, os budiões podem apresentar mudanças morfológicas e
comportamentais marcantes e, dessa forma, desempenhar papéis funcionais diferentes.
3
Além disso, a maior parte das espécies possui duas fases adultas distintas, com transição
rápida e relacionada ao hermafroditismo protogínico, social e demograficamente
controlado. Indivíduos na fase “terminal” (machos adultos) geralmente apresentam cores
mais conspícuas do que indivíduos na fase “inicial” (jovens, fêmeas ou, mais raramente,
machos maduros) (CHOAT; ROBERTSON, 1975; HAWKINS; ROBERTS, 2003). Devido a tais
mudanças ontogenéticas, a taxonomia dos budiões é complexa (e.g. MOURA et al. 2001).
Além disso, estudos filogenéticos recentes concluíram que a tradicional família Scaridae
deveria ser incluída como uma tribo de Labridae (CLEMENTS et al., 2004; WESTNEAT;
ALFARO, 2005; COWMAN et al., 2009). Essa tribo, Scarini, é composta por 10 gêneros e
cerca de 100 espécies (PARENTI; RANDALL, 2011).
Em grupos monofiléticos, espécies morfologicamente similares frequentemente ocorrem
em simpatria (SCHMITT; COYER, 1982). A coexistência de tais competidores em potencial
é possível em função de divergências morfológicas e/ou comportamentais que resultam
em partilha de recursos ou compressão dos nichos realizados (SCHOENER, 1974). Uma das
formas de avaliar o desempenho das espécies envolve a utilização do complexo formafunção e, consequentemente, da relação entre morfologia e papel ecológico (MOTTA;
KOTRSCHAL, 1992; MOTTA et al., 1995). Essa abordagem envolve a utilização de atributos
ecomorfológicos (e.g. índices morfométricos e osteologia) como indicadores de hábitos e
adaptações para o uso de determinados hábitats (GATZ, 1979; WINEMILLER, 1991), sendo
útil para explorar convergências e divergências adaptativas (e.g. GIBRAN, 2007, 2010).
Estudos ecomorfológicos sobre peixes recifais do Atlântico Sul são relativamente recentes
(e.g. STREELMAN et al., 2002; GIBRAN, 2007), e não há estudos sobre budiões na região.
Das aproximadamente 100 espécies de budiões (PARENTI; RANDALL, 2011), 10 são
endêmicas do Atlântico Sul e ocorrem nos recifes de Abrolhos, sendo duas do gênero
Scarus, cinco do gênero Sparisoma, uma do gênero Nicholsina e uma do gênero
Cryptotomus. Dentre estas, três destacam-se pela sua frequência de ocorrência,
abundância e funcionalidade: o budião-azul, Scarus trispinosus Valenciennes, 1984; o
4
budião-de-Zelinda Scarus zelindae (Moura, Figueiredo & Sazima, 2001) e o budiãovermelho Sparisoma amplum (Ranzani, 1842) (Fig. 1). Scarus trispinosus, a espécie de
budião mais abundante em Abrolhos, tem sido uma das mais pescadas, com significativa
redução populacional ao longo dos últimos anos (FRANCINI-FILHO; MOURA, 2008a, b).
Essa é a única espécie de budião do Atlântico Sul incluída na categoria “em perigo de
extinção” na Lista Vermelha de Espécies da IUCN (COMEROS-RAYNAL et al., 2012).
Figura 1. Indivíduos adultos (40-60 cm) das três espécies de budiões estudadas: Scarus
trispinosus (A), Scarus zelindae (B) e Sparisoma amplum (C). Fotos: A e C: Daniel Sartor; B:
Ronaldo B. Francini-Filho.
Em ambientes recifais brasileiros, estudos sobre budiões têm sido focados em aspectos
relacionados à sua alimentação, com ênfase no forrageamento (e.g. BONALDO et al.,
2006, FRANCINI-FILHO et al., 2010), dieta (e.g. FERREIRA; GONÇALVES, 2006) e predação
de corais (FRANCINI-FILHO et al., 2008), não havendo trabalhos voltados a explorar as
conexões entre design e performance. O alto nível de degradação nos recifes brasileiros
(MOURA et al., 2010), que apresentam baixa riqueza e reduzida redundância funcional,
demanda uma melhor compreensão dos processos ecológicos e evolutivos relacionados à
resiliência e à manutenção de propriedades funcionais desses sistemas. Assim, a
identificação de espécies-chave e dos papéis que elas desempenham é uma prioridade
para o delineamento de medidas de conservação, uma vez que mudanças nas
abundâncias e/ou frequências de ocorrência de determinadas classes de tamanho, podem
trazer consequências para toda a comunidade recifal.
O presente trabalho explorou relações entre forma e função de estruturas relacionadas à
alimentação em três espécies de budiões comuns no Banco dos Abrolhos, Sc. trispinosus,
5
Sc. zelindae e Sp. amplum. O estudo teve ênfase na ontogenia, performance alimentar e
bioerosão de Sc. trispinosus, buscando contribuir para elucidar o papel funcional dos
budiões desempenham nos recifes do Atlântico Sul.
OBJETIVO GERAL
Explorar, dentro da abordagem ecomorfológica comparativa, estruturas relacionadas à
alimentação de três espécies de budiões comuns no Banco dos Abrolhos, Sc. trispinosus,
Sc. zelindae e Sp. amplum, com ênfase na ontogenia, na performance alimentar e na
bioerosão desempenhada por Sc. trispinosus, a maior espécie de budião e o peixe recifal
mais abundante nessa região.
OBJETIVOS ESPECÍFICOS

Descrever e quantificar semelhanças ecomorfológicas entre as três espécies
estudadas;

Avaliar variações ontogenéticas relacionadas à ecomorfologia de Sc. trispinosus;

Avaliar as taxas de alimentação de Sc. trispinosus, a fração e os volumes de
mordidas que deixam marcas evidentes no substrato;

Estimar as taxas de bioerosão diária e anual por Sc. trispinosus.
6
ECOMORPHOLOGY, FEEDING PERFORMANCE AND BIOEROSION OF PARROTFISHES
(LABRIDAE: SCARINAE) IN EASTERN BRAZIL
Parrotfishes from the Scarine tribe (Perciformes: Labridae) form a diverse group in reef
environments, and represent the majority of fish biomass in many of these ecosystems.
These fishes feed mainly on algae and detritus, but can also include corals in their diet.
The species are generally divided into three functional groups (grazer, scrapers and
excavators), with diversification in jaw apparatus related to different forms of foraging.
Parrotfish are considered a critical functional group in reef ecosystems, acting as
controllers of macroalgae and contributing to bioerosion. The objectives of this study
were to compare the ecomorphology of three species of parrotfish, Scarus trispinosus, Sc.
zelindae and Sparisoma amplum, with an emphasis on ecomorphology, feeding
performance and bioerosion of Sc. trispinosus, the largest species of parrotfish and the
most abundant in the Abrolhos Bank, a region with the highest coral reef diversity of the
Southern Atlantic Ocean. Premaxilla, dentary and mouth configurations distinguish the
three species and the different size categories of Sc. trispinosus. The weakest and most
mobile oral apparatus of Sc. zelindae and the smaller category from the other species can
be predominantly classified as scrapers. Contrastingly, individuals from the large category
of Sc. trispinosus and Sp. amplum exhibit a robust oral jaw apparatus with simple joints
and are predominantly classified as excavators. In Sc. trispinosus, a strong relationship
was found between the size of the individuals, their feeding rate and volume of substrate
removed from the bites, showing a progressive increase in their ability to excavate.
Depending on the frequency of consumption of different food items, as well as their
relative abundances, species will have different roles in the reef system. In Abrolhos,
bioerosion is exercised only by large individuals of the two parrotfish species (Sc.
trispinosus and Sp. amplum). For Sc. trispinosus, the principal specie, the volume of reef
substrate removed per individual per day was estimated to be 206.94 cm³ and erosion
rates of 75,534.14 cm³ per year. The scenario of overfishing is intensifying and can lead to
profound restructuring in the functioning of reef ecosystems, especially in systems with
low diversity and low functional redundancy, such as South Atlantic reefs. The removal of
the largest ones of these species, one of the first effects of overfishing, may result in such
restructurings, with consequences still poorly understood.
Key words: coral reefs, herbivory, jaw morphology, Abrolhos Bank.
7
INTRODUCTION
Parrotfishes (Labridae: Scarinae) are a speciose clade (~100 species in ten genera) that is
considered one of the most important functional groups in reef ecosystems (Streelman et
al. 2002). In tropical regions they may be the dominant group in terms of fish biomass (up
to 50% of fish biomass) and consumption of the benthic primary production, controlling
algal blooms (Horn 1989; Bellwood et al 2004). Parrotfishes are characterized by unique
beak-like fused teeth within a specialized jaw apparatus that allows highly effective
feeding on algae attached to hard substrates (Bellwood & Choat 1990). Although generally
categorized as herbivores, parrotfishes might be more appropriately placed into an
herbivore-detritivore guild of large-bodied roving and schooling fishes (Wilson et al. 2003),
as their diet may include large amounts of detritus (Crossman et al. 2001; Wilson et al.
2003). Corallivory is also frequent among parrotfishes and may partially counterbalance
their positive effects over corals (Mumby 2009). Indeed, diet and feeding behavior
commonly change during development, and can also differ among species and areas
(Bellwood 1988, Choat et al. 2002). Therefore, parrotfishes’ role in reef systems may be
variable, depending on the regional species pool and on their density and body-size
distribution, besides context-dependent availability of food resources (Bonaldo &
Bellwood, 2008, 2014).
Globally, reefs are facing increasing impacts from climate change, eutrophication and
overfishing (Harvell et al. 2002; Hughes et al. 2003; Bellwood et al 2004). Therefore, it is
increasingly important recognize the functional traits of these highly diverse and
productive ecosystems. In the last two decades, following the widespread demise of
carnivorous fish from overfishing, parrotfishes became a preferred target in reef fisheries
(Jackson et al. 2001; Comeros-Raynal et al. 2012), leading to decreasing densities and
extirpation of larger size-classes. Understanding the different functional performances of
parrotfishes allows for the identification of their specific roles in ecosystem functioning,
8
and their potential contribution to reef health under such restructured parrotfish
assemblages (Wainwright et al 2002).
Based on functional morphology, ecology and size, parrotfishes are grouped into three
functional groups (Bellwood & Choat 1990). Browsers feed mainly on algae and detrital
material overlying the substrate, without exerting significant impacts on the reef matrix,
but significantly reducing algal growth (Hughes 1994; McCook et al. 2001). Scrapers
remove thin substrate pieces while feeding, potentially facilitating the settlement and
survival of coral and coralline algae recruits (Hunte & Wittenberg 1992; Steneck 1988;
McCook et al. 2001). Excavators are those that can leave large and well-evident scars on
the carbonatic framework (Bellwood & Choat 1990; Bellwood et al. 2003), and this feeding
mode is considered one of the main bioerosion pathways in tropical reefs (Bellwood &
Choat 1990; Bruckner et al. 2000; Streelman et al. 2002). Excavators remove crustose
calcareous algae, turf and/or epilithic algae, exposing new areas of the reef matrix for
colonization (Bellwood et al. 2003, 2004). This latter feeding mode is considered one of
the main bioerosion pathways in tropical reefs (Bellwood & Choat 1990; Bruckner et al.
2000; Streelman et al. 2002), but detailed information about jaw morphology, feeding
behavior and actual bioerosion capabilities are lacking for most species, impeding a
thorough recognition of the roles of parrotfishes in reef ecosystems across the globe.
The tropical Southwestern Atlantic (Brazil) encompasses some of the world’s least known
reef systems, with low species diversity (~20 species of reef building corals, 50% endemic)
and high levels of endemism and threat (deforestation, pollution, urban sprawl,
overfishing) concentrated in a small reef area (5% of Atlantic reefs) (Moura 2000). The
region’s largest and richest biogenic reefs occur across the 45,000 km 2 of relatively
shallow waters in the Abrolhos Bank (Moura et al. 2013), where six Brazilian-endemic
parrotfishes are known to occur (Moura et al. 2001; Moura & Francini-Filho 2006). Three
of those species are remarkable for their large size, abundance and potential
disproportionate role in ecosystem functioning: the greenbeack parrotfish, Sc. trispinosus,
9
the zelinda’s parrotfish, Sc. zelindae, and the red parrotfish, Sp. amplum; all recognized as
potential excavators depending on body size (Ferreira & Gonçalves 2006; Francini-Filho &
Moura 2008a; Francini-Filho et al. 2008). These three sympatric species occurring in a low
diversity system which provide a relevant context to explore different functional roles,
once just few parrotfishes species perform important functions (Francini-Filho et al. 2008,
2010). In addition, although the greenbeack parrotfish is still the most abundant reef fish
in the Abrolhos Bank (Francini-Filho & Moura 2008a,b), it is already red-listed as an
Endangered Species, as its abundance has fallen dramatically along most of its distribution
range (Padovani-Ferreira et al. 2012). Previous studies in Brazilian reefs investigated
selected aspects of parrotfish foraging activity (Bonaldo et al. 2006; Francini-Filho et al.
2010), diet (Ferreira & Gonçalves 2006) and corallivory (Francini-Filho et al. 2008a), but
there is a lack of studies connecting design and performance (e.g. Motta & Kotrscha 1992;
Wainwright et al. 2002) and addressing specific feeding and bioerosion capabilities of
these species (e.g. Bellwood & Choat 1990; Bellwood 1995a; Bruggemann 1996).
Ecomorphology links morphology to ecology through performance assessments
(Wainwright 1994, 1996), using osteological and morphometric attributes as indicators of
interactions between the organism and its habitats (Gatz 1979; Winemiller 1991, 1992;
Gibran 2010). Given the high level of degradation in the low diversity Brazilian reefs,
studies with key species should be particularly relevant to understand how critical
functional groups, like parrotfishes, impact the whole community (Bellwood et al. 2004;
Estes et al. 2011). Here, we explored functional aspects of three large-bodied sympatric
parrotfishes: the Greenbeack (Sc. trispinosus), Zelinda (Sc. zelindae) and Red parrotfish
(Sp. amplum), using the ecomorphological approach and accounting for ontogenetic
variation. We also explored the feeding and bioerosion rates of the greenbeack parrotfish,
the main excavator parrotfish in the South Atlantic, with the aim to provide a first
estimate of its role as a bioeroder in this poorly know region with very specific and unique
characteristics.
10
MATERIALS AND METHODS
Study Area
The Abrolhos Bank (16-20S, 37-39W) encompasses three main benthic megahabitats:
rhodolith beds (~20,900 km²), unconsolidated sediments (~9,200 km²) and coralline reefs
(~8,800 km²) (Moura et al. 2013). The four sampling sites included in this study are located
within the reef megahabitat, encompassing two reef arcs: one closer to the coast (~12 km
offshore) and more exposed to natural and anthropogenic impacts (e.g. sedimentation,
fishing) (sites Pedra de Leste and Timbebas) and the other in the mid shelf (~60 km
offshore), less impacted by land-based stressors (sites Abrolhos Archipelago and Parcel
dos Abrolhos). Sites in the outer arc are included within a relatively well enforced no-take
zone of the Abrolhos National Marine Park (ANMP) (Francini-Filho & Moura 2008). In the
inner arc, most reefs are included in a large “paper park” and are open to intense fishing,
with the exception of Timbebas, which is included in a partially protected zone of the
ANMP. The sampled sites (Fig. 1) include rocky reefs with sparse corals in the Archipelago
and coralline reefs in the inner and outer arc, these latter formed by mushroom-shaped
pinnacles that reach near the surface and may have fused tops forming larger banks
(Laborel 1969; Francini-Filho et al. 2013). Soft sediments, seagrass (Halodule and
Halophila) and algal bottom surround the reefs, with the largest vegetated bottoms
around the Archipelago (Creed & Amado-Filho 1999).
11
Figure 1. Map of the study region showing the Abrolhos National Marine Park boundaries
(gray polygons) and sampling sites: (1) Pedra de Leste (inner arc, unprotected reef), (2)
Timbebas (inner arc, partially protected reef), (3) Abrolhos Archipelago (enforced no-take
zone; Marine Protected Area), (4) Parcel dos Abrolhos (outer arc, enforced no-take zone;
Marine Protected Area).
Ecomorphology
For intraespecific and interespecific comparisons of the ecomorphology of the three
studied parrotfishes, we have analysed the structure of jaw apparatus of specimens
collected across the study region (n=29). At least three individuals of each species, for
each of the two size categories (small and large, see below), were used for interspecific
comparisons. Only similar-sized specimens (less than 20% of variation) were included in
each size class, to avoid allometric growth effects (Wikramanayake 1990). While the three
species are protogynous hermaphrodites, only Sc. zelindae and Sp. amplum have
remarkable dichromatism (Moura et al. 2001). Therefore, for Sc. zelindae we used initial
phase (IP) individuals 20cm of total length (TL) (small size class) and terminal phase (TP)
12
individuals 35cm TL (large size class), while for Sp. amplum we used IP individuals 25cm TL
(small size class) and TP individuals 60cm TL (large size class). For Sc. trispinosus,
individuals 25cm TL were included in the small size class, and individuals 55cm TL in the
large size class. For the intraspecific analysis of Sc. trispinosus we used 3-7 individuals in
each of the following sizes (also with less than 20% of variation): 15, 20, 30, 40, 50, 60 cm
TL (n=28).
Structures associated to feeding were measured in fresh specimens that were further
preserved in 10% formalin. To reduce the weight of one or a few variables, as well as to
allow for biological and functional interpretations (Keast & Webb 1966; Winemiller 1991),
five ecomorphological attributes were calculated following Gatz (1979) and Gibran (2007,
2010): (1) Head Length (HL), maximum length of the head divided by Standard Length (SL);
(2) Mouth Width (MW), interior lateral dimension of the mouth (fully opened) divided by
SL; (3) Mouth Height (MH), dorsal-ventral dimension of the mouth (interior) divided by SL;
(4) Mouth Configuration (MC), interior dorsal-ventral dimension of the mouth divided by
its lateral dimension (interior); (5) Head Configuration (HC), dorsal-ventral dimension of
the head divided by its lateral dimension at the eyes’ level.
The five principal structures of the jaw apparatus were extracted by boiling and were
subsequently dried and weighted (Bellwood & Choat 1990): (1) Premaxilla (P); (2) Maxilla
(M); (3) Dentary (D); (4) Articular (A) and (5) Suspensorium (S). The operculum (O) was
also analyzed and was included as a control, representing a structure that is unrelated to
feeding (Bellwood & Choat 1990). Osteological attributes were calculated using the weight
of the bones relative to the weight of eviscerated specimens, to reduce bias related to the
repletion level of the digestive tube and/or maturity stage.
To assess morphological similarity, rectangular data matrices with the mean values of
morphometric and osteological attributes were transformed into variance/covariance
matrices and submitted to Principal Component Analyses (PCA) using the Past Software
13
ver. 2.16 (Hammer et al. 2001). The use of ratios allows for the interpretation of the first
PCA orthogonal axis as a shape-related axis, rather than size-related, also reducing the
chance of bias due to dominance of a single variable, such as body size (Winemiller 1991).
One-way analysis of variance (ANOVA) and the Student-Newman-Keuls (SNK) post hoc test
(Zar 1999) were employed to compare the morphometric and osteological attributes
among the six morphotypes (three species, each one with two size classes).
Feeding activity and bioerosion (performance) of Sc. trispinosus
Feeding activity and bioerosion estimates were conducted by four divers in February 2012
and 2013, at four sites (Fig. 1). Observations were evenly distributed along the day and
started just after sunrise, before initiation of feeding, lasting until 18:00, when all
parrotfish feeding had ceased. Feeding rates were quantified in replicate 1-minute
observation periods (cf. Francini-Filho et al. 2008a) during which we recorded the number
of bites for fishes in six size categories (total lenght, TL): 10-15, 20-25, 30-35, 40-45, 50-55
and 60-70 cm (n=298). Observations were discarded if the individual was lost from sight or
showed disturbance signs. Four periods were further used to analyze daily feeding
patterns: morning (06:00-09:00), late morning (09:01-12:00), afternoon (12:01-15:00) and
late afternoon (15:01-18:00). Additional observations were done by following individuals
(15-60 cm TL) until a visible bite was located. Total number of bites was noted, with forays
used as replicas (n=225). A foray consisted in a series of bites with no visible interval
between them (cf. Bellwood & Choat, 1990). The observer also checked how many bites
left visible marks, assessing the number of significant bites (i.e. those leaving grazing
scars) in a foray event (Bruggemann 1996).
For bioerosion estimates, grazing scars (n=39, individuals >30 cm TL) were collected with
hammer and chisel, always on a same substratum type: calcareous matrix covered by
crustose calcareous algae (CCA) turf and epilithic algae. The size of the individual that left
the scar was noted and the sample was brought to the surface, labeled, photographed,
fixed in 4% formalin and subsequently stored in 10% alcohol. In the laboratory, scars were
14
analyzed for bite volume using alginate impressions with chlorhexidine (cf. Bellwood
1995a). Five molds of each bite were made to minimize filling errors. After drying, molds
were removed and weighed, and the volumes of the bites were estimated based on mean
weight of the five molds and alginate density.
For estimating daily feeding rates, time was standardized to minutes after midnight and
day length (DL) was taken as the time from sunrise to sunset (Bellwood 1995a). Feeding
day length (FDL) is defined as the time from the first recorded bite to the last recorded
bite on a given day (recorded in minutes). The proportion of the day spent feeding equals
to FDL x 100/DL (Bellwood 1995a). To calculate the total number of bites taken in a day,
feeding rate (adjusted to bites/min) was plotted against time. As feeding initiation and
termination was abrupt, all zero values were removed. A quadratic polynomial line was
then fitted to the data and the area under the curve was calculated, representing the total
number of bites taken on that day (cf. Bellwood 1995a). To ensure a representative
sample size, calculations were made for two pooled size categories (<29 and > 30 cm TL).
Erosion rates were estimated using bite volumes, significant bites and daily feeding rates
from fish >30 cm TL (i.e. those leaving significant bites and consistently contributing to
bioerosion). Erosion rates estimates follow Bellwood (1995a), with the modification
proposed by Bruggemann (1996), as follows:
Erosion rate per bite (m³ x bite¯¹) = mean bite volume x proportion of significant bites.
Erosion rate per day (m³ x ind¯¹ x d¯¹) = erosion rate per bite x mean daily bite rate.
Annual erosion rates were calculated by multiplying daily rates by 365, with overall error
terms calculated using the Goodman's estimator (Travis 1982). A regional extrapolation of
total bioerosion by Sc. trispinosus was done from mean density data collected during five
subsequent summers (2005-2009) in eight sites within the inner arc, five in the outer arc
15
and five in the Archipelago. Fish counts were performed using a stationary visual census
technique (Minte-Vera et al. 2008), with individuals recorded in the following size classes:
<10, 10-20, 21-30, 31-40, >40cm TL. Fifteen to 20 samples were obtained per site/year,
totaling 1,999 samples. Mean density of Sc. trispinosus (indiv./m2) for fishes > 30cm were
estimated for each of the three areas (inner arc, outer arc and Archipelago) and were
extrapolated to their respective areas, obtained from remote sensing (Moura et al. 2013).
Abundance of Sc. trispinosus individuals >30 cm TL were further multiplied by the
individual bioerosion rates.
RESULTS
Ecomorphology
In the PCA ordination with morphometric attributes of the three species most of the
variance (99.98%) was explained by the two principal components (PC), with the first axis
(PC1) accounting for 61.3% of the variation, and the second (PC2) accounting for 38.7%
(Tab. 1). These two PC were largely influenced by mouth and head configurations (Tab. 1
and Fig. 2), with a clear discrimination of small and large specimens (negative and positive
values on PC 2, respectively), for all species (Fig. 2).
Table 1. Eigenvalues, variance, eigenvectors and r values of the two Principal Components
of the ordination with morphometric and osteological attributes from Scarus trispinosus,
Sc. zelindae and Sparisoma amplum.
Eigenvalues
% variance
total variance
Morphometrics attributes
Axis 1
Axis 2
0,141
0,089
61,29
38,69
99,98
Eigenvectors
r
Eigenvectors
r
16
Mouth configuration
Head configuration
Mouth height
Mouth width
Head length
Eigenvalues
% variance
total variance
Dentary
Premaxilla
Suspensorium
Maxilla
Operculum
Articular
0,7732
0,8384
-0,6326
-0,545
0,6331
0,7173
0,774
0,6968
0,02676
0,885
-0,01321
-0,3473
-0,02379
-0,7688
0,02319
0,5953
-0,003325 -0,2931 -0,002449 -0,1715
Osteological attributes
Axis 1
Axis 2
1,27E-06
1,34E-07
89,759
9,5245
99,28
r
r
Eigenvectors
Eigenvectors
0,6878
0,9535
-0,6641
-0,2999
0,6711
0,9437
0,722
0,3307
0,2536
0,9406
-0,1509
-0,1823
0,08577
0,92
0,07489
0,2617
0,05549
0,8293
0,09369
0,4561
0,04269
0,93
-0,02385
-0,1692
17
Figure 2. Distribution of the three parrotfish species and two size classes (S = small; L =
large) in a two-dimensional morphospace based on scores from the first two principal
components from morphometric attributes (cumulative % of variance = 99.98%; see Table
1). MW = Mouth Width; HL = Head Length; MH = Mouth Height.
In the ordination with osteological attributes, most of the variance (99.28%) was
explained by the two first principal components (PC1 accounting for 89.8% and PC2 for
9.52% of the total variation), with dentary, premaxilla and suspensorium representing the
most influential attributes (Tab. 1; Fig. 3). Considering the relative weight of bony
structures as an indicative of their relative strength, PC1 discriminated the size classes
with the greatest excavating potential (right side) (Fig. 3), while PC2 corresponds to
osteological discrimination between the two genera, with Sc. trispinosus presenting the
strongest premaxilla and large individuals of Sp. amplum the strongest dentary. The Oneway Analysis of Variance (ANOVA) showed significant differences (p<0.05) among all
ecomorphological attributes (morphometric and osteological) with the exception of head
length (HL; p=0.95) (Tab. 2).
18
Figure 3. Distribution of the three parrotfish species and sizes (S = small; L = large) in a
two-dimensional morphospace based on scores from the first two principal components
from osteological attributes (cumulative % of variance = 99.28; see Table 1). MA = maxilla;
OP = operculum; AR = articular.
Table 2. One-way ANOVA with the 11 ecomorphological attributes for Scarus trispinosus,
Sc. zelindae and Sparisoma amplum in the two size categories (small and large). Highest F
values are highlighted in bold. df = degrees of freedom; SS = sum of squares.
Source
Mouth width
df
SS
F
P
5
0.003
6.00
0.0011
19
Mouth height
5
0.004
3.86
0.0110
Mouth configuration
5
3.374
4.05
0.0088
Head configuration
5
2.308
5.33
0.0021
Head length
5
0.000
0.21
0.9536
Premaxilla
5
0.000
36.12
0.0000
Dentary
5
0.000
28.30
0.0000
Maxilla
5
0.000
6.49
0.0007
Articular
5
0.000
7.58
0.0002
Suspensorium
5
0.000
9.22
0.0001
Operculum
5
0.000
10.18
0.0000
The SNK post hoc test evidenced four groups aggregated by similarities in the mean values
of the premaxilla (Tab. 3) and three groups by similarities in the mean value of the dentary
(Tab. 3) of the small and large categories of Sc. trispinosus, Sc. zelindae and Sp. amplum.
The premaxilla of small Sc. zelindae and small Sp. amplum had the lowest mean values,
while small Sp. amplum were similar to small Sc. trispinosus and large Sc. zelindae, and just
this last one had equal statistics to large Sp. amplum. Large Sc. trispinosus had the highest
premaxilla values, significantly different from all other entities. Analyzing the dentary,
Small Sc. zelindae had the lowest mean values. Small Sc. trispinosus and Sc. zelindae,
together with large Sc. zelindae presented similar values, while large Sc. trispinosus and
large Sp. amplum had the higher dentary means, and those are significantly similar to each
other. In the case of the morphometric means, attributes with highest F values were
mouth width and head configuration (Tab. 3). Large Sp. amplum had the highest mouth
width values, differing significantly from others species and sizes. On the other hand, small
Sp. amplum showed the lowest head configuration value, which was significantly different
from all others entities.
Table 3. Mean values (±SE) for the five morphometric and six osteological attributes calculated for small (S) and large (L) individuals
of Scarus trispinosus (Sca tri), Sc. zelindae (Sca zel) and Sparisoma amplum (Spa amp). MW = mouth width; MH = mouth height; MC
= mouth configuration; HC = head configuration; HL = head length; PM = premaxilla; D = dentary; MA = maxilla; AR = articular; SU =
suspensorium; OP = operculum. Means followed by the same lowercase letters indicate homogeneous groups (SNK test p>0.05).
Morphometric attributes
MW
MH
MC
HC
HL
Sca tri (S)
0.06 (0.01) a
0.08 (0.02) a
1.59 (0.85) b
1.91 (0.11) a
0.33 (0.01) a
Sca tri (L)
0.08 (0.01) b
0.05 (0.01) b
0.64 (0.17) a
1.80 (0.4) a
0.33 (0.01) a
Sca zel (S)
0.06 (0.01) a
0.08 (0.01) a
1.36 (0.34) ab
1.72 (0.28) a
0.33 (0.03) a
Sca zel (L)
0.06 (0) a
0.09 (0) ab
1.22 (0.03) ab
1.69 (0.05) a
0.34 (0.01) a
Spa amp (S)
0.06 (0.01) a
0.08 (0.02) a
1.33 (0.23) ab
2.58 (0.38) b
0.33 (0.02) a
Spa amp (L)
0.08 (0.01) b
0.07 (0.01) ab
0.89 (0.13) ab
1.88 (0.3) a
0.34 (0) a
SU
OP
PM
D
MA
AR
Sca tri (S)
0.0019 (±0.0001) a
0.0017 (±0.0004) a 0.0003 (±0.0001) ab 0.0002 (0) ab 0.0014 (±0.0002) a
0.0006 (±0.0001) a
Sca tri (L)
0.0036 (±0.0006) d
0.0030 (±0.0004) b
0.0005 (±0.0001) b
0.0003 (0) c
0.0017 (±0.0002) b
0.0007 (±0.0001) a
Sca zel (S)
0.0013 (±0.0002) b
0.0012 (±0.0001) c
0.0002 (0) a
0.0002 (0) a
0.0009 (±0.0001) a
0.0005 (0) b
Sca zel (L)
0.0022 (±0.0001) ac
0.0018 (0) a
0.0004 (0) ab
0.0002 (0)
0.0013 (±0.0001) a
0.0006 (0) a
Spa amp (S)
0.0017 (±0.0003) ab 0.0020 (±0.0003) a
0.0003 (±0.0001) a
0.0002 (0) a
0.0012 (±0.0003) a
0.0005 (0) b
Spa amp (L)
0.0025 (±0.0003) c
0.0033 (±0.0006) b
0.0004 (0) ab
0.0003 (0) bc 0.0018 (±0.0004) b
0.0006 (±0.0002) a
Morphology of jaws bones of the three studied species is shown in Figs 4 and 5. In Scarus,
mouth closes with the premaxilla in front of the dentary, with an opposite situation in
Sparisoma. The premaxilla of the two Scarus species exhibited a long ascending process
(short in Sp. amplum) and the alveolar process lacks a maxillary fossa (present in Sp.
amplum). Dental plates in both Scarus species are large and deep (small and shallow in Sp.
amplum) and they present a large number of overlapped small teeth (one row of larger
teeth in Sp. amplum). The maxillary facet of Sc. trispinosus is long and narrow and its
cutting edges are crenate (relatively even in Sc. zelindae and Sp. amplum). Scarus
trispinosus presented a relatively thick layer of blue-green cement (white in Sc. zelindae)
and Sc. zelindae (L) has three lateral canines on the premaxilla at the end of the teeth row
in the anterior part of the alveolar process. Two lateral canines are also present in Sp.
amplum (absent from Sc. trispinosus). The dentary of the two Scarus species have
coronoid process with rounded cutting edges (crenate in Sp. amplum) and a poorly
developed articular socket (more extensive and well developed in Sp. amplum). The
maxilla of Sp. amplum showed an unusual grooved process, where the maxillary arm abuts
the premaxilla and the maxillary arm is limited to the alveolar process of premaxilla. Its
premaxilla process is broad and elongate, extending vertically up to the middle of the
bone. The articular of Sp. amplum is triangular, with a medial flange on the descending
process extending up to the anterior ascending process (flange reduced to an articular
medial spine in the two Scarus species).
22
Figure 4. Premaxilla (upper row) and dentary (lower row) of Scarus trispinosus (A), Sc.
zelindae (B) and Sparisoma amplum (C). ASP = ascending process; DP = dental plates;
ALP = alveolar process; LC = lateral canines; AP = articular process; AS = articular
socket; CP = coronoid process.
Figure 5. Maxilla (upper row) and articular (lower row) of Scarus
trispinosus (A), Sc. zelindae (B) and Sparisoma amplum (C). PMP =
premaxilla process; GP = grooved process; S = spine; F = flange.
23
There was strong ontogenetic variation in Sc. trispinosus (Fig. 6). The first PCA component
(PC1) of the ordination with morphometric attributes (six size classes) explained 82.68% of
the variance, and the two PC were largely influenced by mouth and head configurations
(Tab. 4; Fig. 6).
Components of the ordination with the morphometric and osteological attributes of six
size categories of Scarus trispinosus (±15; ±20; ±30; ±40; ±50 and ±60 of total length).
Morphometric attributes
Eigenvalues
% variance
total variance
Mouth configuration
Head configuration
Mouth height
Mouth width
Head length
Axis 1
Axis 2
0.13094
82.68
0.0267976
16.921
99.6
Eigenvectors
0.992
0.1167
0.03291
-0.03507
-0.001453
r
0.9986
0.2515
0.8441
-0.8273
-0.02271
Eigenvectors
-0.1164
0.9925
0.0003533
0.0102
-0.03526
r
-0.05302
0.9679
0.0041
0.1088
-0.2494
Eigenvalues
% variance
total variance
Premaxilla
Dentary
Maxilla
Articular
Suspensorium
Operculum
Axis 1
2.01E-06
97.873
Axis 2
2.83E-08
1.3791
99.25
Eigenvectors
0.7521
0.606
0.07605
0.03632
0.2373
0.06053
r
0.7521
0.606
0.07605
0.03632
0.2373
0.06053
Eigenvectors
-0.1835
-0.1775
0.1855
0.1081
0.8603
0.3855
r
-0.1835
-0.1775
0.1855
0.1081
0.8603
0.3855
24
Figure 6. Distribution of the six size classes of Scarus trispinosus in a two-dimensional
morphospace, based on scores from the first two morphometrical principal component
axes. MW = mouth width; HL = head length; MH = mouth height.
In the ordination with osteological attributes, most of the variance (99.25%) was also
explained by the two first principal components (PC1 97.9% and PC2 1.4% of the total
variation), with dentary, premaxilla, suspensorium and operculum representing the most
influential attributes (Tab. 4; Fig. 7) and larger Individuals (TL ≥ 40 cm) with stronger jaw
apparatus at the right side or the ordination diagram. The power of the premaxilla and
dentary is well evident for the largest size, as they are strongly related with the premaxilla
and dentary in the PCA (Fig. 7). The One-way ANOVA showed significant differences
25
(p<0.05) among almost all ecomorphological attributes of the six size categories of Sc.
trispinosus (Tab. 5), with the exception of head configuration (HC) and head length (HL).
Premaxilla, mouth configuration and dentary showed the higher variation among the six
size categories, as indicated by the highest F values in the ANOVA (Table 5).The SNK post
hoc test evidenced five groups aggregated by similarities in the premaxilla and dentary,
with a clear size-related pattern (Table 6). The operculum did not show such variation,
allowing for the interpretation of results as functional differences related to feeding.
Figure 7. Distribution of the six size classes of Scarus trispinosus individuals in a twodimensional morphospace, based on scores from the first two osteological principal
26
component axes (cumulative % of variance = 99.25; see Table 4). MA = maxilla; OP =
operculum); AR = articular.
Table 5. One-way ANOVA with the 11 ecomorphological attributes of the six size
categories (±15; ±20; ±30; ±40; ±50 and ±60 cm of total length) of Scarus trispinosus.
Highest F values are highlighted in bold. df = degrees of freedom; SS = sum of squares.
Source
df
SS
F
p
Mouth width
5
0.0041
13.011
0.0000
Mouth height
5
0.0030
4.838
0.0036
Mouth configuration
5
2.913
23.592
0.0000
Head configuration
5
0.0683
0.452
0.8072
Head length
5
0.0026
1.029
0.4241
Premaxilla
5
0.0000
29.618
0.0000
Dentary
5
0.0000
19.757
0.0000
Maxilla
5
0.0000
8.632
0.0001
Articular
5
0.0000
8.688
0.0001
Suspensorium
5
0.0000
12.103
0.0000
Operculum
5
0.0000
5.836
0.0012
Table 6. Mean values (±SE) of the five morphometric and six osteological attributes of Scarus trispinosus (size categories ±15 cm; ±20
cm; ±30 cm; ±40 cm; ±50 cm and ±60 cm TL). MW = mouth width; MH = mouth height; MC = mouth configuration; HC = head
configuration, HL = head length; PM = premaxilla; D = dentary; MA = maxilla; AR = articular; SU = suspensorium; OP = operculum.
Means followed by the same lowercase letters in the same column indicate homogeneous groups (SNK test p>0.05).
Morphometric atributes
MW
MH
MC
HC
HL
±15 cm
0.06 (±0.01) a
0.08 (±0) b
1.47 (±0.23) d
1.93 (±0.23) a
0.32 (±0.03) a
±20 cm
0.06 (±0.01) ab
0.07 (±0.01) ab
1.24 (±0.14) c
1.84 (±0.09) a
0.33 (±0.02) a
±30 cm
0.06 (±0) ab
0.06 (±0.01) ab
1.12 (±0.16) bc
1.86 (±0.22) a
0.34 (±0.02) a
±40 cm
0.07 (±0) bc
0.07 (±0) ab
0.92 (±0.1) b
1.78 (±0.07) a
0.35 (±0.01) a
±50 cm
0.08 (±0.01) cd
0.05 (±0.01) a
0.64 (±0.17) a
1.88 (±0.18) a
0.32 (±0.02) a
±60 cm
0.09 (±0.01) d
0.05 (±0.01) a
0.6 (±0.03) a
1.78 (±0.1) a
0.32 (±0.02) a
PM
D
MA
AR
SU
OP
±15 cm
0.0014 (±0.0001) a
0.0012 (±0.0001) a
0.0002 (<0.0001) b
0.0002 (<0.0001) a
0.0011 (±0.0001) a
0.0005 (±0.0001) a
±20 cm
0.0015 (±0.0002) a
0.0012 (±0.0001) a
0.0002 (<0.0001) b
0.0002 (<0.0001) a
0.0011 (<0.0001) a
0.0005 (±0.0001) ab
±30 cm
0.0018 (±0.0001) a
0.0015 (±0.0005) a
0.0003(±0.0001) ab
0.0002 (<0.0001) a
0.0013 (±0.0002) a
0.0006 (±0.0001) ab
±40 cm
0.003 (±0.0004) b
0.0024 (±0.0004) b
0.0004 (±0.0001) a
0.0003 (±0.0001) b
0.0018 (±0.0003) b
0.0008 (±0.0001) c
±50 cm
0.0035 (±0.0007) bc
0.0028 (±0.0005) b
0.0005 (±0.0001) a
0.0003 (±0.0001) b
0.0018 (±0.0002) b
0.0007 (±0.0001) bc
±60 cm
0.0039 (±0.0005) c
0.0031 (±0.0004) b
0.0004 (<0.0001) a
0.0003 (<0.0001) b
0.0016 (±0.0001) b
0.0007 (<0.0001) abc
Feeding activity and bioerosion (performance) of Scarus trispinosus
Feeding rates, proportion of significant bites per foray and bite volume estimates for Sc.
trispinosus in the Abrolhos Bank is summarized in Table 7. There was a significant sizerelated difference in feeding rates, with the largest category (60 cm TL) presenting the
smallest rate (1.52 bites/min), and the smallest category (10 cm TL) presenting the highest
(8.54 bites/min). The proportion of significant bites per foray was also related to size, and
two groups presented significantly different values, one including the smaller sizes (10, 20
and 30 cm TL), ranging from 9 to 30% of significant bites per foray, and the other including
the larger sizes (40, 50 and 60 cm TL), ranging from 59-75% of significant bites per foray.
Bite volume also increased with size, with individuals’ 50 and 60 cm TL biting up to five
times larger volumes than individuals’ 30 and 40 cm TL (0.12 ±0.09 vs. 0.04 ±0.03 cm³,
respectively).
Table 7. Feeding rates, proportion of significant bites, bite volume and daily feeding rates
for each size-category of Scarus trispinosus in the Abrolhos Bank, Brazil. Means followed
by the same lowercase letters indicate homogeneous groups (SNK test p>0.05).
Size classes
(cm TL)
10
20
30
40
50
60
Feeding rates Significant bites per foray
(bites/min)
(%)
8.54 (±3.6) a
9a
8.49 (±7.3) a
11 a
7.54 (±4.8) a
30 a
6.84 (±4.8) a
59 b
3.06 (±3.4) b
60 b
Bite volumes
(cm³)
0.025 (±0.03) a
0.046 (±0.03) ab
0.13 (±0.12) b
1.52 (±1.8) b
0.11 (±0.07) ab
75 b
Daily feeding rates
(bites/day)
5,584.86 (<30 cm)
4,995.25 (>30 cm)
Table 8. One-way ANOVA performed on feeding rates, proportion of significant bites, bite
volume and feeding periods comparing the six size categories of Scarus trispinosus at the
Abrolhos Bank. df = degrees of freedom; SS = sum of squares.
29
Sources
Feeding rates
Significant bites
Bite volumes
Feeding periods
df
5
5
3
3
SS
1659.5
9.651
0.081
1840.2
F
16.65
10.83
4.25
32.96
p
0.00
0.00
0.01
0.00
Feeding rates of Sc. trispinosus differed significantly along the day (Tab. 8), peaking during
the late morning, between 09:00 and 12:00 (Fig. 8). Individuals <30 cm TL performed an
estimated 5,585 bites.day-1, while individuals >30 cm TL averaged 4,995 bites.day-1 (Tab. 8;
Fig. 8, 9). Bioerosion rates per bite of individuals >30 cm TL was estimated at 206.94
cm³ind¯¹.d¯¹, and annual erosion rates at 75,534.14 cm³ind¯¹.year¯¹. The overall error
Feeding rate (bites/min)
terms calculated with the Goodman’s estimator was 1,710.98.
14
12
10
8
6
4
2
0
0,5
1
06:00-09:00
1,5
2
09:01-12:00
2,5
3
12:01-15:00
3,5
4
4,5
15:01-18:00
Figure 8. Feeding rates (mean and standard error) of Scarus trispinosus throughout the
diurnal period.
30
y = -4E-05x2 + 0.0551x - 10.141
R² = 0.1103
Feeding rate (bites/min)
30
25
20
15
10
5
0
200
300
400
500
600
700
800
900
1000
1100
Time of day (minutes after midnigth)
Figura 9. Daily feeding of Scarus trispinosus (>30 cm TL) with a quadratic polynomial trend
line fitted to the data.
Parameters used for estimating bioerosion rates of Sc. trispinosus in the Abrolhos Bank
are summarized in Table 9. Higher densities of Sc. trispinosus were recorded in the rocky
reefs of the Archipelago, followed by the coralline reefs of the outer arc. Reefs in the inner
arc presented the lower densities. Bioerosion rates were greater in the outer arch,
followed by the inner arc and the Archipelago (Table 9).
Table 9. Parameters used for estimating bioerosion rates of Sc. trispinosus in the Abrolhos
Bank.
Strata
Reef area
(m2)
Mean density
(ind./m2)
Total abundance
(individuals >30 cm)
Daily bioerosion
(cm³/day)
Annual bioerosion
(cm³/year)
Inner arc
38.66 x 106
2.88 x 10-3
11.14 x 106
26.47 x 106
9.66 x 109
Outer arc
292.16 x 106
4.96 x 10-3
144.85 x 106
344.16 x 106
125.62 x 109
2.33 x 106
7.31 x 10-3
1.71 x 106
4.05 x 106
1.48 x 109
Archipelago
31
DISCUSSION
Parrotfishes are viewed as a key functional group in rocky and coralline reefs (Bonaldo et
al. 2014). These fishes represent some of the predominant top-down controllers of algae
and turf biomass (e.g. Mumby 2006), and playing important roles in sediment production
and transport (e.g. Bellwood 1995a,b; Bruggemann et al 1996), and coral predation (e.g.
Francini-Filho et al 2008; Bonaldo & Bellwood 2011). However, the impact of their feeding
activities in reef systems may be variable, depending on their relative abundance,
presence, relative abundance of other keystone herbivores (e.g. sea-urchins), and
differences in feeding modes and richness among the local parrotfish assemblage (e.g.
Hoey & Bellwood 2008). Despite the recent progress in assessing the feeding ecology of
parrotfishes (e.g. Bonaldo et al. 2006; Ferreira et al. 1998; Ferreira & Gonçalves 2006;
Francini-Filho et al. 2010), the tropical Southwestern Atlantic still remains a significant
knowledge gap in terms of their functional roles (Francini-Filho et al. 2008; Bonaldo et al.
2014). The present study provides the first ecomorphological comparison among the
Brazilian-endemic parrotfishes Sc. trispinosus, Sc. zelindae and Sp. amplum (Moura et al.
2001; Robertson et al. 2006), complemented with the first direct estimate of rates of
bioerosion combined with ecomorphology and feeding activity of the large-bodied and
endangered Sc. trispinosus.
Southwestern Atlantic reefs present an overall low diversity (Floeter et al. 2008; Bowen et
al. 2013), which may also imply in a relatively low functional diversity at this region
(Francini-Filho et al. 2008, 2010, 2013). For instance, while only five large-bodied
parrotfish species occur in Brazil, there are 10 such species in the Caribbean and at least
16 in the Indo-Pacific (Moura et al. 2001; Bellwood 1995a; Bonaldo et al. 2014). Nine
species are known to be excavators in the Indo Pacific and three in the Caribbean, while
only two species excavate in the tropical Southwestern Atlantic (Sc. trispinosus and Sp.
amplum) (Bonaldo et al. 2014). The three species studied herein represent 32.4% of the
total biomass of visually accessible reef fishes, and 56.7% of the biomass of large roving
32
herbivorous fishes in the Abrolhos Bank (Francini-Filho & Moura 2008), South Atlantic’s
largest and richest coralline complex. The loose of these parrotfishes could have a
profound impact on the local coral reef dynamics with consequences to a wide range of
species.
Our ecomorphological analyses revealed considerable differences among the three
species, and showed remarkable ontogenetic shifts involving mouth and head
configuration (shape) in Sc. trispinosus, Sc. zelindae and Sp. amplum. While smaller size
classes of the three species studied exhibit relatively larger mouths and slender bodies,
the mouth and head configuration of larger individuals clearly discriminates the scrapper
Sc. zelindae, which exhibits more mobile and complex jaw articulations, from the
excavators Sc. trispinosus and Sp. amplum (Figs. 2 and 3), which presented several traits
associated to this feeding mode. These include smaller gapes and simpler low-mobility jaw
articulations, similar to Indo-Pacific and Caribbean excavators (Bellwood & Choat 1990;
Bellwood 1994).
The shape of the mouth and head can also be related with the body position during
feeding (Price et al. 2010). Similar to other congeners and to Chlorurus and Hipposcarus
species, the genus Scarus presents an intramandibular joint that is responsible for
maintaining a constant orientation of the premaxilla, allowing for a larger opening of the
mouth when the body is in a vertical position. However, for stronger bites this particular
arrangement of the dentary and the articular demands a more inclined/perpendicular
feeding angle. The teeth of large sized Sc. trispinosus are small and present a crenate
cutting edge that decreases the contact area between the jaws and the substrate, typical
of excavators (Bellwood & Choat 1990). The cutting edges exhibited by Sc. zelindae, Sp.
amplum and by the small size individuals of all species are relatively even, as scrapers
species, and increases the contact area of the jaw, spreading the force over the substrate
(Bellwood & Choat 1990).
33
The discrimination of species and size categories in the ecomorphological space was
largely influenced by premaxilla and dentary weight (Tab. 1, Fig. 3). The relative weights of
oral structures are indicative of bite force, as heavier bones are associated to a greater
ability to excavate hard substrates (Bellwood & Choat 1990). For instance, larger-bodied
individuals of Sc. trispinosus (highest values for premaxilla weight) and Sp. amplum
(highest values for dentary weight) exhibited strong and heavier jaw bones, corresponding
to their ability to penetrate the hard carbonatic substrate and to feed on corals. Indeed,
Francini-Filho et al. (2008) recorded large (> 40 cm) specimens of Sc. trispinosus and Sp.
amplum feeding on the corals Mussismilia braziliensis, Montastrea cavernosa, Siderastrea
spp. and Favia gravida in the Abrolhos Bank reefs. Smaller individuals of these two species
presented a weaker jaw apparatus (Fig. 3), corresponding to a scrapping feeding mode in
the initial life stages (Francini-Filho et al. 2008). Scarus zelindae, on the other hand,
presented smaller ontogenetic variation in the premaxilla and dentary (Fig. 3),
corresponding to their scrapping feeding mode throughout the life. Early life stages of all
parrotfish species are browsers or scrapers, with a few larger species changing to an
excavating feeding mode when they attain larger sizes and acquire stronger jaw bones.
Our results confirm that, in the tropical Southwestern Atlantic, the largest Scarus (Sc.
trispinosus) and the largest Sparisoma (Sp. amplum) species are the most relevant
excavators in coralline reefs (Francini-Filho et al. 2008, 2010).
Although some morphological characteristics indicate convergences between the
excavating species (Bellwood 1994), especially in large-sized individuals, several jaw
structures of the three species reflect common ancestry at the genus level, rather than
convergences. These include the premaxilla with a large ascending process in the two
Scarus species (short in Sparisoma), the alveolar process without a maxillary fossa
(present in Sparisoma), and a narrow and elongated maxillary facet (broad and short in
Sparisoma), as well as a rounded coronoid process in the dentary (crenate in Sparisoma)
(Fig. 4). In Sp. amplum the articular socket (or articular fossa) is deep, presenting a
remarkable broad and flat tapering groove where the articular is bound to the dentary
34
(Fig. 4), a unique derived feature of Sparisoma (Bellwood 1994). Parrotfishes are divided in
two clades (Bellwood 1994, 1996; Streelman et al. 2002) that diverged ~42 million years
ago, one consisting of fishes primarily associated with algal beds (Sparisoma, Cryptotomus,
Nicholsina, Leptoscarus, Calotomus) and the other encompassing fishes that predominate
on coral reefs (Scarus, Bolbometopon, Cetoscarus, Hipposcarus and Chlorurus), this latter
including about 80% of all parrotfishes (76% of which belonging to Scarus and Chlorurus).
The origin of parrotfishes is associated to browsing in algal beds, with a subsequent
migration to coralline reefs, resulting in progressively stronger oral morphologies
(Bellwood 1994, 1996). Indeed, genera that predominate on coral reefs, such as Scarus,
have the most recent origin (Bernardi et al. 2000). The scraping feeding mode, typical of
most Sparisoma species and of small individuals of Sp. amplum, is an intermediary
condition between browsing algae and excavating hard bottom, this latter mode
presented by large-sized Sp. amplum individuals. Although some Sparisoma species or
species life phase presented feeding characteristics of both scraper and excavator feeding
mode, these similarities seems associated to functional convergence (Streelman et al.
2002, Robertson et al. 2006).
The level of parrotfish impact on the substrate is highly dependent on life stage (Bonaldo
& Bellwood 2008; Lokrantz et al 2008; Bonaldo et al. 2014), and the relative abundance of
large sized individuals has important implications in ecosystem functioning (Bonaldo &
Bellwood 2008). In Australia and the Caribbean, smaller initial phase Scarus and Sparisoma
exert similar impacts on the epilithic algal matrix, but large terminal phase individuals may
present different behavior, function and impact (Bellwood 1995a; Bruggemann et al.
1994b). In the present study, Scarus trispinosus and Sp. amplum presented strong
ontogenetic variation in jaw structures related to feeding (Figs 2 and 3). The feeding rates
of Sp. amplum don’t show significantly relationship with body size, while bite rates of Sc.
trispinosus were negatively correlated to body size and varied much more in relation to
size than the Sparisoma species (Francini-Filho et al. 2008). Although Sp. amplum is
regarded as a specialized corallivore (Francini-Filho et al. 2008; Bonaldo et al. 2014), its
35
abundance in the Abrolhos reefs is relatively low, with 10 times less biomass than Sc.
trispinosus (Francini-Filho & Moura 2008). Indeed, Sp. amplum is nearly absent from the
rocky reefs of the Abrolhos Archipelago, where most previous studies on parrotfish
feeding were carried out within the study region (e.g. Ferreira & Gonçalves 2006).
Therefore, we carried out more detailed ecomorphological analyzes, including six body
size categories, only for Sc. trispinosus, aiming to provide a more detailed assessment of
its bioerosion.
Smaller Sc. trispinosus individuals presented the highest feeding rates, a pattern that can
be associated to higher relative demand of energy by smaller individuals (Ferreira et al.
1998). Also, smaller size classes bite algal covered substrata more frequently than larger
individuals, an item with low nutritional value in comparison to detritus, possibly
demanding more feeding time (Francini-Filho et al. 2008, 2010). The highest feeding rates
of Sc. trispinosus observed from the late morning until the middle of the day is a common
pattern for herbivorous fish (Zemke-White et al. 2002; Bonaldo & Bellwood 2008),
possibly related to diel nutritional quality of algae (Bellwood 1995a), which increases in
the morning and peaks at midday, being maintained during the afternoon (Zemke-White
et al. 2002).
Frequency of significant bites was also directly related to body size (Tab. 9). The three
smaller size classes (10, 20 and 30cm TL) averaged 30% of significant bites per foray,
meaning that most forays only remove the superficial algal surface. On the other hand,
larger individuals (> 40cm TL) left visible marks on the substrate in up to 75% of the bites,
with significantly larger-volume scars (Tab. 9). Bruggemann (1996) reported large Sp.
viride leaving scars in approximately 80% of the bites taken in Caribbean reefs, while most
bites taken by juveniles did not left scars. Bonaldo & Bellwood (2008) also reported that
removed volume is significant greater in large individuals, while small individuals graze a
much larger substrate area. Our results add to the idea that small individuals control algal
growth by cropping algal surface, while large individuals excavate and open space in the
36
substrate for initial succession and coral settlement. Thus, large individuals of Sc.
trispinosus and Sp. amplum play a unique role as bioerosion agents in Abrolhos Bank, as
there is not another species that performs an equivalent function in this region.
Although the parrotfishes are able to interrupt benthic succession (Paddack et al. 2006;
Hughes et al. 2007), they may be unable to reverse a phase shift once it has occurred
(Bellwood et al. 2006). Thus, the absence of major macroalgal consumers in overfished
reefs ‘locks down’ the ecosystem as a fleshy algal pavement (Francini-Filho et al. 2010). In
the Abrolhos Bank, largest reefs are rhodolith beds (calcareous algae nodules) in the mid
and outer shelf (Moura et al. 2013), which present low structural complexity and high
macroalgal cover (Amado-Filho et al. 2012). While this system is within the depth range of
most parrotfishes, its low structural complexity may constrain survival of juvenile fish and
the establishment of a “complete” reef fish assemblage (author, unpubl. data), resulting in
macroalgal cover close to 100%. Low grazing intensities can induce the development of
climax communities characterized by fast growing taxa and low species diversity (Steneck
& Dethier 1994).
Estimates of parrotfish bite volumes may vary widely depending on substrate type,
species and individuals´ sizes, ranging from 0.002cm³ (Sc. niger, Red Sea) to 0.114
(Chlorurus gibbus, Australia) (Bellwood 1995a; Alwany et al. 2009). Scarus trispinosus
presents a relatively high mean bite volume, estimated at 0.0808 cm³ (all size categories
pooled). This mean bite volume is indeed higher than those for the four Scarus species
studied by Alwany et al. (2009), which ranged from 0.002 to 0.063cm³. Large individuals’
contribution to bioerosion is disproportionate, and the loss of these larger individuals will
reduce bioerosion even if the overall parrotfish biomass remains the same (Bruggemann
1996; Bonaldo & Bellwood 2008; Ong & Holland 2010). Smaller Sc. trispinosus individuals
(categories 30 and 40 cm) presented bite volumes two to five times smaller than the large
ones (50 and 60 cm TL) (Fig. 9).
37
In spite of its relatively large bite volumes, individual estimates of annual bioerosion rates
for Sc. trispinosus (0.076 m3.ind¯¹.year¯¹) are smaller than those for congeners such as Sc.
rubroviolaceus (0.216 m³.ind¯¹.year¯¹) (Ong & Holland 2010), as it presents lower bite
frequencies (4.955 versus 7,560 bites.day-1) and a smaller proportion of significant bites
(51 versus 84%). However, global bioerosion rates by parrotfishes is dependent on factors
such as abundance and size structure of the population, as well as on substrate type
(Bellwood 1995a; Bruggemann 1996; Bonaldo & Bellwood 2008; Alwany et al. 2009; Ong
& Holland 2010).
For instance, bioerosion by Sc trispinosus in Abrolhos is a more
significant process in the no-take outer arc reefs, as they concentrate the larger-sized
specimens that are already depleted in the coastal and unprotected reefs. Influence of this
pattern on the carbonates’ budget of the region remains as an open and interesting
research theme.
Globally, overfishing of parrotfishes is one of the most important issues in coral reef
conservation (Hughes 1994; Mumby 2006), and there are no examples of long-term
successful management experiences. Parrotfish fisheries in Abrolhos are relatively recent,
as they were not consumed before the 1980’s for being regarded as bad-tasting or toxic
by local people (author’s interviews with older fishermen). However, fishing effort has
greatly increased in recent years (Francini-Filho et al. 2008a; Freitas et al. 2011), from an
introduction as a recreational activity to an export-oriented commercial fishery, with clear
declines in open access areas and unsuccessful management stories in multiple-use
marine protected areas (Francini-Filho & Moura 2008a,b). Large specimens are now
largely restricted to enforced no-take zones and deeper reefs. Moreover, as sequential
hermaphrodites, they may be even more susceptible to overfishing, since individuals must
reach a minimum size before changing sex (Francis, 1992; Hawkins & Roberts 2003).
Although, Sc. trispinosus is IUCN red-listed as endangered category (Padovani-Ferreira et
al, 2012), it is not accounted as a threatened species by Brazilian legislation, and there are
no limitations to its exploitation (e.g. size or bag limits). The situation of Sp. amplum may
be even worse than that Sc. trispinosus (Comeros-Raynal et al. 2012), as its biomass is ten
38
times lower at the Abrolhos Bank (Francini-Filho & Moura, 2008,a,b). Despite several
socio-economic constrains, it is clear that unless a well-enforced network of no-take
marine protected areas ensures is established, coupled with unpopular and hard-toenforce maximum size limitations, the Abrolhos reefs will lose an important functional
component. In Brazilian conditions, where just few parrotfish species are able to perform
some functional roles, losing these species that are key components within the ecosystem
its critical to the coral reefs dynamics and health.
REFERENCES
Alwany MA, Thaler E & Stachowitsch M (2009) Parrotfish bioerosion on Egyptian Red Sea
reefs. J Exp Mar Biol Ecol 371:170–176.
Amado-Filho GM, Moura RL, Bastos AC, Salgado LT, Sumida PY, Guth AZ, Francini-Filho RB,
Pereira-Filho GH, Abrantes DP, Brasileiro PS, Bahia RG, Leal RN, Kaufman L, Kleypas JA,
Farina M & Thompson FL (2012) Rhodolith beds are major CaCO3 bio-factories in the
tropical south west atlantic. Plos One 7: e35171.
Bell JD, Galzin R (1984) Influence of live coral cover on coral reef fish communities. Mar
Ecol Prog Ser 15: 265–274.
Bellwood DR (1988) Ontogenetic changes in the diet of early post-settlement Scarus
species. J Fish Biol 33:213–219.
Bellwood DR & Choat, JH (1990) A functional analysis of grazing in parrotfishes (family
Scaridae): the ecological implications. Environmental Biology of Fishes 28: 189–214.
Bellwood DR (1994) A phylogenetic study of the parrotfishes, family Scaridae (Pisces:
39
Labroidei), with a revision of genera. Records of the Australian Museum Supplement 20:
1–86.
Bellwood DR (1995a) Direct estimate of bioerosion by two parrotfish species, Chlorurus
gibbus and C. sordidus, on the Great Barrier Reef, Australia. Mar Biol 121:419–429.
Bellwood DR (1995b) Carbonate transport and within-reef patterns of bioerosion and
sediment release by parrotfishes (family Scaridae) on the Great Barrier Reef. Mar Ecol
Prog Ser 117, 127–136.
Bellwood DR (1996) The Eocene fishes of Monte Bolca: the earliest coral reef fish
assemblages. Coral Reefs 15, 11–19.
Bellwood DR, Hoey AS & Choat JH (2003) Limited functional redundancy in high diversity
systems: resilience and ecosystem function on coral reefs. Ecology Letters 6: 281–285.
Bellwood DR, Hughes TP, Folke C & Nÿstrom M (2004) Confronting the coral reef crisis.
Nature 429: 827–833.
Bellwood DR, Wainwright PC, Fulton CJ & Hoey AS (2006) Functional versatility supports
coral reef biodiversity. Proc R Soc B 273, 101–107.
Bernardi G, Robertson DR, Clifton KE & Azzurro E (2000) Molecular systematics,
zoogeography, and evolutionary ecology of the Atlantic genus Sparisoma. Mol Phyl Evol
15:292–300.
Bonaldo RM, Krajewski JP, Sazima C & Sazima I (2006) Foraging activity and resource use
by three parrotfish species at Fernando de Noronha Archipelago, tropical West Atlantic.
Mar Biol 149, 423–433.
40
Bonaldo RM & Bellwood DR (2008) Size-dependent variation in the functional role of the
parrotfish Scarus rivulatus on the Great Barrier Reef, Australia. Mar Ecol Prog Ser 360:
237–244.
Bonaldo RM & Bellwood DR (2011) Parrotfish predation on massive Porites on the Great
Barrier Reef. Coral Reefs 30, 259–269.
Bonaldo RM, Hoey AS & Bellwood DR (2014) The ecosystem roles of parrotfishes on
tropical reefs. Oceanography and Marine Biology: An Annual Review 52, 81–132.
Bowen BW, Rocha LA, Toonen RJ, Karl SA, Craig MT, DiBattista JD, Eble JA, Gaither MR,
Skillings D & Bird CJ (2013) The origins of tropical marine biodiversity. Trends in Ecology
and Evolution 28(6): 359–366.
Bruckner AW, Bruckner RJ & Sollins P (2000) Parrotfish predation on live coral ‘‘spot
biting’’ and ‘‘focusing biting’’. Coral Reefs 19,50.
Bruggemann JH, Begeman J, Bosma EM, Verburg P & Breeman AM (1994) Foraging by the
stoplight parrotfish, Sparisoma viride. II. Intake and assimilation of food, protein and
energy. Mar Ecol Prog Ser 106: 57–71.
Bruggemann JH, Van Kessel AM, van Rooij JM & Breeman AM (1996) Bioerosion and
sediment ingestion by the Caribbean parrotfish Scarus vetula and Sparisoma viride:
implications of fish size, feeding mode and habitat use. Mar Ecol Prog Ser 134, 59–71.
Choat JH, Clements KD & Robbins WD (2002) The trophic status of herbivorous fishes on
coral reefs 1: dietary analysis. Mar Biol 140:613–623.
41
Comeros-Raynal MT, Choat JH, Polidoro BA, Clements KD, Abesamis R, Craig MT, Lazuardi
ME, McIlwain J, Muljadi A, Myers RF, Nañola CL, Pardede J, Rocha LA, Russell B.
Sanciangco JC, Stockwell B, Harwell H & Carpenter KE (2012) The likelihood of extinction
of iconic and dominant herbivores and detritivores of coral reefs: the parrotfishes and
surgeonfishes. PLoS One 7(7): e39825.
Creed JC & Amado Filho GM (1999) Disturbance and recovery of the macroflora of a
seagrass (Halodule wrightii Ascherson) meadow in the Abrolhos Marine National Park,
Brazil: an experimental evaluation of anchor damage. J Exp Mar Biol Ecol 235: 285–306.
Crossman DJ, Choat JH, Clements K. D., Hardy T & McConochie J (2001). Detritus as food
for grazing fishes on coral reefs. Limnology and Oceanography 46, 1596–1605.
Edmunds PJ & Carpenter RC (2001) Recovery of Diadema antil- larum reduces macroalgal
cover and increases abundance of juvenile corals on a Caribbean reef. Proceedings of the
National Academy of Sciences of the United States of America 98, 5067–5071.
Estes JA, Terborgh J, Brashares JS, Power ME & Berger J (2011) Trophic downgrading of
planet earth. Science 333:301-306.
Ferreira CEL & Gonçalves JEA (2006) Community structure and diet of roving herbivorous
reef fishes in the Abrolhos Archipelago, southwestern Atlantic. Journal of Fish Biology 69,
1533–1551.
Ferreira CEL, Peret AC & Coutinho R (1998) Seasonal grazing rates and food processing by
tropical herbivorous fishes. Journal of Fish Biology 53, 222–235
Francini-Filho RB & Moura RL (2008a) Dynamics of fish assemblages on coral reefs
subjected to different management regimes in the Abrolhos Bank, eastern Brazil. Aquatic
42
Conservation, v. 18, 1166–1179.
Francini-Filho RB & Moura RL (2008b) Evidence for spillover of reef fishes from a no-take
marine reserve: An evaluation using the before-after control-impact (BACI) approach. Fish
Research 93:346-356.
Francini-Filho RB, Moura RL, Ferreira CM & Coni EOC (2008) Live coral predation by
parrotfishes (Perciformes: Scaridae) in the Abrolhos Bank, eastern Brazil, with comments
on the classification of species into functional groups. Neotropical Ichthyology [S. I.], v. 6,
p. 191–200.
Francini-Filho RB, Ferreira CM, Coni EOC, Moura RL & Kaufman L (2010) Foraging activity
of roving herbivorous reef fish (Acanthuridae and Scaridae) in eastern Brazil: influence of
resource availability and interference competition. J Mar Biol Assoc U K 90, 481–492.
Francini-Filho RB, Coni EOC, Meirelles PM, Amado-Filho GM, Thompson FL, Pereira-Filho
GH, Bastos AC, Abrantes DP, Ferreira CM, Gibran FZ, Güth AZ, Sumida PYG, Oliveira NL,
Kaufman L, Minte-Vera CV & Moura RL (2013) Dynamics of coral reef benthic assemblages
of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers.
PLoS ONE 8:e54260.
Francis RC (1992) Sexual lability in teleosts: developmental factors. Rev Biol 67: 1–18.
Freitas MO, Moura RL, Francini-Filho RB & Minte-Vera CV (2011) Spawning patterns of
commercially important reef fish (Lutjanidae and Serranidae) in the tropical western South
Atlantic. Atlantic Scientia Marina 75: 135–146.
Gatz AJ (1979) Ecological morphology of freshwater stream fishes. Tulane Studies in
Zoology and Botany 21(2): 91–124.
43
Hammer O, Harper DAT & Ryan PD (2001) PAST version 1.39: Paleoontological statistical
software package for education and data analysis. Paleontoly Eletronica 4: 9–9.
Harvell CD, Mitchell CE, Ward JR, Sonia A, Dobson AP, Ostfeld RS, Samuel DS (2002)
Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–
2162.
Hawkins JP & Roberts CM (2003) Effects of fishing on sex-changing Caribbean parrotfishes.
Biol Conserv 115:213–226.
Horn MH (1989) Biology of marine herbivorous fishes. Oceanography and Marine Biology
Annual Review 27,167:272.
Hoey AS & Bellwood DR (2008) Cross shelf variation in the role of parrotWshes on the
Great Barrier Reef. Coral Reefs 27:37–47.
Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean
coral reef. Science 265: 1547–1551.
Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, HoeghGuldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR,
Pandolfi JM, Rosen B & Roughgarden J (2003) Climate change, human impacts and the
resilience of coral reefs (2003) Climate change, human impacts, and the resilience of coral
reefs. Science 301, 929–933.
Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh- Guldberg O, McCook L,
Moltschaniwsky N, Pratchett MS, Steneck RS & Willis B (2007) Phase shifts, herbivory, and
the resilience of coral reefs to climate change. Curr Biol 17:360–365.
44
Hunte W & Wittenberg M (1992) Effects of eutrophication and sedimentation on juvenile
corals. II. Settlement. Mar Biol 114, 625–631.
Gibran FZ (2007) Activity, habitat use, feeding behavior, and diet of four sympatric species
of Serranidae (Actinopterygii: Perciformes) in southeastern Brazil. Neotropical Ichthyology
5(3): 387-398.
Gibran FZ (2010) Habitat partitioning, habits and convergence among coastal nektonic fish
species from the São Sebastião Channel, southeastern Brazil. Neotropical Ichthyology
8(2):299–310.
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH,
Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM,
Peterson CH, Steneck RS, Tegner MJ & Warner RR (2001) Historical overfishing and the
recent collapse of coastal ecosystems. Science 293, 629–638.
Laborel J (1969) Madreporaires et hydrocorallaires récifaux des cotes Brasiliennes. Ann
Inst Océanogr. 47: 171–229.
Lokrantz J, Nyström M, Thyresson M & Johansson C (2008) The non-linear relationship
between body size and function in parrotfishes. Coral Reefs 150, 1145–1152.
Luckhurst BE & Luckhurst K (1978) Analysis of the influence of substrate variables on coral
reef fish communities. Mar Biol 49: 317–323.
McClanahan TR & Arthur R (2001) The effect of marine reserves and habitat on
populations of east African coral reef fishes. Ecological Applications 11: 559–569.
45
Minte-Vera CV, Moura RL & Francini-Filho RB (2008) Nested sampling: an improved visualcensus technique for studying reef fish assemblages. Mar Ecol Prog Ser 367: 283-293.
Motta PJ & Kotrschal KM (1992) Correlative, experimental, and comparative evolutionary
approaches in ecomorphology. Netherlands Journal of Zoology 42(2-3): 400-415.
Moura RL (2000) Brazilian reefs as priority areas for biodiversity conservation in the
Atlantic Ocean. In: International Coral. Reef Symposium, 9th, 2000, Bali, Indonésia.
Proceedings… [S. I.], v. 2, p. 917-920.
Moura RL, Figueiredo JL & Sazima I (2001) A new parrotfish (Scaridae) from Brazil, and
revalidation of Sparisoma amplum (Ranzani, 1842), Sparisoma frondosum (Agassiz, 1831),
Sparisoma axillare (Steindachner, 1878) and Scarus trispinosus (Valenciennes, 1840). Bull
Mar Sci 68:505–524.
Moura RL & Francini-Filho RB (2006) Reef and shore fishes of the Abrolhos Region, Brazil.
In: Dutra GF, Allen GR, Werner T, McKenna SA (eds) A rapid marine biodiversity
assessment of the Abrolhos Bank, Bahia, Brazil. RAP Bulletin of Biological Assessment 38,
Washington, pp 45–55.
Moura RL, Francini-Filho RB, Minte-Vera CV, Sumida PYG, Amado-Filho GM, Amaral J,
Bastos AC, Motta FS, Thompson FL, Kruger, Ricardo H & Dutra GF (2010) Pesquisa no
oceano: Desafio e oportunidades. Scientific American Brasil v. 39, p. 30–35.
Moura RL, Secchin NA, Amado-Filho GM, Francini-Filho RB, Freitas MO, Minte-Vera CV,
Teixeira JB, Thompson FL, Dutra GF, Sumida PYG, Guth AZ, Lopes RM & Bastos AC (2013)
Spatial patterns of benthic megahabitats and conservation planning in the Abrolhos Bank.
Continental Shelf Research 70: 109–117.
46
Minte-Vera CV, Moura RL & Francini-Filho RB (2008) Nested sampling: an improved visualcensus technique for studying reef fish assemblages. Mar Ecol Prog Ser 367: 283-293.
Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of
Caribbean coral reefs. Ecological Applications 16: 747–796.
Mumby PJ (2009) Herbivory versus corallivory: are parrotfish good or bad for Caribbean
coral reefs? Coral Reefs 28, 683– 690.
Nash KL, Graham NAJ, Januchowski-Hartley FA & Bellwood DR (2012) Influence of habitat
condition and competition on foraging behaviour of parrotfish. Mar Ecol Prog Ser 457:
113–124
Ong L & Holland KN (2010) Bioerosion of coral reefs by two Hawaiian parrotfishes: species,
size, differences and fishery implications. Mar Biol 157, 1313–1323.
Paddack MJ, Cowen RK & Sponaugle S (2006) Grazing pressure of herbivorous coral reef
Wshes on coral reefs. Coral Reefs 25:461–472.
Padovani-Ferreira B, Floeter S, Rocha LA, Ferreira CE, Francini-Filho RB, Moura RL, Gaspar
A. L. & Feitosa C. (2012) Scarus trispinosus. In: IUCN Red List of Threatened Species, v.
2013.2. <www.iucnredlist.org>.
Price SA, Wainwright PC, Bellwood DR, Kazancioglu E, Collar DC & Thomas JN (2010)
Functional innovations and morphological diversification in parrotfish. Evolution 64(10):
3057–3068.
Price SA, Holzman R, Near TJ & Wainwrigh PC (2011) Coral reefs promote the evolution of
morphological diversity and ecological novelty in labrid fishes. Ecology Letters 14:462–
47
469.
Robertson DR, Karg F, Moura RL, Victor BC & Bernardi G (2006) Mechanisms of speciation
and faunal enrichment in Atlantic parrotfishes. Mol Phyl Evol 40:795-807.
Steneck RS (1988) Herbivory on coral reefs: A synthesis. Proc. 6th Int. Coral Reef Symp. 1:
37–49.
Steneck RS & Dethier MN (1994) A functional group approach to the structure of algaldominated communities. Oikos 69:476–498.
Streelman JT, Alfaro M, Westneat MW, Bellwood DR & Karl SA (2002) Evolutionary history
of the parrotfishes: biogeography, ecomorphology, and comparative diversity. Evolution
56(5): 961–971.
Travis J (1982) A method for the statistical analysis of time-energy budgets. Ecology 63:1925
Van Rooij JM, Kroon FJ & Videler JJ (1996) The social and mating system of the
herbivorous reef fish Sparisoma viride: one-male versus multi-male groups. Environ Biol
Fishes 47:353-378.
Wainwright PC, Bellwood DR & Westneat MW (2002) Ecomorphology of locomotion in
labrid fishes. Environ Biol Fishes 65, 47–62.
Wilson SK, Bellwood DR, Choat JH & Furnas MJ (1988) Detritus in the epilithic algal matrix
and its use by coral reef fishes. Oceanography and Marine Biology: An Annual Review
41:279-309.
48
Winemiller KO (1991) Ecomorphological diversification in lowland freshwater fish
assemblages from five biotic regions. Ecological Monographs 61(4): 343-365.
Winemiller KO (1992) Ecomorphology of freshwater fishes. Ecological divergence and
convergence in freshwater fishes. National Geographic Research & Exploration, 8(3): 308327.
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River, New Jersey
Zemke-White WL, Choat JH & Clements KD (2002) A re-evaluation of the diel feeding
hypothesis for marine herbivorous fishes. Mar Biol 141:571–579.
49
CONCLUSÕES
Dentre os onze atributos ecomorfológicos analisados em Sc. trispinosus, Sc. zelindae e Sp.
amplum, as principais características que distinguiram os dois gêneros, bem como as duas
categorias de tamanho das três espécies, estão relacionadas à pré maxila, dentário e
configuração da boca. De uma forma geral, os indivíduos menores das três espécies
apresentaram pré-maxila e dentário significativamente mais leves, valores mais alto do
atributo configuração da boca e menor valores de configuração da cabeça do que os
indivíduos maiores. Scarus zelindae apresentou os menores valores das estruturas ósseas
do aparato bucal comparados com as duas categorias de tamanhos das duas outras
espécies. Os pesos relativos dos ossos do aparato bucal são indicativos da força de
mordida. Quanto mais pesado for o aparato mais potência ele terá e, consequentemente,
o indivíduo apresentará maior capacidade de escavação do substrato coralíneo
(BELLWOOD; CHOAT, 1990). O aparato bucal mais fraco e móvel dos menores indivíduos
das três espécies (e das duas categorias de tamanho de Sc. zelindae) indica que estes
desempenham papel de raspadores no Banco dos Abrolhos. Por outro lado, indivíduos
maiores de Sc. trispinosus e Sp. amplum possuem aparato bucal robusto, com pouca
abertura e articulações simples, capaz de penetrar o substrato coralíneo, e podem ser
considerados os principais peixes escavadores da região. Esses resultados adicionam
dados ecomorfológicos às categorizações funcionais realizadas até o presente para essas
espécies, com base em dados ecológicos alimentares (FERREIRA; GONÇALVES, 2006;
FRANCINI-FILHO et al., 2008, 2010). Além disso, os resultados revelam similaridade
ecomorfológica entre as espécies escavadoras endêmicas do Atlântico Sul e as congêneres
do Caribe e Indo Pacífico (BELLWOOD; CHOAT, 1990; BELLWOOD, 1994).
Na análise ecomorfológica ontogenética de Sc. trispinosus os atributos pré-maxila,
dentário e configuração da boca diferenciaram as seis categorias de tamanho, com
indivíduos <40 cm apresentando pré-maxila e dentário significativamente mais fracos,
além de maior abertura da boca. Além disso, na medida em que crescem, a taxa de
50
alimentação é reduzida e o volume e proporção de mordidas aumenta. As taxas de
alimentação mais altas nos indivíduos menores provavelmente estão relacionadas a
fatores como maior demanda de energia (FERREIRA et al., 1998), menor valor nutricional
das algas (FRANCINI-FILHO et al., 2008, 2010), maior tempo gasto para se alimentar e
menos tempo gasto em interações sociais (VAN ROOIJ ET AL., 1996; BONALDO et al.,
2006). A frequência de mordidas significativas aumentou em até sete vezes entre a menor
e maior categoria de tamanho, e o volume das mordidas foi até cinco vezes mais alto nos
indivíduos maiores, demonstrando aumento ontogenético na capacidade de escavação.
Esse padrão onde indivíduos menores desempenham significativamente menos impacto
para bioerosão quando comparados aos indivíduos maiores foi também encontrado para
outras espécies de budiões em diferentes localidades (BELLWOOD & CHOAT 1990;
BRUGGEMANN ET AL. 1994B; 1996; BONALDO & BELLWOOD 2008; LOKRANTZ ET AL 2008;
ONG & HOLLAND 2010). No Banco dos Abrolhos, indivíduos de Sc. trispinosus <30 cm são
predominantemente raspadores, ao passo que os indivíduos >40 cm são raspadores e
escavadores.
Os comportamentos ecológicos distintos exercidos pelos budião Sc. trispinosus, Sc.
zelindae e Sp. amplum e suas fases de crescimento evidenciam a importância que essas
espécies desempenham na dinâmica dos recifes coralíneos do Banco dos Abrolhos. A
depender da composição e da estrutura etária da comunidade, os budiões irão exercer
funções distintas e poderão contribuir diferentemente para a estruturação dos sistemas
habitados, sendo a resiliência desses recifes altamente relacionada com os budiões de
grande porte, que atuam como escavadores (BONALDO & BELLWOOD 2008; LOKRANTZ et
al 2008).
Os resultados aqui apresentados podem ser incorporados no manejo pesqueiro /
ecossistêmico de ambientes recifais, uma vez que foi reconhecido e quantificado um papel
funcional praticamente exclusivo dos indivíduos de grande porte de Sc. trispinosus em
Abrolhos, a escavação do substrato (a abundância de Sp. amplum, o único outro budião
escavador, é baixíssima em toda a região).
Scarus trispinosus é hoje um dos mais
51
importantes alvos da pesca no Banco dos Abrolhos (FRANCINI-FILHO; MOURA, 2008a,b;
FRANCINI-FILHO et al., 2008; FREITAS et al., 2011), dada a intensa diminuição das
populações de grandes carnívoros na região. A espécie é categorizada como em perigo de
extinção na Lista Vermelha da IUCN (PADOVANI-FERREIRA et al., 2012). No entanto, não é
considerado como espécie ameaçada pela legislação brasileira e não há quaisquer limites
para sua exploração (e.g. tamanho ou quantidade). Dentre as 179 espécies de budiões
analisadas pela IUCN, somente três foram incluídas em categorias de ameaça, duas como
vulneráveis e apenas Sc. trispinosus como em perigo de extinção (COMEROS-RAYNAL et
al., 2012). A situação de Sp. amplum talvez seja ainda pior, visto que sua biomassa é dez
vezes mais baixa que Sc. trispinosus (FRANCINI-FILHO & MOURA, 2008a,b). Tomadas de
decisões relacionadas aos budiões envolvem questões sociais, econômicas e culturais, e é
urgentemente necessário que políticos, gestores da pesca e demais atores envolvidos,
realizem ações que visem a persistência e manutenção dos recifes coralíneos do Banco
dos Abrolhos para manter a diversidade e os processos ecológicos da região.
REFERÊNCIAS BIBLIOGRÁFICAS
BELLWOOD, D. R.; CHOAT, J. H. A functional analysis of grazing in parrotfishes (family
Scaridae): the ecological implications. Environmental Biology of Fishes, v. 28, p. 189-214,
1990.
BELLWOOD, D. R. A phylogenetic study of the parrotfishes, family Scaridae (Pisces:
Labroidei), with a revision of genera. Records of the Australian Museum Supplement, v.
20, p. 1-86, 1994.
BELLWOOD, D. R. Direct estimate of bioerosion by two parrotfish species, Chlorurus
gibbus and C. sordidus, on the Great Barrier Reef, Australia. Mar Biol, v. 121, p. 419–429,
52
1995a.
BELLWOOD, D. R. Carbonate transport and within-reef patterns of bioerosion and
sediment release by parrotfishes (family Scaridae) on the Great Barrier Reef. Mar. Ecol.
Prog. Ser., v. 117, p. 127–136, 1995b.
BELLWOOD, D.R. Production and reworking of sediment by parrotfishes (family Scaridae)
on the Great Barrier Reef, Australia. Mar Biol 125, 795–800. 1996.
BELLWOOD, D. R.; HOEY, A. S.; CHOAT, J. H. Limited functional redundancy in high
diversity systems: resilience and ecosystem function on coral reefs. Ecology Letters, v. 6,
p. 281-285, 2003.
BELLWOOD, D. R. et al. Confronting the coral reef crisis. Nature, v. 429, p. 827-833, 2004.
BONALDO, R.M. et al. Foraging activity and resource use by three parrotfish species at
Fernando de Noronha Archipelago, tropical West Atlantic. Mar Biol, v. 149, p. 423–433,
2006.
BONALDO, R. M.; BELLWOOD, D. R. Size-dependent variation in the functional role of the
parrotfish Scarus rivulatus on the Great Barrier Reef, Australia. Marine Ecology Progress
Series, v. 360, p. 237–244, 2008.
BONALDO, R. M.; HOEY, A. S.; BELLWOOD, D. R. The ecosystem roles of parrotfishes on
tropical reefs. Oceanography and Mar Biol: An Annual Review, 52, 81-132. 2014
BRUGGEMANN, J.H.; VAN ROOIJ, J.; VIDELER, J.; & BREEMAN, A. Dynamics and limitations
of herbivore populations on a Caribbean coral reef. In Parrotfish grazing on coral reefs: a
trophic novelty. PhD thesis, University of Groningen, the Netherlands, 153–178. 1995.
53
BRUGGEMANN, J. H.; VAN OPPEN, M. J. H.; BREEMAN, A. M. Foraging by the stoplight
parrotfish, Sparisoma viride. 1. Food selection in different, socially determined habitats.
Marine Ecology Progress Series, v. 106, p. 41-55, 1994a.
BRUGGEMANN, J. H. et al. Foraging by the stoplight parrotfish, Sparisoma viride. II. Intake
and assimilation of food, protein and energy. Marine Ecology Progress Series, v. 106, p.
57-71, 1994b.
BRUGGEMANN, J. H. et al. Bioerosion and sediment ingestion by the Caribbean parrotfish
Scarus vetula and Sparisoma viride: implications of fish size, feeding mode and habitat
use. Marine Ecology Progress Series, v. 134, p. 59–71, 1996.
CHOAT, J. H.; ROBERTSON, D. R. Protogynous hermaphroditism in fishes of the family
Scaridae. In: RHEINBOTH, R. (ed) Intersexuality in the animal kingdom. Springer Verlag,
Heidelberg, p. 263-283, 1975.
CHOAT, J. H. The biology of herbivorous fishes on coral reefs. In: SALE P. F. (ed) The
ecology of fishes on coral reefs. Academic Press, p. 120-155, 1991.
CLEMENTS, K. D. et al. RelationshSs of the temperate Australasian labrid fish tribe Odacini
(Perciformes; Teleostei). Molecular Phylogenetics and Evolution, v. 32, p. 575–587, 2004.
COMEROS-RAYNAL, M.T. et al. The likelihood of extinction of iconic and dominant
components of coral reefs: the parrotfishes and surgeonfishes. PLoS ONE v. 7, p. 6, 2012.
COWMAN, P.F., et. al. Dating the evolutionary origins of the wrasses (Labridae) and the
rise of trophic novelty on coral reefs. Molecular Phylogenetics and Evolution, v. 52, p.
621–631, 2009.
54
CROSSMAN, D. J. et al. Detritus as food for grazing fishes on coral reefs. Limnology and
Oceanography, v. 46, p. 1596–1605, 2001.
FLOETER S. R.; HALPERN B. S.; FERREIRA C. E. L. Effects of fishing and protection on
Brazilian reef fishes. Biol Conserv, v. 128, p. 391–402, 2006.
FERREIRA, C. E. L.; GONÇALVES, J. E. A. Community structure and diet of roving
herbivorous reef fishes in the Abrolhos Archipelago, southwestern Atlantic. Journal of Fish
Biology, v. 69, p. 1533–1551, 2006.
FERREIRA, C. E. L.; PERET, A. C.; COUTINHO, R. Seasonal grazing rates and food processing
by tropical herbivorous fishes. Journal of Fish Biology, v. 53, p. 222–235, 1998.
FRANCINI-FILHO, R. B.; MOURA, R. L. Dynamics of fish assemblages on coral reefs
subjected to different management regimes in the Abrolhos Bank, eastern Brazil. Aquatic
Conservation, v. 18, p. 1166-1179, 2008a.
FRANCINI-FILHO R. B.; MOURA R. L. Evidence for spillover of reef fishes from a no-take
marine reserve: An evaluation using the before-after control-impact (BACI) approach. Fish
Res, v. 93, p. 346-356, 2008b.
FRANCINI-FILHO, R. B. et al. Live coral predation by parrotfishes (Perciformes: Scaridae) in
the Abrolhos Bank, eastern Brazil, with comments on the classification of species into
functional groups. Neotropical Ichthyology, v. 6, p. 191-200, 2008.
FRANCINI- FILHO, R. B. et al. Foraging activity of roving herbivorous reef fish (Acanthuridae
and Scaridae) in eastern Brazil: influence of resource availability and interference
competition. Journal of the Marine Biological Association of the United Kingdom, v. 90,
55
p. 481–492, 2010.
FREITAS, M. O. et al. Spawning patterns of commercially important reef fish (Lutjanidae
and Serranidae ) in the tropical western South Atlantic. Atlantic. Scientia Marina, v. 75, n.
135-146, 2011.
HAWKINS, J. P.; ROBERTS, C. M. Effects of fishing on sex-changing Caribbean parrotfishes.
Biol Conserv, v. 115, n. 213–226, 2003.
HUGHES, T. P. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral
reef. Science, v. 265, n. 1547–1551, 1994.
HUGHES, T. P. et al. Climate change, human impacts, and the resilience of coral reefs.
Science, v. 301, p. 929–933, 2003.
HUGHES, T. P. et al. New paradigms for supporting the resilience of marine ecosystems.
Trends in Ecology and Evolution, v. 20, p. 380–386, 2005.
HOEGH-GULDBERG, O. et al. Coral reefs under rapid climate change and ocean
acidification. Science, v. 318, n. 1737–1742, 2007.
HUMANN, P.; DELOACH, N. Reef fish identification: Florida, Caribbean and Bahamas.
New World Publications, Jacksonville, 2002.
GATZ, A. J. Ecological morphology of freshwater stream fishes. Tulane Studies in Zoology
and Botany, v. 21, n. 2, p. 91-124, 1979.
GIBRAN, F. Z. Activity, habitat use, feeding behavior, and diet of four sympatric species of
Serranidae (Actinopterygii: Perciformes) in southeastern Brazil. Neotropical Ichthyology,
56
v. 5, n. 3, p. 387-398, 2007.
GIBRAN, F. Z. Habitat partitioning, habits and convergence among coastal nektonic fish
species from the São Sebastião Channel, southeastern Brazil. Neotropical Ichthyology, v.
8, n. 2, p. 299-310, 2010.
LEWIS, S.M. The role of herbivorous fishes in the organization of a Caribbean reef
community. Ecological Monographs, v. 56, p. 183–200, 1986.
LETOURNEUR, Y. Dynamics of fish communities on Reunion fringing reefs, Indian Ocean. I.
Patterns of spatial distribution. Journal of Experimental Marine Biology and Ecology, v.
195, p. 1-30, 1996.
LOKRANTZ, J. et al. The non-linear relationship between body size and function in
parrotfishes. Coral Reefs, v. 150, p. 1145–1152, 2008.
MOTTA, P. J.; KOTRSCHAL, K. M. Correlative, experimental, and comparative evolutionary
approaches in ecomorphology. Netherlands Journal of Zoology, v. 42, n. 2-3, p. 400-415,
1992.
MOTTA, P. J.; NORTON, S. F.; LUCZKOVICH, J. J. Perspectives on the ecomorphology of
bony fishes. Environmental Biology of Fishes, v. 44, n. 1-3, 11-20, 1995.
MOURA, R. L. Brazilian reefs as priority areas for biodiversity conservation in the Atlantic
Ocean. In: International Coral Reef Symposium, 9th, 2000, Bali, Indonésia. Proceedings…
v. 2, p. 917-920, 2000.
MOURA, R. L. Brazilian reefs as priority areas for biodiversity conservation in the Atlantic
Ocean. Proc. Int. Coral Reef Symp., v. 9, n. 2, p. 917-920, 2002.
57
MOURA, R. L.; FRANCINI-FILHO, R. B.; MINTE-VERA, C. V.; SUMIDA, P.Y.G., AMADO-FILHO,
G. M.; AMARAL, J.; BASTOS, A. C.; MOTTA, F. S.; THOMPSON, F. L.; KRUGER; RICARDO H.;
DUTRA, G. F.; Pesquisa no oceano: Desafio e oportunidades. Scientific American Brasil, v.
39, p. 30-35. 2010.
ONG, L.; HOLLAND, K. N. Bioerosion of coral reefs by two Hawaiian parrotfishes: species,
size, differences and fishery implications. Marine Biology, v. 157, p. 1313–1323, 2010.
PADOVANI-FERREIRA, B.; FLOETER, S.; ROCHA, L.A.; FERREIRA, C.E.; FRANCINI-FILHO, R.B.;
MOURA, R.L.; GASPAR, A. L. & FEITOSA, C. (2012) Scarus trispinosus. In: IUCN Red List of
Threatened Species, v. 2013.2. <www.iucnredlist.org>.
PARENTI P.; RANDALL J. E. Checklist of the species of the families Labridae and Scaridae:
an update. Smithiana Bulletin, v. 13, p. 29–44, 2011.
RANDALL, J. E.; ALLEN, G. R.; STEENE, R. C. Fishes of the Great Barrier Reef and and Coral
Sea. Honolulu, University of Hawaii Press, 1997.
SHIN, Y-J. et al. Using size-based indicators to evaluate the ecosystem effect of fishing.
ICES J. Mar Sci, v. 62, p. 384-396, 2005.
SCHMITT, R. J.; COYER, J. A. The foraging ecology of sympatric marine fish in the genus
Embiotoca (Embiotocidae): importance of foraging behavior in prey size selection.
Oecologia, v. 55, p. 369-378, 1982.
SCHOENER, T. W. Resource partitioning in ecological communities. Science, v. 185, p. 2739, 1974.
58
STREELMAN, J. T. et al. Evolutionary history of the parrotfishes: biogeography,
ecomorphology and comparative diversity. Evolution, v. 56, n. 5, p. 961-971, 2002.
VAN ROOIJ, J. M.; KROON, F. J.; VIDELER, J. J. The social and mating system of the
herbivorous reef fish Sparisoma viride: one-male versus multi-male groups. Environ Biol
Fishes, v. 47, p. 353-378, 1996.
WESTNEAT, M. W.; ALFARO, M. E. Phylogenetic relationships and evolutionary history of
the reef fish family Labridae. Molecular Phylogenetics and Evolution, v. 36, p. 370–390,
2005.
WILSON, S. K. et al. Detritus in the epilithic algal matrix and its use by coral reef fishes.
Oceanography and Marine Biology: An Annual Review, v. 41, p. 279-309, 2003.
WINEMILLER, K. O. Ecomorphological diversification in lowland freshwater fish
assemblages from five biotic regions. Ecological Monographs, v. 61, n. 4, p. 343-365,
1991.

Ecomorfologia, performance alimentar e bioerosão de budiões da

Transcrição

Documentos relacionados

Spatial distribution of benthic macroorganisms on reef flats at Porto

From Critical to Carbon Neutral, Grassroots Sustainable Urban

tourism impact on reef flats in porto de galinhas beach, pernambuco

Abiotic variables and human activities on the reef flats of Porto de

Doc 1985 - Céu Aberto

Accomodation File

Ecological speciation in tropical reef fishes

BENTHIC MARINE ALGAE OF THE CORAL REEFS OF BRAZIL: A

Oporto - Mimoa

Brazil drops Rafinha and Ederson over Injury

Crossing the Luzon Strait - National Museum of Prehistory