como a variação espacial das assembleias de peixes...
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UNIVERSIDADE FEDERAL DO ABC
Curso de Pós-Graduação em Evolução e Diversidade
Dissertação de Mestrado
Gabriela Pastro
Como a variação espacial das assembleias de peixes determina a
pressão de predação sobre as comunidades incrustantes?
Santo André
2015
ii
UNIVERSIDADE FEDERAL DO ABC
Curso de Pós-Graduação em Evolução e Diversidade
Dissertação de Mestrado
Gabriela Pastro
Como a variação espacial das assembleias de peixes determina a
pressão de predação sobre as comunidades incrustantes?
Trabalho apresentado como requisito parcial
para obtenção do título de Mestre em
Evolução e Diversidade, sob orientação do Professor Doutor
Fernando Zaniolo Gibran e coorientação do
Professor Doutor Gustavo Muniz Diaz.
Santo André
2015
iii
iv
Este exemplar foi revisado e alterado em relação à versão original, de acordo com as
observações levantadas pela banca no dia da defesa, sob responsabilidade única do autor
e com a anuência de seu orientador.
Santo André, ____de _______________ de 20___.
Assinatura do autor: _____________________________________
Assinatura do orientador: _________________________________
Assinatura do coorientador: ___________________________________
v
AGRADECIMENTOS
Ao Prof. Dr. Fernando Zaniolo Gibran pela orientação, conselhos e parceria nos últimos
cinco anos e ao Prof. Dr. Gustavo Muniz Dias que acrescentou ao grupo sua sabedoria e
experiência.
À Universidade Federal do ABC e à Capes pelas bolsas de Mestrado concedidas e ao
Programa de Pós-Graduação em Evolução e Diversidade.
À FAPESP pelo Auxílio à Pesquisa concedido para execução do projeto “Como
diferenças nas condições ambientais em microescala afetam o recrutamento e a
predação sobre a comunidade incrustante e a aptidão e do briozoário Schizoporella
errata?” (2013/11286-2), sob a responsabilidade do coorientador deste trabalho, Prof.
Dr. Gustavo M. Dias – esta dissertação é um dos produtos deste projeto, e os recursos
financeiros e equipamentos foram cruciais para sua realização.
A todo o pessoal do Laboratório de Evolução e Diversidade I da UFABC,
especialmente Felipe Dutra, Felipe T. Oricchio, Karina Kitasawa e Mariane Tavares,
pois sem vocês este projeto não teria sido realizado com tanto sucesso, obrigada.
Ao Yacht Club de Ilhabela (YCI) pelo acolhimento, apoio logístico e incentivo à
pesquisa. Um agradecimento especial ao Júlio Cardoso, Diretor Ambiental, pelo seu
entusiasmo e incentivo à pesquisa na área da marina.
Ao Centro de Biologia Marinha da Universidade de São Paulo (CEBIMar-USP) por
todo o suporte durante as atividades de campo, em especial aos técnicos Alex W. A.
Monteiro, Eduardo Honuma, Joseilto M. de Oliveira e Elso A. da Silva.
Em especial, à minha família que me apoiou durante todo este período, ao Iles pela
paciência e compreensão em todas minhas ausências, devido ao intenso trabalho de
campo. À minha mãe, Heloisa, e minha irmã, Marina, por acreditarem e me apoiarem, e
a todos meu familiares e amigos que, de perto ou de longe, me apoiaram.
vi
“A coisa mais indispensável a um homem é reconhecer o uso que deve fazer do seu
próprio conhecimento.” Platão
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CONTEÚDO
Resumo 02
Abstract 05
Introdução Geral 06
Referências Bibliográficas 09
Capítulo 1: Fish assemblages associated to a man-made habitat in
Southwestern Atlantic
1. Abstract 13
2. Introduction 14
3. Material and Methods 16
4. Results 19
5. Discussion 28
References 31
Capítulo 2: How marina facilities affect the role of fish predation on early-life
stages of benthic organisms?
1. Abstract 35
2. Introduction 36
3. Material and Methods 38
4. Results 41
5. Discussion 51
References 54
Considerações Finais 58
2
RESUMO
Construções antrópicas podem aumentar a disponibilidade de substrato consolidado, o
que normalmente resulta no desenvolvimento de comunidades incrustantes
diversificadas. Aliada às alterações no hidrodinamismo local, provocadas por quebra-
mares ou molhes, essa nova disponibilidade de recursos espaciais, alimentares e
refúgios pode resultar também em assembleias de consumidores abundantes e
diversificados. Entretanto, este efeito positivo é dependente da intensidade de outros
impactos que normalmente estão associados à submersão dessas estruturas (e.g.
aumento da sedimentação e de poluentes). Um dos principais processos que estruturam
as comunidades de organismos incrustantes é a predação exercida por peixes
actinopterígios de diferentes estágios pós-larvais, podendo causar variações em micro-
escala (i.e. metros), não necessariamente notáveis em escalas maiores (i.e. quilômetros).
Desta forma, a predação pode ser responsável por certa variação temporal e espacial na
estruturação e composição das comunidades recifais. Neste contexto, os objetivos deste
estudo foram caracterizar quali e quantitativamente, e temporalmente, por meio de
censos visuais subaquáticos, a ictiofauna de duas áreas próximas (130 m) em um
mesmo ambiente recifal artificial do Yacht Club de Ilhabela (Canal de São Sebastião,
São Paulo, Brasil) (Capítulo 1), além de investigar, por meio de observações, registros
em vídeos e experimentação in situ, o papel da predação por estes peixes sobre as
comunidades locais incrustantes (Capítulo 2). Diferenças em relação às assembleias de
peixes entre as áreas estudadas foram evidenciadas nas estações quentes e úmidas
(verão e primavera), quando a área abrigada apresentou maior riqueza e abundância. A
área do quebra-mar foi caracterizada pela intensa presença do herbívoro territorialista
Scartella cristata, enquanto a área dentro da marina apresentou dominância de
cardumes de Harengula jaguana e do onívoro generalista Diplodus argenteus. Ao se
avaliar a frequência alimentar das espécies foi registrado um pico de atividade no
período das 12h00-14h00 na área de dentro da marina, o qual pode ter relação direta
com a luminosidade. Cinco espécies de peixes recifais foram registradas predando a
comunidade incrustante estabelecidas em placas de PVC, sendo que D. argenteus foi a
que exerceu maior pressão de predação, atribuindo-se a esta espécie 94% das 1.6652
mordidas registradas. A área do quebra-mar apresentou maior pressão de predação, com
maior número de registros de predação e de mordidas na comunidade incrustante. Os
principais itens alimentares predados foram ascídias (especialmente dideminídeos),
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serpulídios e briozoários arborescentes em ambas as áreas. Este estudo monstra que
diferentes áreas podem responder de forma contrastante a um distúrbio ambiental, além
de apresentar estruturas de comunidade variáveis no tempo e espaço. Diferenças em
micro-escala nas condições ambientais, como as causadas pela construção de marinas,
podem afetar a predação por peixes sobre a comunidade incrustante e assim modular
sua estrutura, porém isto também pode ser relacionado à disponibilidade de alimento
(presas).
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ABSTRACT
Anthropic constructions can increase the availability of consolidated substrate, which
usually results in the development of diverse incrusting community. Coupled with local
hydrodynamics changes, caused by breakwaters or jetties, this new availability of
shelter, food and space resources can also result in abundant and diverse consumer
assemblages. However, this positive effect is highly dependent on the intensity of other
impacts that are usually associated to the submersion of coastal structures (e.g.
sedimentation and pollution). One of the main processes that structure the communities
of incrusting organisms is predation exerted by Actinopterygii fishes of different post-
larval stages, what may cause variations in micro-scale (i.e. meters), not necessarily
recorded at larger scales (i.e. kilometers). Thus, predation may be responsible for certain
temporal and spatial variation in the structure and composition of reef communities,
especially when it occurs on the recruits of the species with the highest representation in
the larval plankton (higher potential for recruitment) before the interactions of
competition post-settlement entered in progress. In this context, the objectives of this
study were characterize qualitatively and quantitatively, and temporally, fish
populations in two nearby areas (130 m) in the same artificial reef environment
(Chapter 1), and investigate the role of predation by these fishes on local incrusting
communities (Yacht Club de Ilhabela, São Sebastião Channel, São Paulo, Brazil)
(Chapter 2). Differences from the abundance and richness of fishes between the studied
areas were observed in the hot and wet seasons (spring and summer), when the area
inside the marina showed higher richness and abundance than breakwater. The area of
breakwater was characterized by intense presence of territorial herbivore Scartella
cristata, while the area inside the marina presented dominance by schools of Harengula
jaguana and generalist species Diplodus argenteus. When assessing the food frequency,
I recorded a peak of activity during 12h00-14h00. Five reef fish species were recorded
preying on the incrusting community, and D. argenteus exerted the highest predation
pressure, accounting for 94% of the 16,652 registered bites. The area of the breakwater
showed higher predation pressure, but had lower richness of predators. The main food
items preyed were ascidians (especially didemnids), serpulids and arborescent
bryozoans, varying according to the area. The data showed that different areas may
respond differently in relation to an environmental disturbance, with community
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structures varying in time and space. Differences in micro-scale environmental
conditions, such as those caused by the construction of marinas, can affect predation by
fish and so modulate the structure of in the incrusting community, but it may also be
related to the availability of food (prey items).
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INTRODUÇÃO GERAL
Um dos objetivos dos estudos em Ecologia é entender os padrões de distribuição dos
organismos com relação aos hábitats disponíveis e ao tempo (Anderson & Millar 2004),
os quais podem ser influenciados por vários fatores físico-químicos como, por exemplo,
a temperatura, luz, produtividade, oxigênio e nutrientes disponíveis. Além dos fatores
físicos, há importantes fatores bióticos atuando na sobrevivência e permanência dos
organismos nos hábitats, tais como interações biológicas como competição e predação.
Sabendo que fatores bióticos e abióticos podem variar mais ou menos de acordo com as
escalas espaciais consideradas (e.g. Olff & Ritchie 1998, Wyatt & Silman 2004, Creel
& Winnie 2005), reconhecer quais processos operam em micro-escalas é fundamental
para compreender a dinâmica das populações e comunidades e com isso minimizar os
impactos das atividades antrópicas sobre as comunidades e os ecossistemas.
A predação é um dos principais processos que estruturam as comunidades (Steele
1996) e, em sistemas marinhos, peixes de diferentes estágios pós-larvais (jovens e
adultos) são considerados um dos principais predadores, especialmente em substrato
biogênico ou recifal, habitados por organismos incrustantes coloniais ou solitários
(Choat 1982, Hixon 1997, Connel & Anderson 1999). A presença de substratos
biogênicos em ambientes bentônicos é responsável por aumentar a diversidade local, o
que resulta em maior disponibilidade de micro-habitats e recursos que podem ser
utilizados por diversos organismos (efeito bottom-up), como por assembleias de peixes
(Sebens 1991, Thompson et al. 1996, Morgado & Tanaka 2001), sendo que a presença
destes organismos estabelecidos no substrato consolidado também está suscetível aos
efeitos causados pelos níveis trópicos superiores, como predação por peixes invertívoros
(efeito top-down). Desta forma, a predação por peixes pode ser responsável por certa
variação temporal e espacial na estrutura e composição das comunidades recifais (e.g.
Kingsford 1992, Connel & Kingsford 1998). Distúrbios causados por animais
herbívoros têm sido amplamente estudados em sistemas marinhos bentônicos (Calderon
2008; e.g. Choat & Andrew 1986, McClanahan et al. 1999, Smith et al. 2001,
McClanahan et al. 2001), porém o efeito da predação por carnívoros e invertívoros
sobre a comunidade incrustante tem recebido pouca atenção (Hunt & Scheibling 1997),
assim como são escassos estudos comportamentais destes grupos (Krajewski et al.
2011). Como a predação por peixes pode controlar o recrutamento e/ou a sobrevivência
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de diversos organismos bentônicos podemos afirmar que ela pode desempenhar um
papel-chave na organização das comunidades recifais.
Os ambientes recifais brasileiros fazem parte do sistema de recifes do Atlântico
Tropical e apresentam algumas características únicas (Ferreira et al. 2004). Variações na
geografia da costa brasileira, principalmente decorrentes da existência de diferentes
tipos de susbtrato (e.g. recifes de corais, costões rochosos e bancos de algas calcárias),
resultam em diferentes assembleais de peixes (Floeter et al. 2001). Ambientes recifais
da costa Sudeste apresentam um pico de diversidade de peixes das famílias Serranidae e
Labridae, sendo que regiões mais ao sul apresentam um empobrecimento gradual da
fauna, o que é observado entre a costa de São Paulo e Santa Catarina (Evans et al. 1985,
Stramma 1989, Floeter et al. 2001). As regiões Sul e Sudeste do Brasil são desprovidas
de recifes de corais, mas são caracterizadas pela presença de inúmeros ambientes
recifais rochosos, como ilhas, lajes e parcéis, além de, principalmente, costões rochosos
formados por rochas ígneas e metamórficas (Rabelo 2007, Gibran & Moura 2012).
Além destes ambientes recifais naturais há uma série de construções antrópicas que
servem de substrato consolidado, sujeitos as mesmas condições e dinâmicas ambientais
dos ambientes recifais naturais (Mineur et al. 2012).
A ocupação de regiões costeiras promove alterações na estrutura dos ecossistemas
marinhos. O aumento da poluição orgânica e inorgânica, aliado à construção de
estruturas como marinas, píeres, molhes e portos promovem alterações nas condições
ambientais, afetando a distribuição dos organismos e a organização das comunidades e
teias tróficas (i.e. Dugan et al. 2011). Tais construções geralmente aumentam a
disponibilidade de substrato consolidado, o que normalmente resulta no
desenvolvimento de comunidades incrustantes diversificadas. Aliada a reduzida
turbulência provocada por quebra-mares ou molhes, esta nova disponibilidade de
recursos espaciais, alimentares e refúgios podem resultar também em assembleias de
consumidores abundantes e diversificados. Construções antrópicas no ambiente marinho
funcionam, portanto, como recifes artificiais (e.g. Chandler et al. 1985, Rooker et al.
1997, Hackradt & Félix-Hackradt 2009). Entretanto, seu efeito positivo sob os
organismos recifais é dependente da intensidade de outros impactos que normalmente
estão associados à submersão de estruturas costeiras (e.g. sedimentação). Em locais
onde tais estruturas estão associadas a um contexto de poluição e pesca exploratória,
marinas e portos podem funcionar de forma negativa, restringindo a ocorrência de
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espécies nativas e muitas vezes facilitando a introdução de espécies exóticas, além das
alterações evidentes na circulação da água e suas consequências locais, como perda de
habitats devido à sedimentação (e.g. Freitas et al. 2009).
Dentre os organismos mais afetados por tais construções estão os organismos
incrustantes e os peixes actinopterígios, cujas assembleias podem variar
significativamente em micro-escala (i.e. metros), diferentemente de quando
consideramos escalas maiores (i.e. quilômetros). Em micro-escala, o hidrodinamismo, o
oxigênio dissolvido, a luminosidade, a composição do plâncton, a produtividade
primária e a disponibilidade e o tipo de substrato podem modular a distribuição desses
organismos (e.g. McGehee 1994, Bellwood & Wainwrogth 2001). Desta forma,
alterações nas condições físico-químicas na costa têm o potencial de afetar a
distribuição, composição, abundância e riqueza dos chamados organismos recifais.
Nos substratos duros, artificiais e naturais, organismos como corais, algas calcárias,
esponjas, ascídias, briozoários e poliquetas, por exemplo, podem assentar e
desenvolver-se em colônias rígidas de estruturas complexas e tridimensionais, o que
aumenta a disponibilidade de alimentos e recursos espaciais no infralitoral e permite a
sucessão ecológica e colonização destes lugares por organismos com mais exigências
ambientais, como peixes e outros vertebrados (Gore et al. 1978, Bradstock & Gordon
1983, Lewis & Snelgrove 1990, Safriel & Bem-Eliahu 1991, Nalesso et al. 1995, Cocito
et al. 2000, Morgado & Tanaka 2001). Ascídias e briozoários são os mais frequentes
organismos da fauna recifal bentônica e costeira do infralitoral, embora ainda
relativamente pouco estudados quando comparados a esponjas, cnidários, crustáceos e
moluscos (McKinney & Jackson 1989, Reed 1991, Migoto 2000, Calderon 2008). Estes
animais têm ampla distribuição espacial e, muitas vezes, dominam locais protegidos,
tanto em substratos naturais como artificiais. Além de lidarem com a competição pelo
espaço, estes organismos incrustantes também estão sujeitos a uma forte pressão por
predadores móveis, principalmente quando recrutas/recém-assentados.
O Yacht Club de Ilhabela (YCI) está localizado no Sudeste da costa brasileira,
região caracterizada pela ocorrência de inúmeros ambientes recifais rochosos e diversas
construções antrópicas. Diferentemente de muitas marinas recreativas, o YCI possui um
rigoroso controle das perturbações causadas pelos seus barcos e frequentadores, pois há
proibição de despejo de dejetos, do uso de produtos não biodegradáveis e da pesca de
arpão e rede. A marina do YCI é formada por plataformas flutuantes de concreto e
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isopor, criadas em 2011, as quais funcionam como recifes artificiais. Características
mais similares a ambientes naturais de costões rochosos são encontradas nas áreas
externas da marina, na presença do quebra-mar, com exposição às ondas, maior
visibilidade e menor impacto antrópico; já as áreas internas apresentam águas mais
calmas, com maior acúmulo de matéria orgânica e sedimentação e, consequentemente,
menor luminosidade e maior turbidez, mostrando-se com condições ambientais mais
similares a pequenas baías costeiras. As áreas internas apresentam também intensa
presença de barcos e maior potencial de poluição orgânica e inorgânica. Neste contexto,
os objetivos deste estudo foram caracterizar quali e quantitativamente, e temporalmente,
a ictiofauna de duas localidades em duas áreas recifais artificiais do Yacht Club de
Ilhabela distantes apenas 130 m (Capítulo 1), as quais estão submetidas a condições
ambientais distintas, além de investigar o papel da predação por estes peixes sobre as
comunidades incrustantes locais (Capítulo 2). Trabalhei com as seguintes hipóteses:
duas áreas recifais próximas, porém com condições ambientais distintas, apresentam
assembleias de peixes com estrutura trófica distinta, as quais variam temporalmente, e
tais diferenças resultam em pressões de predação também distintas sobre os organismos
incrustantes, alterando sua composição, riqueza e abundância.
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13
CAPÍTULO 1
FISH ASSEMBLAGES ASSOCIATED TO A MAN-MADE HABITAT IN
SOUTHWESTERN ATLANTIC
ABSTRACT
The occupation of the coastal region has promoted major changes in the structure of
marine ecosystems. Marine constructions cause modifications on several physical
factors, by increasing sedimentation, organic and inorganic pollution, but can also
increase the availability of hard substrata. This new habitat available usually results in
the development of a diverse sessile community which can also support a rich reef fish
fauna. In micro-scale, local conditions as action of waves, phytoplankton, light and
habitat complexity, which are directly affected by the construction of marinas, harbors
and piers, can modulate the distribution of fish assemblages. In this context, using a
visual census technique, I compared quali-quantitatively, and temporally, the fish
assemblages between two close areas (130 m of distance) exposed to distinct
environmental conditions: the area inside the marina (protected from waves) and the
breakwater (exposed to waves) of the Yacht Club de Ilhabela. More than 3,350 fish
individuals, from 19 species and 13 families (Actinopterygii), were recorded in the
studied areas. The area inside the marina presented a more abundant and rich
assemblage than the breakwater, during the hot/wet (summer and spring). The reef fish
assemblage from the breakwater was characterized by a higher abundance of the
territorial herbivore Scartella cristata, while the area inside the marina was dominated
by schools of Harengula jaguana and generalist omnivore species as Abudefduf
saxatilis and Diplodus argenteus. These results indicate that such man-made habitat
results in significant structural modifications on local fish assemblages that can be
perceived in micro-scale. The structure of an assemblage is susceptible to spatial and
temporal variations due to fluctuations in environmental factors (mainly hydrodynamics
and turbidity) and biological (mainly predation and competition).
Keywords: artificial reef, reef fishes, visual censuses, Scartella cristata, Diplodus
argenteus, São Sebastião Channel.
14
INTRODUCTION
In micro-scale, action of waves, depth, temperature, phytoplankton and habitat
complexity can modulate the distribution of fish assemblages (i.e. Ferreira et al. 2001;
Floeter et al. 2007, Pinheiro et al. 2013). Substratum composition is another variable
capable of influencing fish distribution (Jones & Syms 1998, Valdés-Münoz &
Mockeck 2001, Floeter et al 2007, Sabater & Tofaeono 2007). Finally, these structures
may also influence by abundance of their prey (Hobson & Chess 1978, 1986, Bouchon-
Navarro & Bouchoun 1989, Jennings et al. 1996, Floeter et al. 2007) and potential
competitors (Jones 1987, 1988, Robertson 1996, Krajewski & Floeter 2011). As biotic
and abiotic factors are not fixed in each area, the structure of assemblages may suffer
temporal variations (e.g. Choat et al. 1988, Cunha et al. 2007).
The structure of the reef communities is susceptible to environmental changes, such
as through marine constructions. Organic and inorganic pollution combined with the
construction of solid structures, such as marinas, jetties, piers and ports, promote several
changes in environmental conditions which, directly or indirectly, affect the distribution
of organisms and the organization of communities and trophic webs. These man-made
constructions bring with them a range of sedimentological and geomorphological
problems (Freitas et al. 2009), but can be increase the availability of hard substratum,
which usually results in the development of a diverse incrusting organism fauna that can
support rich consumer assemblages. So, anthropic construction in the marine
environment may act as artificial reefs. However, the positive effect under the reef
organisms is highly dependent on the intensity of other impacts that are due to the
submersion of such structures, as sedimentation. On the other hand, these structures can
increase fishing results, boosting the potential for exploitation and increasing the
probability of overexploitation (Grossman et al. 1997), besides increase pollution with
oil from boats and local nutrient enrichment from organic matter waste besides
pollution as oil from boats, and nutrient enrichment (e.g. Rivero et al. 2013). Among the
group of organisms most affected by man-made structures are the incrusting organisms
and bone fishes, which can vary widely in community structure considering micro-scale
(i.e. meters) (e.g. Krajewski & Floeter 2011, Vieira et al. 2012, Anderson & Millar
2014, Oricchio 2015).
15
Artificial structures may also provide shelter and nursery sites for fishes, frequently
increasing local densities (Coleman & Connell 2001, Rivero et al. 2013). On the other
hand, these artificial structures often facilitate the introduction of exotic species, which
can exclude native ones by competitive exclusion – many studies documented
extinctions of long-term resident species caused by the introduction of predators or
pathogens (King 1984, Gill & Martinson 1991, Kaufman 1992, Fritts & Rodda 1998,
Loope 1999, Davis 2003). Pimentel et al. (2005) studied the effects of alien-species in
diverse groups, including fishes, and concluded that about 42% of the species on the
species lists risk are vulnerable primarily because of alien-invasive species.
Changes in fish assemblages caused by human actions or natural cases can result in
changes in communities at lower trophic levels, as incrusting communities, through top-
down control. Biodiversity is predicted to be greatest at intermediate levels of stress or
disturbance, because at low levels of disturbance (or low environmental stress or
predation), communities are monopolized by a single competitive dominant species,
while where stresses are intense, only few species are tolerant enough to persist
(Stachowicz 2001). This impact alters the dynamics of the fish assemblages, which may
give advantage to a single fish species, through competition and predation, making this
the dominant species. These changes may also result in local extinction of one or more
species (prey or fish competitor). Therefore, fishes have the potential to increase the
resistance of incrusting communities to bioinvasions (Stachowicz 2001), according to
the modulation of structure of biogenic substrate.
Southeastern coast of Brazil is formed predominantly by rocky shores, what
represents the main habitat for reef fishes (Floeter et al. 2001, Gibran & Moura 2012).
However, artificial substrata promote a supply of space for local reef assemblages,
through the settlement and development of larvae of incrusting organisms and
emergence of rich substrate biogenic. The Yacht Club de Ilhabela (YCI) is an example
of this, a marina formed by floating platforms (created in 2011), located inside the São
Sebastião Channel (Southeastern Brazil), which have a high diversity of benthic
incrusting organisms. Unlike many marinas, the YCI is a recreational marina where
human activities are strictly controled to minimize dumping of waste on the water, such
as the prohibition of use of non-biodegradable products and non hook-and-line fisheries
are forbidden. The floating platforms, where the boats are moored, are surrounded by a
breakwater that presents physical conditions more similar to the natural rocky shores
16
nearby, while the area inside the marina have more calm waters with higher
accumulation of organic matter and sedimentation and lower luminosity, characteristics
more similar to coastal bays, but with high potential to organic and inorganic pollution.
In this context, the objectives of this study were to characterize quali-quantitatively, and
temporally, the reef fish assemblages at these two areas, close to each other (130 m), but
exposed to distinct environmental conditions. To describe the local effect caused by the
construction of the marina I tested the following hypotheses: (1) the same reef with two
closely areas submitted to different environmental conditions have fish assemblages
with distinct trophic structure; and (2) these assemblages vary temporally.
MATERIAL AND METHODS
Study site. São Sebastião Island is the main island of an archipelago with 348.3 km²
which delimits the São Sebastião Channel (23º41’–23º54’S, 45º19’–45º30’W), a 25 km
strait on the northern coast of São Paulo State, in Southeastern Brazil (Figure 1). This
region is under the influence of warm oligotrophic waters from the Brazil Current, cold
nutrient-rich waters from the Falklands Current and is also influenced by cold and
nutrient-rich water intrusions from the South Atlantic Central Water over the shelf and
summer upwelling (Matsuura 1986, Castro-Filho & Miranda 1998, Gibran & Moura
2012). This study was conducted at the floating platforms of the Yacht Club de Ilhabela
(YCI), at Ilhabela City, in two neighbouring areas separated by 130 meters. One area is
at the breakwater, where environmental conditions are similar to those of natural rocky
habitats of the insular margin of the São Sebastião Channel, while the other area is
sheltered from waves, inside the marina, where boats are moored (Figure 1).
17
Fig. 1. Map of the study region – Yacht Club de Ilhabela - YCI, São Sebastião Channel
(modified from Gibran 2010 and Gibran & Moura 2012). Aerial view (Google Maps) of
the floating platform of YCI: (A) breakwater (area exposed to waves); (B): area inside
the marina (area protected from waves).
Field work. I conducted this study between September 2013 and June 2015, totalling
ten trips to the local of study. The samplings were diurnal and replicated over hot/wet
(October to March) and cold/dry (April to September) months.
Abiotic factors. To characterize the physical condition in both areas, I monthly (August
2014 to March 2015) measured environmental variables that can be vary according to
sheltered area and intensity of anthropic impact: water temperature, redox potential
(ORP), salinity, dissolved oxygen, turbidity, turbulence, and chlorophyll A. The first
five variables were recorded using the multi-parameter equipment Hana HI9829, and
water turbulence was indirectly measured by weight loss of plaster blocks (modified
from Kasten & Flores 2013). To measure primary productivity, chlorophyll A
concentration was measured using CTD JFE Advantec CO.LTD (AAQ127 model)
equipment (three occasions during the study period: November 2014 and January and
March 2015) by sampling water column.
18
Fish fauna. Fish fauna surveys were performed in floating platforms by non-stationary
visual census technique conducted during daytime by snorkelling; each sample had five
minutes of duration and covered an area of 1 m depth by 12 m width, this depth was
chosen because floating platform of the marina has 1-2 m depth. Visual censures at both
areas were six times replicated during each field trip. During this procedure the diver
swan over transects at a constant speed (1.5 m away from the platform), recording all
fishes displayed, considering fish species and individual size classes (< 2 cm, 2-10 cm,
10-20 cm, 20-30 cm, 30-40 cm and >40 cm of Total Length – TL). Recorders were
conducted from 9:00-16:00 and care was taken to equally distribute samples along the
day. Data from censuses were used to describe fish composition, abundance, species
richness and the trophic structure for each area. During the study period each area was
sampled 44 times, totalling 88 samples in seven occasions (25 during hot/wet months
and 19 during cold/dry months). Species found in transects were classified into trophic
categories following Ferreira et al. (2004) and Halpern & Floeter (2008).
Data analyses. Water temperature, redox potential (ORP), salinity, dissolved oxygen,
turbidity, turbulence were compared between areas (inside the marina vs. breakwater)
and months through multivariate methodologies with normalized data and Euclidian
distance (PERMANOVA: nMDS: SIMPER (Clarke 1993, Clarke & Warnick 2001,
Anderson 2001, McArdle & Anderson 2001), using PRIMER 7. The chlorophyll data
was analyzed separately from the others abiotic factors using univariate analysis. To
compare the species richness and abundance of the two areas considering the sampling
period (nested in season) and season (hot/wet vs. dry/cold) I used analysis of variance
(nested ANOVA) and post-hoc Tukey test, wherein sampling period, season and area
were predictor variables and richness and abundance were variable response. The
interactions studied were: area, season, sampling period (season), area*season and
area*sampling period (season). The difference in fish size class distribution and the
percentage of different feeding habitats between areas were visually explored. To access
the differences in the fish assemblages between areas (inside the marina vs. breakwater)
and months were applied multivariate methodologies with normalized data and the tests
were performed from a matrix of species abundance x samples using Bray-Curtis
distance (PERMANOVA: nMDS: SIMPER).
19
RESULTS
The two study areas always presented different abiotic conditions within each
sampled month, but the magnitude of this difference ranged in time, resulting in an
interaction between area-month of sampling (Pseudo F7; 143 = 16.51, p <0.001; posteriori
tests for each month: p<0.001; Figure 2). In a few months, this difference was more
pronounced, while in others more discreet, but always with the breakwater and the area
inside the marina exposed to different conditions.
Fig. 2. Non-metric multidimensional scaling (nMDS) showing the differences in environmental
conditions (temperature, redox potential (ORP), salinity, dissolved oxygen, turbidity,
and water turbulence) between the two studied areas (closed symbols = inside the
marina; open symbols = breakwater). Different colors represent different months: light
green: August/2014; black: September/2014; rose: October/2014; blue:
November/2014; orange: December/2014; dark green: January/2015; brown:
February/2015 and red: March/2015.
The abiotic variables that most contributed to the differences between the two areas
were turbulence (higher in breakwater, accounts for 45% of the dissimilarity between
areas); the redox potential (ORP) and turbidity (both higher in the area inside the
marina, accounting for 19.4% and 10.4% of dissimilarity between areas, respectively).
Chlorophyll A concentration was also higher inside the marina, showing that this area
presents higher primary productivity than breakwater (Figure 3).
20
Fig. 3. Chlorophyll A concentration for each area (breakwater vs. inside the marina). Each point
represents the average monthly values.
I recorded 3,355 fish individuals during the censuses (2,376 inside the marina
and 979 at breakwater), from 19 species and 13 families (Actinopterygii). The most
speciose family was Blennidae, with four species (Scartella cristata, Parablennius
marmoreus, Parablennius pilicornis and Hypleurochilus fissicornis), followed by
Pomacentridae (Adudefduf saxatilis and Stegastes fuscus), Labrisomidae (Labrisomus
nuchipinnis and Malacoctenus delalandii), and Epinephelidae (Epinephelus marginatus
and Mycteroperca acutirostris). The remaining families were represented by only one
species each (Table 1).
21
Table I. Trophic guilds and abundance of fish species recorded in both areas
(breakwater vs. inside the marina).
Species (abbreviation) Trophic guild Total abundance
Breakwater Inside the marina
Balistidae
Balistes capriscus (Bcap) mobile benthic
invertebrate feeder 0 1
Blennnidae
Hypleurochilus fissicornis (Hfis) omnivore 0 22
Parablennius marmoreus (Pmar) omnivore 3 5
Parablennius pilicornis (Ppil) omnivore 6 18
Scartella cristata (Scri) territorial
herbivore 593 79
Carangidae
Caranx latus (Clat) piscivore 1 0
Clupeidae
Harengula jaguana (Hjan) planctivore 100 1139
Haemulidae
Anisotremus virginicus (Avir) mobile benthic
invertebrate feeder 0 2
Kyphosidae
Kyphosus spp. (Kspp) macroalgal
browser 0 8
Labrisomidae
Labrisomus nuchipinnis (Lnuc) mobile benthic
invertebrate feeder 0 1
Malacoctenus delalandii (Mdel) mobile benthic
invertebrate feeder 0 7
Monacanthidae
Stephanolepsis hispidus (Shis) omnivore 0 1
Mulgilidae
Mugil curema (Mcur) plaktivore 34 0
Pomacanthidae
Pomacanthus paru (Ppar) spongivore 0 3
Pomacentridae
Abudefduf saxatilis (Asax) omnivore 161 611
Stegastes fuscus (Sfus) territorial
herbivore 0 1
Epinephelidae
Epinephelus marginatus (Emar) carnivore 1 0
Mycteroperca acutirostris (Macu) piscivore 0 2
Sparidae
Diplodus argenteus (Darg) omnivore 80 476
Total number of individuals 979 2376
22
The most abundant species was Harengula jaguana (37%), which forms schools
with more than 100 individuals, followed by Abudefduf saxatilis (23%), Scartella
cristata (20%) and Diplodus argenteus (17%). These species represented 96.5% of total
fish abundance, but different species dominated each locality – while H. jaguana, A.
saxatilis and D. argenteus were more abundant inside the marina, fish assemblages at
the breakwater were dominated by S. cristata. Besides that, 10 of the 19 species
recorded during the study were exclusive of the area inside the marina (Figure 4). These
differences in composition and abundance resulted in distinct fish assemblages (Figure
5; Table II), in which the most abundant species were responsible for the dissimilarity
between localities: S. cristata (24.2%), D. argenteus (20.1%), A. saxatilis (19.4%), and
H. jaguana (18.7%), resulting in 64.6% of average dissimilarity between areas
(SIMPER analysis). The temporal differences in fish assemblages between the two
areas were mainly due to the greater abundance of H. jaguana inside the marina and of
S. cristata in the breakwater area in the hot/wet period (Figure 6).
Fig. 4. Dominance of fish species recorded for the two studied areas (breakwater vs. inside the
marina) (see Table I for abbreviation of species names).
23
Fig. 5. Non-metric multidimensional scaling (nMDS) for fish assemblages considering the two
studied areas and periods. BW: breakwater; IM: inside the marina; H/W: hot/wet period;
C/D: cold/dry period.
Table II. PERMANOVA comparing fish assemblage composition across areas (breakwater vs.
inside the marina), sampling periods, and seasons (hot/wet vs. cold/dry).
Source of variation df MS Pseudo-F p
Area 1 47109 44.831 0.001
Season 1 13233 12.593 0.001
Sampling period(Season) 5 3540.3 3.3692 0.001
Area*Season 1 2999.4 2.8544 0.028
Area*Sampling period(Season) 5 3128.7 2.9775 0.001
Res 67 1050.8
Total 80
BW (H/W) BW (C/D)
IM (H/W) IM (C/D)
24
Fig. 6. Mean abundance per sample (transect) for the mains species responsible by
dissimilarities of the two areas (breakwater vs. inside the marina) along the seasons
(hot/wet vs. cold/dry)
The 19 species recorded belong to eight trophic guilds, five in breakwater and
seven inside the marina: carnivores, macroalgal browsers, mobile benthic invertebrate
feeders, omnivores, planktivores, piscivores, spongivores and territorial herbivores
(Table I). Territorial herbivores, omnivores and planktivores were the most abundant
guilds (99% of total fishes recorded). The breakwater was dominated by territorial
herbivores S. cristata, while the area inside the marina was dominated by generalist
omnivores (especially D. argenteus e A. saxatilis) and planktivores (H. jaguana)
(however, planktivores were not very frequent; Figure 7).
25
Fig. 7. Relative abundance of trophic guilds of fishes presented in the two studied areas
(breakwater vs. inside the marina). Values inside each bar correspond to total
abundance for each guild.
The abundance of fishes changed through seasons and even whitin seasons
(differents sampling periods), but the breakwater showed more abundance than inside
the marina area just during the hot/wet seasons. No differences were found in
abundance between areas during cold/dry months (post-hoc tests, p>0.05) (Tables I-III;
Figure 8). The two areas showed variation on abundance across seasons, with more
fishes in hot/wet period.
593
250
134
1239
1133
26
Fig 8. Mean abundance (± standard error) of fishes at hot/wet vs. cold/dry months for the two
studied areas (inside the marina vs. breakwater). *p<0.001.
Table III. Analyze of variance (nested ANOVA) on fish abundance considering area
(breakwater vs. inside the marina), sampling period, and seasons (hot/wet vs. cold/dry) effects
(*= p<0.05).
Source df MS F-ratio p-value
Season 1 14167.5 14.07 <0.001
Area 1 21478.6 21.34 <0.001
Season*Area 1 908.6 0.90 0.345
Sampling period(Season) 5 2579.6 2.56 *0.035
Area* Sampling period(Season) 5 820.0 0.82 0.543
Error 70 1006.6
The area inside the marina was richer than breakwater, and there was no
difference between sampling periods within each season. The interaction between
season and area was caused by the larger difference on species richness during the
hot/wet season, no differences were found between areas in cold/dry richness (post-hoc
tests, p>0.05) (Figure 9; Table IV). Both areas showed variation on richness across
seasons, with more fishes in hot/wet periods.
Seasons
*
27
Fig 9. Mean species richness (± standard error) of fishes at hot/wet vs. cold/dry months for the
two studied areas (inside the marina vs. breakwater) (*= p<0.001).
Table IV. Analysis of variance (nested ANOVA) on species richness of fishes considering the
area (breakwater vs. inside the marina), sampling periods, and seasons (hot/wet vs.
cold/dry) effects (*= p<0.05).
Source df MS F-ratio p-value
Area 1 27.3 25.86 <0.001 Season 1 60.0 56.79 <0.001 Season*Area 1 7.3 6.94 *0.010
Sampling period(Season) 5 1.5 1.49 0.202
Area* Sampling period (Season) 5 1.4 1.41 0.230
Error 70 1.0
Both areas showed high abundance of fishes with 2-10 cm TL (approximately
80% of total individuals recorded), showing that both areas are composed either of
juvenile fish individuals, mainly represented by H. jaguana, D. argenteus and A.
saxatilis, or of small species, as the Blennidae species (Figure 10).
Seasons
*
28
Fig. 10. Mean abundance of fishes for six size classes of total length (TL) for the two studied
areas (breakwater vs. inside the marina).
DISCUSSION
Although very spatially close, the two studied areas showed clear differences in
environmental conditions. Local assemblages of reef fishes are influenced by
interactions among availability of larval and survival of recruits with abiotic and biotic
factors, as well by event disorders (naturals or caused by human). Within the abiotic
factors turbulence has been cited as the main factor responsible for distribution of
species in reef environments; local with more wave exposure tends to have lower
abundance of fishes (e.g. Floeter et al. 2007, Krajewski et al. 2011, Krajewski & Floeter
2011). Fish species richness and abundance can be associated with food resources (e.g.
phytoplankton abundance) and shelters, what can explain why we observed a more
diverse fish assemblage inside the marina. One reason for the low abundance in areas
with high exposure to waves is because in these areas fishes have to spend a lot of
energy swimming (Johansen et al. 2007, Krajewski et al. 2011). So, these areas may
have a predominance of fishes with morphological characteristics that keep them in
contact with the substrate or make them good swimmers (Krajewski & Floeter 2011); an
example is S. cristata, abundant at the breakwater, that has several morphological (e.g.
junction of pelvic fins) and physiological adaptations that enable it to inhabit areas with
29
higher hydrodynamics. In other words, the distribution of species is strongly related to
the swimming ability of each species of fish (Fulton & Bellwood 2005, Johansen et al.
2007, Krajewski et al. 2011). Additionally, S. cristata is a territorial herbivore and
because of this is dependent on light, since this fishes depend on algal growth in their
territories to feed on (Barnecle et al. 2008, Krajewski & Floeter 2011).
On the other hand, the low hydrodynamics can make the environment highly turbid,
which affect the orientation of various fishes, such as planktivorous and mobile
invertebrate feeders (Hobson 1991). The higher turbidity and nutrient enrichment inside
the marina is the result of sedimentation of fine particles, including organic material,
due to the calm waters between floating platforms and the presence of many vessels (see
Guiral et al. 1995). Indeed, an increase in algae density or organic material, such as
feces and dead organisms, is usually associated to the inner parts of artificial reefs
(Ambrose & Anderson 1990, Zalmon et al. 2012), and may reduce water transparence.
The high abundance of fishes inside the marina was due, in part, by the presence of
large schools of the scaled herring Harengula jaguana, a planktivore species, which
may be attracted by the potential high concentration of plankton and protection from
pelagic predators. This area also presented more concentration of chlorophyll due to
higher concentration of phytoplankton. Besides being a less productive area, the
breakwater has more turbulence (high hydrodynamism) where planktivores are usually
absent or scarce (Pinheiro et al. 2013), but this was the main habitat for the molly miller
Scartella cristata, a territorial herbivore that rarely exceeds 4 m² during foraging
activities (Mendes, 2006) and may be favored by the availability of turf and calcareous
algae at breakwater and surf zones (Costa 2009, Pinheiro et al. 2013), besides low
density or absence of predators and competitors, what ensures some advantage in terms
of food supply and use of space (see Graham et al. 1985, Mendes 2006, Mendonça-Neto
et al. 2008).
Despite being an artificial reef, the studied areas showed similarity in composition
and species dominance with natural rocky habitats (e.g. Ferreira et al. 2001, Mendonça-
Neto et al. 2008, Gibran & Moura 2012), to be dominated by species with wide
geographic range, as D. argenteus, A. saxatilis and H. jaguana. Besides this, reef
species diversity found here was lower than recorded in other studies along the
Brazilian coast (e.g. Floeter et al. 2001, Ferreira et al. 2004) and at the São Sebastião
region (e.g. Gibran e Moura 2012), but this can be a result of the depth sampled during
30
visual censuses (only 1 m, very close to the surface, and almost not sampled during
other fish studies). Depth is an important variable for reef fish assemblages, as some
species and trophic groups may occur at specific depth zones on reefs (Clarke 1977,
Green 1996, Fox & Bellwood 2007, Krajewski & Floeter 2011)
Regardless of abiotic factors, biological factors that control these local communities
are related to recruitment, ecological interactions (as predation and competition), as well
as human impacts, which are difficult to measure (Pinheiro et al. 2013). Distinct local
assemblages can be modulated by the abundance of food and their predators, as well as
the presence and abundance of competitors. Marina facilities cause changes in physical
and chemical conditions on the coast that may affect the abundance, composition and
richness of fishes at local assemblages, through impacts, direct or indirect. Nevertheless,
two close areas may be affected in different ways, resulting in different assemblage
structures.
Oricchio (2015) conducted several experiments in these same two areas, and found
that sessile animals usually eaten by fishes (mostly ascidians) are more abundant in the
breakwater than inside the marina. In addition, I found that predation pressure exerted
by fish is much higher in the breakwater than inside the marina (see Chapter 2:
according to personal observations, D. argenteus and A. saxatilis feed mostly on
plankton when inside the marina, but feed almost exclusively on incrusting organisms
on the platforms when at breakwater). Therefore, I suggest that fishes are using different
foraging strategies as a result of the differences of circulation and productivity between
areas. Studies quantifying the source of food eaten by D. argenteus and A. saxatilis
from the two areas can help to the test this hypothesis. When different areas are spatially
close, with no physical barriers between them, fishes are able to swim from one area to
another (two areas need to be at least 0.5 miles or 806 m away to have no flow of reef
fishes; cf. Chang et al. 1977, Cummings 1994). An example are the generalist
omnivores Diplodus argenteus and Abudefduf saxatilis, that probably swim along the
study areas and are able to succeed both in exposed as sheltered areas (e.g. Floeter et al.
2007, Gibran & Moura 2012). However, with the exception of the Blennidae and
Labrisomidae species, all other fish species recorded are able to swim by the whole
studied site.
The use of artificial reefs has been encouraged with enthusiasm in the last decades
(see Pickering et al. 1999, Epstein et al. 2001) but was under extensive discussion (e.g.
31
Svane & Petersen 2001). These environments can be an important tool to mitigate
environmental stresses, especially if they have a biogenic substratum similar to the
naturally find on adjacencies (Carr & Hixon 1997). However, although floating
platforms may have less impact on local hydrodynamics than no-floating ones, reef
systems are strongly context-dependent due to the influence of a broad array of
ecological processes (see Gibran & Moura 2012). Large ports, as the expected
expansion of the São Sebastião Port, at the continental margin of the São Sebastião
Channel, will greatly alter environmental conditions, impacting a mangrove area that
will be fully covered by platforms preventing light penetration and surface water
circulation (thus reducing productivity and increasing eutrophication), with additional
stressors and severe loss of local biodiversity (see Freitas et al. 2009, Amaral et al.
2010, Gibran & Moura 2012).
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35
CAPÍTULO 2
HOW MARINE FACILITIES AFFECT THE ROLE OF FISH PREDATION
ON EARLY-LIFE STAGES OF BENTHIC ORGANISMS?
ABSTRACT
Predation is one of the key processes structuring communities. In marine systems, fishes
are the main predators of sessile benthic organisms that dominate hard substrata. The
southern and southeastern Brazil are devoid of coral reefs, but are characterized by
intense presence of rocky reef habitats and diverse man-made structures, like marinas
and piers. In both natural and artificial hard substrata, organisms like calcareous algae,
sponges, ascidians, bryozoans and polychaetes can settle and create a complex
tridimensional structure. These organisms are exposed to predation, especially by reef
fishes (both juveniles as adults) and, thus, may show differences in community structure
when subjected to different predation pressures. In this context, I investigated the
feeding activity and composition of fishes in two close areas (130 m of distance) of the
same artificial reef (a marina), one in breakwater (exposed to waves) and other inside
the marina (protected from waves), and analyzed feeding preferences of invertivore
fishes for both areas. To quantify feeding rates I performed underwater observations
(covering the range of 06:00 to 20:00): each area was sampled twice during hot/wet
(summer and spring) and twice during cold/dry (winter and autumn) months. To
quantify the pressure of predation I performed field experiments, as follow: six PVC
recruitment plates protected against predators by cages of exclusion was disposed at
each studied area for 40 days, when the cages were then removed and the incrusting
communities exposed to predators. Each plate community was video recorded (80 hours
of video for each area) and the numbers of fish bites, as the identification of predator-
prey species were recorded during daytime. Each area was video recorded twice during
hot/wet (summer and spring) and twice during cold/dry (winter and autumn) months.
There was a peak of feeding activity between 12:00-14:00 inside the marina. Five reef
fish species were recorded preying on incrusting animals, but the omnivore Diplodus
argenteus was the main predator among fishes for both areas, accounting for 94% of the
16,652 observed bites. The breakwater had more intense predation than the area inside
the marina. The most preyed items were ascidians (especially didemnids), serpulids and
36
arborescent bryozoans, varying according to the area. This work shows that different
environmental conditions in micro-scale due to marina facilities affect fish predation on
early-life stages of benthic organisms, which can also be influenced by availability of
prey.
Keywords: artificial reef, reef fishes, recruitment, Dideminidae, ascidian predation,
Diplodus argenteus, São Sebastião Channel.
INTRODUCTION
Predation is one of the key processes structuring communities (Steele 1996).
Nevertheless predation is not a fixed factor and can vary depending on the habitat,
environmental conditions and biotic interactions (e.g. competition). In marine systems,
fishes at different stages of development act as some of the main predators, especially in
biogenic substrata and reef sites, where colonial and solitary benthic organisms
dominate the bottom (Choat 1982, Hixon 1997, Connel & Anderson 1999). Most of
fish’s day is spend either pursuing food or avoiding predators; many fishes exhibit an
active, food-gathering phase, and a relatively inactive, resting phase, linked with
predators avoidance (Helfman 1993), and because of this, predation by fishes may also
vary during the 24h cycle. In addition to variation according to the area, biotic
interactions, environmental conditions, trophic complexity and time of day, predation
may also vary seasonally with relation to temporal fluctuations in environmental
conditions, reflected in the fish assemblages, such as reproductive period and periods of
decreased activity, such as during winter.
Incrusting organisms live on hard substrata and contribute to the composition,
richness and diversity of local communities, because they increase spatial heterogeneity
and complexity (providing more micro-habitats and spatial/feeding resources for other
organisms) (Sebens 1991, Thompson et al. 1996, Morgado & Tanaka 2001), what
results in high presence of benthic and nektobenthic fishes and, consequently, increases
the pressure of fish predation over incrusting organisms. So, fishes can be responsible
for some temporal and spatial variation in reef community structure and composition
(e.g. Kingsford 1992, Connel & Kingsford 1998). Ascidians and bryozoans are the most
frequent benthic organisms of the costal rocky reef fauna, although they are still
37
underestimated regarding ecological importance, when compared to sponges,
cnidarians, crustaceans and mollusks (McKinney & Jackson 1989, Reed 1991, Migoto
2000, Calderon 2008). These animals are widely distributed and often dominate hard
substrata, where they tend to monopolize space reducing local species diversity (Russ
1980; Vieira et al. 2012). On the other hand, these incrusting organisms are susceptible
to predators, especially during larval stages and during the first hours/days of post-
settlement, when colonies are so small and fragile that can be easily removed from the
community, through predation. The consequences of the disturbances caused by
herbivore fishes in algae communities have been better studied (e.g. Choat & Andrew
1986, McClanahan et al. 1999, McClanahan et al. 2001, Smith et al. 2001, Francini-
Filho et al. 2008) than the role of carnivore and invertivore predators (Hunt &
Scheibling 1997, Calderon 2008). Since predation can affect the establishment and
survival of recruits, it can play a key role in benthic community organization.
The southern and southeastern coast of Brazil are devoid of coral reefs, but are
characterized by intense presence of rocky reef environments, as islands, rocky outcrops
and parcels, besides rocky shores composed by igneous and metamorphic rocks (Rabelo
2007, Gibran & Moura 2012). Beyond these natural reef habitats there are many piers,
marinas, and others man-made structures that serve as artificial reefs, which are exposed
to the same conditions and dynamics than the natural and adjacent ones (Mineur et al.
2012). In these hard substrata, organisms like corals, calcareous algae, sponges,
ascidians, bryozoans and polychaetes growth to create a complex and tridimensional
structure which increases the feeding and spatial resources availability for fishes at the
infralittoral. This structural complexity allows ecological succession and post-
colonization by organisms with more environmental requirements (Gore et al. 1978,
Bradstock & Gordon 1983, Lewis & Snelgrove 1990, Safriel & Bem-Eliahu 1991,
Nalesso et al. 1995, Cocito et al. 2000, Morgado & Tanaka 2001).
Marinas and other marine facilities can change pressure of fish predation in a
positive or negative way (e.g. Chandler et al. 1985). For example, when such
constructions are associated with pollution and fisheries, it can reduce the abundance of
fishes and facilitate the dominance of communities of sessile animals by more resistant
species (inclusive exotic ones). But, when the construction is associated to a good
environmental management, it can increase the abundance and diversity of fishes
resulting in strong predation pressure which can increase local biodiversity (if
38
predation is focused on the dominant benthic species) or reduce local biodiversity (if
predation is diffuse) (Ruiz et al. 2009). So, an understanding of the effects of anthropic
interferences on top-down control are important in the context of marina facilities, since
marinas and ports are usually highly susceptible to bioinvasions that can threaten native
species. The goals of this study were compare the pressure of predation by fishes at two
close areas (130 m) in a marina with distinct environmental conditions based on data
from feeding activity and preferences of invertivore fish species, testing the following
hypotheses: differences in the trophic structure of fish assemblages and environmental
conditions of two closely reef areas result in different predation pressures by fish of
incrusting organisms.
MATERIAL AND METHODS
Study site. São Sebastião Island is the main island of an archipelago with 348.3 km²
which delimits the São Sebastião Channel (23º41’–23º54’S, 45º19’–45º30’W), a 25 km
strait on the northern coast of São Paulo State, in southeastern Brazil (Figure 1). This
region is under the influence of warm oligotrophic waters from the Brazil Current, cold
nutrient-rich waters from the Falklands Current and also by cold and nutrient-rich water
intrusions from the South Atlantic Central Water over the shelf and summer upwelling
(Matsuura 1986, Castro-Filho & Miranda 1998, Gibran & Moura 2012). This study was
conducted at the floating platforms of the Yacht Club de Ilhabela (YCI), at Ilhabela
City, in two neighbouring areas separated by 130 meters. One area is at the breakwater,
where environmental conditions are similar to those of natural rocky habitats of the
insular margin of the São Sebastião Channel (see Gibran & Moura 2012), while the
other area is protected from waves, inside the marina, where boats are moored, therefore
more susceptible to chemical (organic and inorganic) and physical pollution (Figure 1).
The sessile communities inside the marina are characterized by high densities of
bryozoans, especially Schizoporella errata, while the breakwater presented more
abundance of ascidian, especially Didemnum perlucidum, and serpulids. Because the
artificial reefs are set on floating platforms, all organisms are susceptible to the daily
tidal ranges.
39
Fig. 1. Map of the study region – Yacht Club de Ilhabela - YCI, São Sebastião Channel
(modified from Gibran 2010 and Gibran & Moura 2012). Aerial view (Google Maps) of
the floating platform of YCI: (A) breakwater (area exposed to waves); (B): inside the
marina (area protected from waves).
Feeding rates. To assess fish feeding rates throughout the diurnal and crepuscular
periods (06:00-20:00), and to detect if there was any peak of feeding activity at the two
studied areas, I did underwater observations on snorkeling on platforms at 1 m depth
(the smaller height of the platforms). This cycle of 14 hours was divided into seven
periods of two hours each. In each period I conducted 15 replicas of three minutes of
observations in which I recorded the species identification and the number of bites
performed by each fish individuals observed feeding on benthic incrusting organisms of
the floating platforms of YCI. Between March 2014 to March 2015 I performed four
cycles of observation (two during hot/wet – October to March – months and two
during cold/dry – April to September – months) for each one of the two studied areas
(i.e. breakwater and the area inside the marina).
Pressure of fish predation. To quantify fish predation on benthic organisms I vertically
hung six PVC plates (30 x 30 x 0.5 cm) on each area, at the floating platforms of the
marina. The plates were installed with a spacing of approximated three meters away and
1.2 m depth (Figure 2). Plates were left in the sea during 40 days, protected against
40
predators by plastic cages with a mesh of 0.5 cm. This procedure aimed to enable larval
recruitment at these plates, which will be composing by early-life stages of benthic
organism. After this period of time I removed the cages and recorded predation over
incrusting organisms with a high-definition (HD) digital video camera (GoPro Hero3
Black Edition) coupled to each plate. The records were taken simultaneous at the two
areas in two periods of the day, one in the morning (10:00, during 100 minutes) and
another in the afternoon (14:00, during 100 minutes), totaling 20 hours for each area
(200 minutes for each plate). Each area was sampled twice during hot/wet (October to
March) and twice during cold/dry (April to September) months, totaling 80 hours in
each period. Each plate was photographed before and after the exposure to predators, in
order to identify the preyed organisms. Videos were analyzed taking into account the
number of bites performed by each fish individual in each type of benthic prey available
on each plate, also considering the six size classes (< 2 cm, 2-10 cm, 10-20 cm, 20-30
cm, 30-40 cm and >40 cm of Total Length – TL) and species of the predators.
Fig. 2. Ilustration of the six plates installed in each area (breakwater and inside the marina) (left)
and photography of a plate during video redord (right).
Data analyses. To compare the predation pressure along the day of the two studied
areas I used analysis of variance (nested ANOVA) and post-hoc Tukey test, with
log(x+1) transformed data, wherein area and period of day were predictor variables and
bites were response variable. The interactions (with pressure predation – bites) studied
were: area, period of day, and area*period of day. The analysis of variance (nested
ANOVA) and post-hoc Tukey test, on log(x+1) transformed data was also used to
41
compare predation pressure by fishes (bites) considering sampling period (nested in
season) and season (hot/wet vs. dry/cold), wherein sampling period, season and area
were predictor variables and bites by predator and number of predation records were
response variables. The interactions (with pressure predation – bites) studied were: area,
season, sampling period (season), area*season and area*sampling period (season). The
differences in fish size classes’ distribution and the percentage of different feeding
habitats between areas were visually explored.
RESULTS
I recorded 960 fish individuals from 13 species and nine families of Actinopterygii
feeding on incrusting organisms of the platforms of the YCI. These species included
diverse trophic guilds following Ferreira et al. (2004) and Halpern & Floeter (2008), as
omnivores, piscivores, territorial herbivores, macroalgal browsers and mobile
invertebrate feeders. The more abundant species, considering both studied areas, were
Diplodus argenteus (63%), Abudefduf saxatilis (10.7%), and Scartella cristata (10%)
(Table I).
42
Table I. Predators (fish species) and abundances (total and relative) for both areas (breakwater
vs. inside the marina).
Species Total abundance (relative
abundance) Trophic guilds
Breakwater
Inside the
marina
Blennnidae
Hypleurochilus fissicornis 4 (0.6 %) 18 (6.1%) omnivore
Parablennius marmoreus 11 (1.6%) 5 (1.7%) omnivore
Parablennius pilicornis 4 (0.6%) 2 (0.7%) omnivore
Scartella cristata 97 (14.6%) 31 (10.5%) territorial herbivore
Carangidae
Caranx latus 0 (0%) 1 (0.3%) piscivore
Kyphosidae
Kyphosus spp. 3 (0.4%) 46 (15.6%) macroalgal browser
Labrisomidae
Labrisomus nuchipinnis 1 (0.1%) 0 (0%) mobile invertebrate feeder
Malacoctenus delalandii 0 (0%) 13 (4.4%) mobile invertebrate feeder
Monacanthidae
Stephanolepsis hispidus 0 (0%) 9 (3%) omnivore
Pomacanthidae
Pomacanthus paru 0 (0%) 6 (2%) spongivore
Pomacentridae
Abudefduf saxatilis 63 (9.5%) 37 (12.5%) omnivore
Epinephelidae
Mycteroperca acutirostris 4 (0.6%) 0 (0%) piscivore
Sparidae
Diplodus argenteus 478 (72%) 127 (43%) omnivore
The fish species with the largest number of predation events observed in the
breakwater were D. argenteus (44%), Kyphosus spp. (37%), A. saxatilis (7%) and
Scartella cristata (5%), while inside the marina was D. argenteus (91%), followed by
A. saxatilis (5%) and S. cristata (2%).
The assemblages of fishes at inside the marina did show a peak of feeding
activity between the 12:00 – 14:00, but at breakwater area they presented higher levels
of feeding activity between the 12:00 – 18:00 (Figure 3; Table II). These results were
used to the next stage (= video records).
43
Fig. 3. Mean fish bites per hour (± standard error) throughout the diurnal and crepuscular
periods performed by fishes for both studied areas (breakwater vs. inside the marina).
Table II. Analysis of variance of feeding pressure (fish bites on platforms) considering area
(breakwater vs. inside the marina) and period of day (06:00-20:00).
Source df MS F-ratio p-value
Area 1 0.3 3.37 0.067
Period of day 6 1.0 9.62 <0.001
Period of day*Area 6 0.0 0.21 0.971
Error 407 0.1
I recorded six reef fish species preying on the PVC plates (five species per area):
D. argenteus, A. saxatilis and Stephanolepis hispidus in both areas; Hypleurochilus
fissicornis only in breakwater; and Pomacanthus paru only inside the marina. Diplodus
argenteus, the main predator for both areas, had 95% of total fishes recorded and
performed 94% of all bites combined (Figure 4). Diplodus argenteus was the major
predator in the breakwater, but inside the marina were D. argenteus and S. hispidus.
Herbivorous fishes were almost absent from the video records because there was no
significant growth of macroalgae on the PVC plates. The two studied areas were
exposed to different intensity of predation (i.e. number of fish bites). I recorded 13,409
44
bites (average = 558 ± 114) at breakwater and 3,243 inside the marina (average = 135 ±
75) (F1;11.4 = 17.9; p<0.001; Table III). The high standard error values found is due to
the variability of predation during shooting, approximately 100 hours of 160 hours
(60%) showed no predation record. Considering the fishes recorded, 2,076 were
preying on PVC plates at breakwater and 386 inside the marina (F1;5.1 = 13.7; p<0.001;
Table IV).
Fig. 4. Relative percentage of fish bites for both areas (breakwater vs. inside the marina). Values
inside the bars correspond to the total bites of each species.
Table III. Analysis of variance of predation pressure (fish bites on plates) considering the area
(breakwater vs. inside the marina), sampling period, and season (hot/wet vs. cold/dry
periods) effects (*= p<0.05).
Source df MS F-ratio p-value
Area 1 11.438 17.918 <0.001
Season 1 0.361 0.565 0.456
Season*Area 1 4.377 6.857 *0.012
Sampling period(Season) 2 15.477 24.245 <0.001
Area*Sampling period(Season) 2 1.704 2.67 0.082
Error 40 0.638
13219 2504
687
45
Table IV. Analysis of variance of fish records (predators) considering the area (breakwater vs.
inside the marina), sampling period, and season (hot/wet vs. cold/dry periods) effects.
Source df MS F-ratio p-value
Area 1 5.1 13.79 <0.001 Season 1 0.04 0.12 0.728
Season*Area 1 0.8 2.16 0.149
Sampling period(Season) 2 7.7 20.63 <0.001 Area*Sampling period(Season) 2 0.4 1.30 0.282
Error 40 0.3
Diplodus argenteus presented different predation pressure between the two
areas, with more bites on the breakwater (Table V, post-hoc tests, p>0.05). I found an
interaction between fish predation pressure and sampling periods. No difference in
predation pressure by S. hispidus was recorded, but it vary according to sampling period
and season, with interactions between season and area, and sampling period and area
(Table VI).
Table V. Analysis of variance of predation pressure (fish bites on plates) by Diplodus argenteus
considering the area (breakwater vs. inside the marina), sampling period, and season (hot/wet vs.
cold/dry periods) effects (*= p<0.05).
Source df MS F-ratio p-value
Area 1 13.9 12.12 <0.001
Season 1 0.01 0.06 0.806
Season*Area 1 1.5 1.33 0.255
Sampling period(Season) 2 8.8 7.67 *0.002
Area*Sampling period(Season) 2 1.0 0.87 0.426
Error 40 1.1
Table VI. Analysis of variance of predation pressure (fish bites on plates) by Stephanolepsis
hispidus considering the area (breakwater vs. inside the marina), sampling period, and season
(hot/wet vs. cold/dry periods) effects (*= p<0.05).
Source df MS F-ratio p-value
Area 1 1.4 7.80 0.008
Season 1 1.8 10.00 *0.003
Season*Area 1 1.2 6.70 *0.013
Sampling period (Season) 2 1.3 7.25 *0.002
Area* Sampling period (Season) 2 1.9 10.67 <0.001
Error 40 0.1
Results of shooting showed that predation on plates of YCI were more intense in
the breakwater, but only during the hot/wet periods (Figure 5). In contrast, predation did
not differ between the two areas during the cold/dry season, but there was large
46
variation of the predation pressure within this season (Figure 5; Table IV). Considering
each area, any pattern in relation to seasons was detected.
Fig. 5. Mean fish bites (± standard error) per plates for each studied area (breakwater vs. inside
the marina) and during hot/wet vs. cold/dry months (*= p<0.001).
Both areas recorded through filming showed a high abundance of fishes with 10-
20 cm TL (approximately 80% in breakwater and 50% in inside the marina area of total
individuals recorded), showing that both areas are composed by predators of incrusting
organisms during juvenile phase, represented almost exclusively by D. argenteus
(Figure 6).
* *
47
Fig. 6. Relative abundance of fishes for six size classes of total length (TL) for the two studied
areas (breakwater vs. inside the marina).
The following benthic incrusting organisms were preyed throughout the study:
turf algae, solitary ascidian, colonial ascidian, arborescent bryozoan, incrusting
bryozoan, serpulids, barnacles and oysters. The most preyed taxa on settlement plates
were the colonial ascidians Botrylloides sp., Didemnum sp. (Didemnidae), Distaplia sp.,
Clavelina oblonga, Perophora sp., and Symplegma (Styelidae). Ascidians of
Didemnidae family were the main preyed items in breakwater area, while ascidians of
Didemnidae and serpulid polychaets were the most preyed items inside the marina
(Figures 7-8).
48
Fig. 7. Percentage of bites on the most preyed benthic organisms (taxa) for both areas
(breakwater vs. inside the marina). Values inside the bars are the total number of bites.
Among the groups heavily preyed, ascidians and bryozoans presented
differences in predation pressure for both areas (F1;7.4=11.20 and F1;9.3=17.69,
respectively; p>0.01), and more consumption of these preys at breakwater (Tukey test
p>0.01). The consumption of ascidians, bryozoans, turf algae and serpulids differ
between different sampling periods (Table VII-X; Figure 8).
Table VII. Analysis of variance of predation pressure (fish bites on plates) on ascidians,
considering area (breakwater vs. inside the marina), sampling period, and season (hot/wet vs.
cold/dry periods) effects (*= p<0.05).
Source df MS F-ratio p-value
Area 1 7.4 11.20 *0.002
Season 1 1.5 2.28 0.139
Season*Area 1 2.7 4.17 *0.048
Sampling period (Season) 2 12.0 17.96 <0.001
Area*Sampling period(Season) 2 1.4 2.17 0.127
Error 40 0.6
1590
5546
3961
954
375
1129
529
49
Table VIII. Analysis of variance of predation pressure (fish bites on plates) on bryozoan,
considering area (breakwater vs. inside the marina), sampling period, and season (hot/wet vs.
cold/dry periods) effects.
Source df MS F-ratio p-value
Area 1 9.3 17.69 <0.001
Season 1 0.4 0.84 0.364
Season*Area 1 1.7 3.37 0.074
Sampling period(Season) 2 6.8 12.98 <0.001
Area*Sampling period(Season) 2 0.5 1.10 0.342
Error 40 0.5
Table IX. Analysis of variance of predation pressure (fish bites on plates) on turf algae,
considering area (breakwater vs. inside the marina), sampling period, and season (hot/wet vs.
cold/dry periods) effects (*= p<0.05).
Source df MS F-ratio p-value
Area 1 1.2 3.49 0.069
Season 1 1.5 4.33 *0.044
Season*Area 1 0.3 1.00 0.322
Sampling period(Season) 2 1.2 3.40 *0.043
Area*Sampling period(Season) 2 0.3 0.89 0.418
Error 40 0.3
Table X. Analysis of variance of predation pressure (fish bites on plates) on serpulids,
considering area (breakwater vs. inside the marina), sampling period, and season (hot/wet vs.
cold/dry periods) effects (*= p<0.05).
Source df MS F-ratio p-value
Area 1 0.1 0.55 0.461
Season 1 4.1 13.69 *0.001
Season*Area 1 1.2 4.08 0.050
Sampling period(Season) 2 6.4 21.37 <0.001
Area*Sampling period(Season) 2 0.8 2.90 0.067
Error 40 0.3
50
Fig. 8. Mean fish bites (± standard error) on the most preyed benthic organisms (taxa) for both
areas (inside the marina vs. breakwater) and at different moments.
The main predator on the sessile animal communities in the YCI, D. argenteus,
demonstrated broad consumption of different food items, mainly Didemnid ascidians
(Figure 9). At breakwater, consumption was less varied and showed no significant
difference among the main items consumed.
51
Fig. 9 Total bites of the silver porgy Diplodus argenteus (Sparidae) on benthic organisms for
the two studied areas (breakwater vs. inside the marina) (*colonial ascidians).
DISCUSSION
Predation pressure depends on the abundance of predators and the availability of
prey, as well as of environmental disturbances caused by human activities. Different
* * * *
* *
* * * * *
*
Breakwater
Inside the marina
*
52
areas may respond differently to a disturbance, resulting in different predation
pressures. The results found here corroborate to the knowledge that predation may vary
over time and space and can be also a result of differences in local conditions due to the
organism-organism interactions (e.g. top-down and bottom-up effects) and interactions
between organisms and environment. The results of fish feeding activity throughout the
day can be closely related to the availability of light in each studied area, as fish
predators of incrusting organisms depend mainly on visual orientation to feed, with
lighter periods of the day having higher levels of predation (Helfman 1993). on benthic
communities at breakwater along the entire period of the day, but as the area inside the
marina is shaded by boats in high-to-this period, this area had higher fish feeding
activity only at midday.
While fishes foraging inside marina have more protection from predators, fishes at
the breakwater spend more energy swimming due to wave action, but the availability of
ascidians, the main prey consumed, is higher at breakwater than inside marina (personal
observations). On the other hand, the area inside marina has more phytoplankton
concentration, an important resource for omnivore opportunistic species as D. argenteus
and A. saxatilis (see Chapter 1). Diplodus argenteus individuals use to feed mainly on
benthic invertebrates, but when in large groups they also feed on plankton (Ferreira et
al. 2004, Marques & Barreiros 2015). As inside marina has higher abundance of D.
argenteus and more concentration of phytoplankton, plankton consumption were
exclusive at this area (Chapter 1). In other words, changes in surface water circulation
caused by a floating marina seem to change local food web structure, by enhance habitat
heterogeneity and thus, resulting in different communities.
Studies on D. argenteus feeding are rare (but see e.g. Krajewski 2007, Reisser et al.
2010 for cleaning behavior performed by juveniles). Studies of fish diet available,
especially of adult D. argenteus never cite ascidians and bryozoans as important food
items (e.g. Dubiaski-Silva & Masunari 2006), the main items consumed herein for both
areas. However, the consumption of such items differed both between areas as sampling
period.
The sessile communities inside the marina are characterized by high densities of
bryozoans, especially Schizoporella errata, while the breakwater presented more
ascidians, especially Didemnum perlucidum, and serpulids (Oricchio 2015). It is
important to emphasize that the benthic organisms preyed by fishes during this study
53
were recently settled, with a maximum of 40 days after settlement, when colonies are
more vulnerable because physical and chemical defenses were not established yet.
Besides large colonies are more likely to avoid predation than small ones, older colonies
are more defended by secondary compounds and calcareous spicules than initial
colonies (i.e. Lindquist et al. 1992). So, the importance of predation on community
structuration is underestimated, because the majority of the studies are focused only on
established communities (Sebens 1991). Predation pressor during initial stages of
benthic communities is important to module the composition of species and abundance
in the later stages of community – as an example, when predators remove ascidians in a
community the response is an increase of bryozoan richness (Oricchio 2015).
Ascidians are considered unpalatable as a result of chemical and physical defenses
(e.g. Russel 1983), but the studies that tested the palatability of ascidians were generally
conducted in artificial conditions, selecting only one or just a few potential predators,
besides be based in chemical extracts (e.g. Stoecker 1980, Teo & Ryland 1994).
Another common problem is the lack of accuracy on prey identification in studies based
on stomach content analysis of fishes, always underestimating food items as ascidians,
sponges, briozoans etc.
Another relevant find of this study was that the number of fishes preying on PVC
plates decreased through time, probably as a result of the reduction in the food resources
availability, what is supported by the "Marginal Value Theory", which predicts that the
optimal time of predator permanence should be higher in the most productive spots than
in less productive, and if this productivity is very low the time of permanence would be
zero (Begon et al. 2007). It was observed in plates with low benthic cover, especially
with low coverage of Diplosoma listerianum and Didemnium perlucidum (ascidians
Didemnidae).
This study shows that different environmental conditions in micro-scale due to
marina facilities affect fish predation on early-life stages of benthic organisms in time
and space, which can also be influenced by availability of prey. The abundance of
predators is also relevant, as the feeding plasticity (i.e. use of food) and swimming
abilities (i.e. use of space) by each fish species.
54
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58
CONSIDERAÇÕES FINAIS
Os resultados deste estudo contribuem para o entendimento da estruturação das
comunidades de organismos incrustantes e das assembleias de peixes recifais, além de
destacar os efeitos ecológicos locais das construções humanas costeiras como marinas e
píeres nessas comunidades. Além disso, fornece dados inéditos sobre o papel da
predação dos peixes nos estágios iniciais das comunidades de organismos incrustantes,
mostrando que ascídias, geralmente ignoradas em análises de dieta, são importantes
itens alimentares para peixes, com detalhes da alimentação e atividade alimentar do
marimbá Diplodus argenteus (Sparidae).
As principais conclusões são:
1. Diferenças em pequena escala nas condições ambientais, como as causadas pela
instalação de marinas, podem tanto afetar as assembleias de peixes quanto as
comunidades incrustantes, assim como também resultar em diferentes pressões
de predação por peixes sobre a comunidade incrustante, modulando sua estrutura
após assentamento.
2. A plasticidade alimentar dos peixes pode ser resultado de dois importantes
fatores que podem operar conjuntamente ou não: o emprego de diferentes táticas
alimentares e a oferta alimentar – D. argenteus, a espécie de peixe recifal mais
abundante em ambas as áreas, preda exclusivamente organismos incrustantes no
quebra-mar, com intensa pressão de predação sobre eles, mas alimenta-se
principalmente de plâncton na área interna, onde é muito mais abundante.
3. Ascídias e briozoários, que normalmente não são considerados como itens
alimentares de peixes (especialmente ascídias, conhecidas por possuírem defesas
químicas e físicas, como espículas calcárias), foram amplamente consumidos,
principalmente pelo marimbá D. argenteus e pelo porquinho Stephanolepis
hispidus.
Por fim, reconhecer quais processos operam em micro-escalas é fundamental para
compreender a dinâmica das populações e comunidades e com isso minimizar os
impactos das atividades antrópicas sobre as comunidades e os ecossistemas.
59
Os próximos passos devem incluir a análise da disponibilidade de presas (oferta
alimentar) nas duas áreas de estudo, buscando dados mais adequados para avaliação das
preferências alimentares dos peixes que habitam o quebra-mar e a área interna da
marina do YCI. Cada um dos capítulos desta dissertação será submetido à publicação
como um manuscrito independente, sendo que o segundo (referente ao conteúdo do
capítulo 2) será em conjunto com os resultados de outra dissertação do nosso grupo de
pesquisa (ver Oricchio 2015*), sobre a importância do tamanho dos predadores e da
predação sobre recrutas para a organização de comunidades incrustantes marinhas.
*Oricchio, F.T. 2015. Qual a importância do tamanho dos predadores e da predação sobre recrutas para
a organização de comunidades incrustantes marinhas? Dissertação de Mestrado. Universidade
Federal de São Paulo, Diadema, 61 p.