Victor Emmanuel Lopes da Silva

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UNIVERSIDADE FEDERAL DE ALAGOAS
INSTITUTO DE CIÊNCIAS BIOLÓGICAS E DA SAÚDE
PROGRAMA DE PÓS-GRADUAÇÃO EM DIVERSIDADE BIOLÓGICA E
CONSERVAÇÃO NOS TRÓPICOS

VICTOR EMMANUEL LOPES DA SILVA

PADRÕES E PROCESSOS QUE REGEM AS DIMENSÕES DA DIVERSIDADE DE
PEIXES ESTUARINO-COSTEIROS DO ATLÂNTICO OCIDENTAL

MACEIÓ - ALAGOAS
Março / 2022

VICTOR EMMANUEL LOPES DA SILVA

PADRÕES E PROCESSOS QUE REGEM AS DIMENSÕES DA DIVERSIDADE DE
PEIXES ESTUARINO-COSTEIROS DO ATLÂNTICO OCIDENTAL

Tese apresentada ao Programa de PósGraduação em Diversidade Biológica e
Conservação nos Trópicos do Instituto de
Ciências Biológicas e da Saúde, Universidade
Federal de Alagoas, como requisito para
obtenção do grau de doutor em CIÊNCIAS
BIOLÓGICAS na área da Biodiversidade.

Orientadora: Dra. Nidia Noemi Fabré
Coorientadora: Dra. Marina Dolbeth

MACEIÓ - ALAGOAS
Março / 2022

Catalogação na fonte
Universidade Federal de Alagoas
Biblioteca Central
Divisão de Tratamento Técnico
Bibliotecária: Taciana Sousa dos Santos – CRB-4 – 2062
S586p Silva, Victor Emmanuel Lopes da.
Padrões e processos que regem as dimensões da diversidade de peixes
estuarino-costeiros do Atlântico Ocidental / Victor Emmanuel Lopes da Silva.
– 2022.
125 f. : il. color.
Orientadora: Nidia Noemi Fabré.
Coorientadora: Marina Dolbeth.
Tese (Doutorado em Ciências Biológicas) – Universidade Federal
de Alagoas. Instituto de Ciências Biológicas e da Saúde. Programa de PósGraduação em Diversidade Biológica e Conservação nos Trópicos. Maceió,
2021.
Inclui bibliografias.
Anexos: f. 123-125.
1. Biodiversidade - Conservação. 2. Ambiente estuarino. 3. Peixes. I.
Título.
CDU: 597: 504.74

Folha de aprovação
Victor Emmanuel Lopes da Silva
PADRÕES E PROCESSOS QUE REGEM AS DIMENSÕES DA
DIVERSIDADE DE PEIXES ESTUARINO-COSTEIROS DO
ATLÂNTICO OCIDENTAL
Tese apresentada ao Programa de Pós-Graduação
em Diversidade Biológica e Conservação nos
Trópicos, Instituto de Ciências Biológicas e da
Saúde. Universidade Federal de Alagoas, como
requisito para obtenção do título de Doutor(a) em
CIÊNCIAS
BIOLÓGICAS
na
área
da
Biodiversidade.

Tese aprovada em 31 de março de 2022.

Dra. Nídia Noemi Fabré/UFAL (orientadora)

Dra. Taciana Kramer de Oliveira Pinto

Dra. Luisa Maria Diele Viegas

Dr. Lucas Augusto Kaminski

Dr. Bruno Vilela de Moraes e Silva

Dr. José Amorim dos Reis Filho
MACEIÓ - ALAGOAS
Março / 2022

DEDICATÓRIA

Dedico esta dissertação a minha mãe
Ana Lucia Lopes da Silva, que sempre me
apoiou em todos os momentos e decisões.
Sem ela, esse produto não seria possível!
Te amo.

AGRADECIMENTOS

Embora seja praticamente impossível agradecer a todos que de alguma forma
me ajudaram durante o processo de produção deste trabalho, existem aquelas
pessoas que eu gostaria de dizer um obrigado muito especial.
Primeiramente, a Deus, por tudo!!
A minha mãe, Ana Lucia Lopes da Silva, pelos ensinamentos, apoio,
companheirismo, exemplo de vida e educação. Por ter estado ao meu lado em todos
os momentos, desde a escolha do curso de graduação até o final desta nova etapa.
A todos os meus familiares, em especial à minha irmã, Valeska Elynne, meu
padrasto, José Flávio e minha avó, Maria Lucia.
A minha sobrinha, Luna Lopes, que preencheu meus dias de alegria e felicidade
durante os anos finais do doutorado, tornando esse processo mais prazeroso.
As amigas de todas as horas, Elizabeth Costa Teixeira e Daniele Souto.
Obrigado por toda força e ajuda, pelos trabalhos desenvolvidos, pelos planos
compartilhados, por todo incentivo, pelas viagens, pelas vezes que nos perdemos em
alguma cidade desconhecida e principalmente pela amizade.
A minha orientadora Profa. Dra. Nidia Noemi Fabré, e ao Prof. Dr. Vandick da
Silva Batista por terem aberto as portas do Laboratório de Ecologia, Peixes e Pesca
(LaEPP) em 2010 e terem me acolhido, me proporcionando constantes momentos de
aprendizagem que levarei comigo por toda minha vida.
A todos que fizeram ou ainda fazem parte da equipe do LaEPP e LaCOM
(Laboratório de Conservação e Manejo de Recursos Pesqueiros): Monica, Matheus,
Myrna, Samantha, Ivan, Joyce, Jordana, Fernando, e Gilmar, por toda ajuda,
conversas e momentos compartilhados quase que diariamente.
As amizades construídas durante o meu processo de formação dentro do PPG,
em especial a amiga Jessika Neves, pelos momentos de descontração,
principalmente durante as amostragens e horário de almoço.

A Luiz Carlos Lopes, que foi e tem sido um grande suporte e incentivador
durante o final desse processo.
A todos os professores do Programa de Pós-Graduação em Diversidade
Biológica e Conservação nos Trópicos (PPG-DiBiCT) da Universidade Federal de
Alagoas, por todo conhecimento repassado, em especial as Profas. Ana Malhado e
Tami Mott.
Um obrigado muito especial a Juliane (secretária do PPG), que desde o início
me auxiliou e com toda paciência do mundo conseguiu resolver todos os problemas
burocráticos.
Ao Programa Ecológico de Longa Duração Costa dos Corais Alagoas
(PELDCCAL) e a Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior
(CAPES), pelo apoio financeiro.
Agradeço!

“Para onde vão os trens, meu pai?
Para Mahal, Tamí, para Camirí, espaços
no mapa... e depois o pai ria.
Também para lugar algum meu filho.
Tu podes ir e ainda que se mova o trem,
tu não te moves de ti.”
Hilda Hilst

RESUMO
Durante as últimas décadas, ecologistas têm direcionados seus esforços para o
desenvolvimento de estudos que visam a conservação de espécies e
ecossistemas. Ainda assim, vivemos uma das maiores crises da biodiversidade,
com taxas de extinções elevadas e processos de degradação de habitat cada
vez mais rápidos. Tal problemática resulta, em parte, da constante negligência
do conceito multidimensional de biodiversidade, que engloba não apenas quais
e quantas espécies residem em uma determinada área, mas também suas
características fenotípicas, histórias evolutivas e variabilidade de genes. A
compreensão integrada dessas diferentes dimensões, além de seus padrões e
quais processos os regem, é fator determinante para o desenvolvimento de
estratégias efetivas de manejo e conservação, principalmente para ambientes
de alta produtividade e grande importância ecológica, tais como os ambientes
estuarino-costeiros. Sendo assim, o presente trabalho tem como objetivo
desenvolver uma análise integrada dos componentes distintos da diversidade de
peixes estuarino-costeiros em diferentes escalas espaciais. No primeiro capítulo
discutimos como a diversidade de habitats e a sazonalidade de áreas tropicais
atuam de forma sinérgica para manutenção da redundância funcional de áreas
costeiras. O segundo capítulo, por sua vez, avalia a importância relativa de
mosaicos costeiros para diferentes partes das comunidades, identificando as
relações entre variáveis abióticas e guildas ecológicas. Por fim, o terceiro
capítulo, faz uma análise regional das dimensões da biodiversidade de peixes
estuarinos ao longo Atlântico Ocidental, visando a compreensão de processos e
padrões que regem as comunidades ictiícas e sua participação no dinâmica
natural de ambientes estuarino-costeiros.

Palavras-chave: estuários, peixes, biogeografia, biodiversidade

ABSTRACT
During the last decades, ecologists have focused their efforts on the development
of studies aimed at the conservation of species and ecosystems. Even so, we are
experiencing one of the greatest biodiversity crises, with high extinction rates and
increasingly rapid habitat degradation processes. This problem results, in part,
from the constant neglection of the multidimensional concept of biodiversity,
which encompasses not only which and how many species reside in a given area,
but also their phenotypic characteristics, evolutionary histories and gene
variability. The integrated understanding of these different dimensions, in addition
to their patterns and which processes drive them, is a determining factor for the
development of effective management and conservation strategies, especially for
environments of high productivity and great ecological importance, such as
estuarine-coastal environments. Therefore, the present work aims to develop an
integrated analysis of the distinct components of estuarine-coastal fish diversity
at different spatial scales. In the first chapter we discussed how the diversity of
habitats and the seasonality of tropical areas act synergistically to maintain the
functional redundancy of coastal areas. The second chapter, in turn, assesses
the relative importance of coastal mosaics for different parts of communities,
identifying the relationships between abiotic variables and ecological guilds.
Finally, the third chapter makes a regional analysis of the dimensions of estuarine
fish biodiversity along the Western Atlantic, aiming at understanding the
processes and patterns that govern ichthyic communities and their participation
in the natural dynamics of estuarine-coastal environments.
Keyword: estuaries, fish, biogeography, biodiversity

LISTA DE FIGURAS
Figure 1. Study area, showing the three sampled estuarine systems: Manguaba
river estuary (A), Santo Antônio river estuary (B) and Pontal estuary (C).
Sampling stations are represented according to habitat type: mangrove (▲),
seagrass beds (●) and sandy beach (■).......................................................... 40
Figure 2. Variability in the α-component (abundance-weighted) of each diversity
dimension of fish species for habitats and seasons of three tropical estuaries.
The * represents a statistically significant difference between seasons. ......... 45
Figure 3. α and β components of the three diversity dimensions of tropical fish
assemblages among habitats and seasons of three estuarine systems. ........ 46
Figure 4. Taxonomic (A), phylogenetic (B) and functional (C) spaces occupied
by fish assemblages of three tropical estuarine systems across different habitats
(mangrove = red; seagrass = green; sandy beach = blue)) and seasons (dry =
sun symbol; wet = rain symbol). ...................................................................... 47
Fig. 1 Location of sampling sites for each habitat type: mangrove (▲), seagrass
beds (●) and sandy beach (■) in the Manguaba river estuary (A), the santo
Antônio river estuary (B) and the Pontal estuary (C). ...................................... 71
Fig. 2 Variability in the density of individuals of identified estuarine use functional
guilds across habitats and seasons. Plot also shows rainfall data (in mm) for
each month to highlight differences between seasons. SE – solely estuarine;
E&M – estuarine and marine; MED – marine estuarine dependent; MEO –
marine estuarine opportunist; MS – marine straggler ..................................... 75
Fig. 3 Non-metric multidimensional scaling (NMS) ordination plots showing guild
composition in relation to environmental factors. ............................................ 78
Fig. 1 – Map of the Western Atlantic showing the location of the 232 estuarine
systems and coastal lagoons that were analyzed in the present study (A). The
plot also shows the number and percentage of unique and shared species for
all biogeographic realms with the representation of one of the most common
species that was unique in each realm (B). TNA – Temperate Northern Atlanti;
TA – Tropical Atlantic; and TSA – Temperate South America. ..................... 102

Fig. 2 – General Linear Model coefficient estimates (±95% confidence intervals)
showing the magnitude and direction of effects of explanatory variables on each
diversity dimension of estuarine fish species along the Western Atlantic. Blue
dots and lines represent a positive effect, red dots and lines show a negative
effect, and gray dots and lines indicate no significant effect found for the
variable. ......................................................................................................... 102
Fig. 3 – Model coefficient estimates (±95% confidence intervals) showing the
magnitude and direction of effects of explanatory variables on each diversity
dimension of estuarine fish species along the biogeographic realms of the
Western Atlantic: A) Temperate Northern Atlantic, B) Tropical Atlantic, and C)
Temperate South America. SR – species richness, PD – phylogenetic diversity
and FD – functional diversity. Blue dots and lines represent a positive effect, red
dots and lines show a negative effect, and gray dots and lines indicate no
significant effect found for the variable. ......................................................... 104

LISTA DE TABELAS
Table 1. Functional traits used to estimate the functional diversity of fish species
along the sampled systems. ............................................................................ 41
Table 2. Three-way permutational analysis of variance (PERMANOVA) with
1,000 permutations for estuarine fish species data. The analysis was carried out
considering a mixed design with habitats nested in estuaries and crossed with
seasons. .......................................................................................................... 44
Table 1 Estuarine-use functional guilds used to classify fish species collected in
the present study following Potter et al. (2015) ............................................... 72
Table 2 ANOVA results for the variability in the overall density of individuals
across estuarine-use functional guilds, habitats, and seasons ....................... 75
Table 3 PERMANOVA results for the density of estuarine-use functional guilds,
obtained through the Bray–Curtis similarity matrix, showing the partitioning of
multivariate variation and tests by habitats and seasons, as well as their
interaction. SE – solely estuarine; E&M – estuarine and marine; MED – marine
estuarine dependent; MEO – marine estuarine opportunist; MS – marine
straggler .......................................................................................................... 77
Table 4 Multivariate correlations between the environmental variables and
estuarine-use functional guilds, displaying the top model from the BEST output
for each guild, as well as its strength (ρ) and significance (p-value). SE – solely
estuarine; E&M – estuarine and marine; MED – marine estuarine dependent;
MEO – marine estuarine opportunist; MS – marine straggler ......................... 78
Table 1 – Functional traits used to estimate the functional diversity of fish
species along the estuarine systems of the Western Atlantic ......................... 99
Table 2 – Generalized Linear Models fitted to the variation of diversity
dimensions of estuarine fish species from the Western Atlantic, and its
biogeographic realms: total explained deviance (Exp. %), linear regression of
observed and predicted values (r2), total number of samples (n). Biogeographic
realms: TNA – Temperate Northern Atlantic, TA – Tropical Atlantic and TSA –
Temperate South America. ........................................................................... 103

SUMÁRIO
1. APRESENTAÇÃO ...................................................................................... 15
2. REVISÃO DA LITERATURA ...................................................................... 18
2.1. Ambientes estuarino-costeiros e assembleias ictiícas ...................... 18
2.2. Abordagens funcionais e filogenéticas ............................................... 20
2.3. A estrutura funcional de comunidades estuarino-costeiras .............. 22
2.4. Diversidade filogenética ........................................................................ 24
2.5. Referências ............................................................................................. 26
3. CAPÍTULO I: Assessing tropical coastal dynamics across habitats and
seasons through different dimensions of fish diversity ........................... 34
3.1. Introduction ............................................................................................ 36
3.2. Materials and methods .......................................................................... 38
3.2.1. Study area, sample design and fish survey ........................................... 38
3.2.2. Functional traits and species phylogeny ............................................... 40
3.2.3. Data analysis ......................................................................................... 42
3.3. Results .................................................................................................... 43
3.4. Discussion .............................................................................................. 48
3.4.1. Species composition among coastal habitats and seasons .................. 48
3.4.2. Relationship between diversity dimensions throughout the estuarine
dynamics ......................................................................................................... 50
3.4.3. Limitations, current concerns, and implications for conservation .......... 51
3.5. Acknowledgements ................................................................................ 53
3.6. References .............................................................................................. 54
4. CAPÍTULO II: Relative importance of habitat mosaics for fish guilds in
the northeastern coast of Brazil .................................................................. 65
4.1. Introduction ............................................................................................ 67
4.2. Material and methods ............................................................................ 70
4.2.1. Study area and sample design .............................................................. 70
4.2.2. Fish surveys and environmental information ......................................... 71
4.2.3. Data analysis ......................................................................................... 73
4.3. Results .................................................................................................... 74

4.4. Discussion .............................................................................................. 79
4.5. Conclusion .............................................................................................. 83
4.6. Acknowledgments .................................................................................. 83
4.7. References .............................................................................................. 84
5. CAPÍTULO III: Biogeographic patterns in the biodiversity dimensions
of estuarine fish assemblages from the Western Atlantic ........................ 92
5.1. Introduction ............................................................................................ 94
5.2. Materials and methods .......................................................................... 97
5.2.1. Estuarine fish assemblages’ dataset ..................................................... 97
5.2.2. Explanatory variables ............................................................................ 97
5.2.3. Phylogeny and functional traits of fish species ...................................... 98
5.2.4. Diversity dimensions ............................................................................. 99
5.2.5. Data analysis ....................................................................................... 100
5.3. Results .................................................................................................. 101
5.4. Discussion ............................................................................................ 104
5.5. References ............................................................................................ 108
6. DISCUSSÃO GERAL ............................................................................... 118
7. REFERÊNCIAS ......................................................................................... 121
8. ANEXOS ................................................................................................... 123

1. APRESENTAÇÃO
Abordagens funcionais têm emergido como uma das principais
ferramentas no manejo e conservação de espécies e ecossistemas (POOL;
GRENOUILLET; VILLÉGER, 2014; VILLÉGER et al., 2012, 2017). Isso deve-se
ao fato de que componentes funcionais das assembleias, tais como riqueza,
equitabilidade e divergência auxiliam na compreensão de diversos processos
ecológicos, tais como fatores que afetam a estabilidade ecossistêmica, relações
entre biodiversidade e serviços ecossistêmicos, e mecanismos de coexistência
de espécies (DIAZ; CABIDO, 2001; TILMAN, 2001). Ainda assim, o
conhecimento sobre a estrutura funcional de algumas áreas ainda é limitado, até
mesmo para ecossistemas com alta produtividade e de alta importância
ecológica. Um exemplo disso, embora não seja o único, é a baixa quantidade de
informações que temos sobre a estrutura funcional de ambientes estuarinocosteiros (BAPTISTA et al., 2015; DOLBETH et al., 2016a; SILVA-JÚNIOR et al.,
2017).
Estuários e habitats costeiros estão entre os ecossistemas mais
produtivos da terra, contribuindo com diversos serviços ecológicos, econômicos
e ecossistêmicos. Além de estarem diretamente relacionados com a manutenção
de populações futuras de diversas espécies (BECK et al., 2003; DOLBETH et
al., 2008), estes ambientes apresentam uma conexão direta com ecossistemas
adjacentes (CLAUDINO et al., 2015), criando corredores que permitem o fluxo
intenso de transição entres os ambientes marinhos, estuarinos e de água doce.
Essa

dinamicidade

complexa

criada

por

essa

conectividade

ecossistêmica afeta a composição taxonômica e até mesmo funcional destas
áreas. Por exemplo, o trabalho de Passos et al. (2016) discute que a extensão
de condições estuarinas para áreas marinhas tem alterado a estrutura funcional
de comunidades de peixes demersais nos trópicos, ressaltando a importância de
uma melhor compreensão sobre a estrutura funcional de assembleias de peixes
estuarinos e análises mais detalhadas sobre essa conexão entre estuários e
áreas adjacentes.

Uma vez que a dinamicidade de ecossistemas estuarinos causa
alterações constantes na composição específica das assembleias ictiícas (DA
SILVA et al., 2018), entender o arranjo funcional destas comunidades parece ser
um componente chave para o manejo e conservação eficaz das espécies e
destes ambientes. Especificamente, uma análise dos traços que as espécies
estuarinas possuem e como as funções são desempenhadas por estas espécies
em tais ecossistemas é necessária para que possamos compreender os
processos ecossistêmicos. Porém, para a caracterização de padrões na
estrutura destas assembleias é necessária uma compreensão prévia e ampla
dos fatores que podem influenciar a dinâmica funcional das espécies ictiícas.
Sendo assim, o estudo integrado das diferentes dimensões da biodiversidade de
peixes em ambientes estuarino-costeiros deve ser realizado em diferentes
escalas espaciais.
Por exemplo, o trabalho de Henriques et al. (2017) mostra que barreiras
biogeográficas, tais como correntes oceânicas e condições climáticas distintas
(ex.: temperatura e precipitação) afetam não apenas a composição e riqueza de
espécies, mas também a distribuição dos seus traços funcionais. Já em escalas
mais finas (regionalmente e localmente falando) uma outra gama de fatores, tais
como forma do estuário, tipo de conectividade com ambientes costeiros e
variações sazonais em salinidade e temperatura atuam mais ativamente na
estruturação funcional das comunidades estuarinas (DOLBETH et al., 2016a;
SILVA-JÚNIOR et al., 2017). Isso ocorre porque a transição entre escalas
resulta em passagens hierárquicas de reino para províncias biogeográficas, que
por sua vez são definidas por características distintas de produtividade, vazão,
entre outras condições ambientais.
Porém, é importante ressaltar que não apenas fatores abióticos estão
atrelados com os processos que influenciam a estrutura funcional destas
assembleias. A história evolutiva das espécies pode ter um papel determinante
na distribuição de traços e grupos funcionais, influenciando assim as funções
ecossistêmicas desempenhas por estas espécies (PAVOINE; BONSALL, 2011).
Tal característica deve-se ao fato que sinais filogenéticos podem ter uma estreita

relação com a conservação de traços de espécies durante sua história evolutiva,
moldando a estrutura taxonômica e funcional existente (FLYNN et al., 2011).
Além disso, processos de especiação e dispersão são capazes de introduzir
novas espécies a comunidades já estabelecidas, podendo alterar a dinâmica das
comunidades e a funcionalidade de todo o ecossistema, além de criar uma
conexão entre diferentes escalas espaciais (VELLEND, 2010).
A diversidade de fatores que influenciam as diferentes dimensões da
diversidade faz com que seja necessário um estudo que considere diferentes
escalas espaciais (ex.: global e regional) e incluam em suas análises além de
fatores abióticos (ex.: condições ambientais, estrutura do estuário e etc) as
relações filogenéticas entre as espécies, fornecendo assim um conjunto de
informações que nos permita direcionar esforços para a conservação das
espécies e do ecossistema estuarino como um todo. Sendo assim, o presente
trabalho tem como objetivo analisar as dimensões da diversidade de peixes em
ambientes estuarino-costeiros em diferentes escalas espaciais, visando a
compreensão de padrões e os processos que regem não apenas a estruturação
das comunidades nessas áreas, mas também a funcionalidade ecossistêmica
desses ambientes.

2. REVISÃO DA LITERATURA
2.1. Ambientes estuarino-costeiros e assembleias ictiícas
Ambientes estuarino-costeiros são zonas de transição entre o ambiente
marinho e de água doce, onde a mistura de massas d’água de diferentes
densidades causa grandes variações dos parâmetros físicos e químicos destes
habitats criando um ecossistema complexo e bastante dinâmico (BIANCHI,
2007). Esta complexidade estrutural associada ao influxo contínuo de nutrientes
proveniente de ambientes aquáticos continentais confere a estes ecossistemas
altos níveis de produtividade e abrigo para indivíduos juvenis (AZEVEDO;
BORDALO; DUARTE, 2014; SCHELSKE; ODUM, 1962), sendo utilizados por
diversas espécies em pelo menos uma parte do seu ciclo de vida. Além disso,
estudos têm evidenciado que tais ecossistemas estão diretamente relacionados
com a sobrevivência e manutenção de populações futuras, uma vez que várias
espécies de peixes (BECK et al., 2003; DA SILVA et al., 2018), crustáceos
(MARTINS; RODRIGUES; KINAS, 2014) e outros organismos, tais como aves e
anfíbios (BRANCO, 2000; GROSE; HILLEBRANT; CREMER, 2013) dependem
desses

ambientes

para

alimentação,

reprodução

e/ou

crescimento

(NAGELKERKEN et al., 2015).
Por serem ambientes dinâmicos, as comunidades biológicas que habitam
tais ambientes usualmente sofrem constantes mudanças em sua estrutura. Isso
ocorre porque diversos fatores bióticos e abióticos influenciam a composição e
abundância de espécies nestes ecossistemas, tais como interações intra e
interespecíficas (ELLIOTT et al., 2007), salinidade (BARLETTA et al., 2005),
temperatura (HARRISON; WHITFIELD, 2006), turbidez (OOI; CHONG, 2011) e
disponibilidade de alimento (GRENOUILLET; PONT; SEIP, 2002). Contudo, a
estrutura básica de alguns grupos se mante relativamente estável, apesar das
mudanças recorrentes que ocorrem na composição específica. Por exemplo,
assembleias de peixes estuarinos geralmente são compostas por um conjunto
de espécies de água doce, marinhos migrantes e residentes que utilizam tais
ecossistemas em pelo menos uma parte do seu ciclo de vida (SELLESLAGH et
al., 2009).

Os peixes são um grupo de grande particularidade em estuários e habitats
costeiros, pois muitas espécies marinhas e de água doce, incluindo espécies de
alto valor econômico, utilizam essas áreas como berçários e/ou criação (BECK
et al., 2003). Historicamente, a estrutura de assembleias ictiícas destas áreas
tem sido alvo de diversos estudos ecológicos (ABLE, 2005; ELLIOTT;
MCLUSKY, 2002), o que tem ajudado na compreensão de processos e fatores
que afetam a composição especifica destas assembleias no tempo e espaço
(BARLETTA et al., 2008; BLABER; GRIFFITHS; PILLANS, 2010; MÉRIGOT et
al., 2017). Por exemplo, diversos trabalhos têm evidenciado que os fatores
estruturantes da ictiofauna estuarina são variados, tais como as características
físicas do próprio estuário como tamanho, profundidade e grau de conectividade
com o ambiente marinho (RUEDA; DEFEO, 2003), os padrões climáticos
regionais, principalmente as flutuações nas taxas de pluviosidade e temperatura
(DA SILVA et al., 2018) e condições locais, como nível de produtividade e
variação da salinidade (BARLETTA et al., 2005). Os peixes respondem a este
conjunto de fatores por aclimatação ou migração sazonal, fazendo com que as
assembleias ictiícas sejam marcadas por constantes mudanças em sua estrutura
taxonômica com um número grande de espécies que passam um curto período
de tempo nestes ambientes, e um número reduzido de espécies que apresentam
permanência anual (ELLIOTT et al., 2007; GIBSON et al., 1996; PATERSON;
WHITFIELD, 2000).
Contudo, ainda que a produção científica sobre a estrutura de
assembleias de peixes estuarinos seja relativamente extensa, lacunas em
alguns campos de conhecimento ainda existem, fazendo com que exista uma
falta de informação que é crucial para a conservação destes ecossistemas como
um todo (BLABER; BARLETTA, 2016). Por exemplo. apenas alguns trabalhos
recentes têm utilizados abordagens que integrem o conhecimento taxonômico
com a funcionalidade ecossistêmica, tal como a caracterização funcional de
assembleias de peixes estuarinos (DOLBETH et al., 2016b; HENRIQUES et al.,
2017; MÉRIGOT et al., 2017; SILVA-JÚNIOR et al., 2017). Menor ainda é o
número de estudos que especializam tais análises, uma vez que estuários e

habitats costeiros podem estar conectados em um mosaico de habitat que
funciona de forma interdependente. Uma vez que a dinamicidade destes
ecossistemas causa alterações constantes na composição específica das
assembleias, entender as funções desempenhadas pelas espécies destas
comunidades parece ser um componente chave para o manejo e conservação
eficaz das espécies e destas regiões, já que mudanças funcionais na estrutura
das assembleias podem afetar diretamente a funcionalidade dos ecossistemas.
Um bom exemplo é o trabalho recente de Passos et al. (2016) que mostra
que extensão das condições estuarinas para o ambiente marinho influencia até
mesmo a estrutura funcional de áreas costeiras adjacentes, criando corredores
que permitem a migração de espécies estuarinas com traços funcionais distintos
para áreas mais profundas. Isso ocorre porque muitos estuários possuem uma
conexão direta com o ambiente marinho. O problema é que diversos autores têm
pontuado que as atuais mudanças que sistemas naturais têm sofrido no mundo
todo podem estar afetando negativamente a conectividade biológica entre
diferentes ecossistemas, colocando em risco a diversidade de comunidades
biológicas e a sobrevivência de populações futuras de muitas espécies
(SELLESLAGH; AMARA, 2008; SHEAVES, 2005). Parte do problema resulta da
falta de um conhecimento mais aprofundado e detalhado de como está conexão
ocorre e é mantida (DE JONGE; ELLIOTT; BRAUER, 2006). Por exemplo,
Vasconcelos et al. (2011) em seu estudo discutem como a abordagem tradicional
de estruturação e quantificação das comunidades biológicas utilizada em
diversos estudos para se avaliar a conectividade entre ecossistemas não fornece
informações suficientes sobre os mecanismos que permitem que essa
conectividade exista, sendo necessária a implementação de abordagens
ecossistêmicas e funcionais em tais trabalhos.

2.2. Abordagens funcionais e filogenéticas
Nas últimas décadas, abordagens funcionais têm emergido como uma
das principais ferramentas de estudos ecológicos que visam o manejo e

conservação de espécies e ecossistemas (KANG et al., 2015; TERESA;
CASATTI; CIANCIARUSO, 2015; VILLÉGER; GRENOUILLET; BROSSE, 2013).
Isso ocorreu porque abordagens baseadas em características comportamentais,
fisiológicas ou morfológicas que impactam a adaptabilidade dos indivíduos
(VIOLLE et al., 2007) têm um alto poder preditivo sobre o funcionamento dos
ecossistemas, a estrutura de comunidades biológicas e relações espécieambiente (MESSIER; MCGILL; LECHOWICZ, 2010; TILMAN, 2001). Por
exemplo, a diversidade de funções desempenhadas pelas espécies, conhecida
como diversidade funcional, tem sido de grande importância para a
compreensão das relações entre biodiversidade e serviços ecossistêmicos,
como também dos mecanismos de coexistência de espécies (DIAZ; CABIDO,
2001; TILMAN, 2001).
Historicamente, diversas hipóteses foram formuladas na tentativa de se
compreender a relação entre diversidade de espécies e o funcionamento de um
determinado ecossistema (KANG et al., 2015). Tais hipóteses, usualmente, são
atreladas principalmente a participação das espécies na cadeia trófica (KANG et
al., 2015; WANG; BROSE, 2018), uma vez que a transferência de energia é um
componente principal da funcionalidade ecossistêmica. Por exemplo, uma das
teorias mais conhecidas e estudadas é a hipótese da diversidade-estabilidade
postulada por MacArthur (MACARTHUR, 1955) que relaciona alta diversidade
de espécies com máxima estabilidade ecossistêmica. Para MacArthur (1955), a
estabilidade de sistemas naturais é alcançada pelo aumento no número de
espécies, uma vez que tal incremento faz com que um maior número de nichos
tróficos disponíveis no ecossistema seja ocupado. Ou seja, quanto mais funções
são desempenhadas pelas espécies mais resiliente será o ecossistema.
Contudo, trabalhos posteriores mostraram que a relação entre diversidade e
estabilidade ecossistêmica é bem mais complexa, uma vez que fatores como a
capacidade que a comunidade tem de suportar diferentes espécies e grupos
funcionais são bem mais significativos na determinação dos processos e
estabilidade dos ecossistemas do que o apenas a diversidade de espécies
(MCCANN, 2000).

Embora muitos estudos tenham mostrado uma relação positiva entre a
riqueza de espécies e a diversidade de funções (DIMITRIADIS; KOUTSOUBAS,
2011), um debate acerca das similares entre diferentes espécies emergiu nos
anos 90, fazendo com que novas perspectivas nascessem dentro do estudo das
relações entre espécies e funções. Com isso, entender padrões sobre a estrutura
funcional de comunidades biológicas e sua relação com os ecossistemas tem
cada vez mais se tornado o objetivo de diversos estudos, na tentativa de elucidar
questões cruciais no ramo da ecologia (BELLWOOD; HOEY; CHOAT, 2003;
TILMAN et al., 1997; UMAÑA et al., 2017). Neste contexto não é surpreendente
que tenha acontecido um aumento expressivo na produção científica acerca da
estrutura funcional de diversos grupos em ecossistemas variados, além do
desenvolvimento de novas métricas (BOTTA-DUKÁT, 2005; PETCHEY;
GASTON, 2002, 2006). Ainda assim, lacunas de conhecimento sobre alguns
grupos de espécies, tais como os peixes, são comuns e geralmente dificultam o
desenvolvimento de medidas eficientes de conservação.

2.3. A estrutura funcional de comunidades estuarino-costeiras
Embora estuários sejam um dos ambientes mais produtivos do mundo,
contribuindo com diversos serviços ecossistêmicos (HARLEY et al., 2006),
existem poucos trabalhos que utilizam abordagens funcionais para avaliar as
comunidades biológicas estuarinas e sua relação com o ecossistema (DOLBETH
et al., 2016a; MICHELLI; HALPERN, 2005; SILVA-JÚNIOR et al., 2017). Uma
constante dificuldade para a realização de tais estudos com comunidades ictiícas
é a atual quantidade limitada de informação sobre traços funcionais de peixes
(ALBOUY et al., 2011; SIBBING; NAGELKERKE, 2001). Por exemplo, não existe
uma classificação detalhada sobre quais traços funcionais das assembleias
ictiícas respondem a variações do ambiente (traço resposta), e quais são os
atributos que interferem na dinâmica ecossistêmica – (traço efeito) (VIOLLE et
al., 2007). Estas informações são de importância análises mais detalhadas sobre
a variabilidade de respostas que ocorrem dentro de um conjunto de espécies
que desempenham funções similares (grupo funcional), e consequentemente

são necessárias para a compreensão das relações entre as comunidades e os
serviços ecossistêmicos (LALIBERTÉ et al., 2010).
Os poucos trabalhos existentes sobre a estrutura funcional de
assembleias de peixes estuarinos têm fornecido dados importantes para
entendimento das relações espécies-ambiente e sobre resiliência ecossistêmica.
O estudo de Baptista et al. (2015) ao analisar a mudança na estrutura funcional
nas comunidades ictiícas de um estuário em Portugal durante 30 anos revelou
que ao longo do tempo, embora diferentes espécies transitaram pelo estuário, a
funcionalidade ecossistêmica se manteve estável graças a alta redundância
funcional entre as espécies que habitam tais ambientes. Ou seja, apesar das
constantes alterações na composição específica, as funções desempenhadas
pelas espécies ictiícas tendem a serem mantidas para promover resiliência
ecossistêmica.

Padrões

similares

foram

encontrados

trabalhos

desenvolvidos em estuários no nordeste do Brasil, onde estuários com baixa
redundância funcional se mostram mais sensíveis a impactos naturais e/ou
antropogênicos (DOLBETH et al., 2016a).
Porém, qual os fatores que afetam a estrutura funcional de peixes
estuarinos e o que pode causar redundância? Assim como na estrutura
taxonômica, uma variedade de fatores pode influenciar a composição funcional
de assembleias ictiícas, tais como ações antropogênicas (DOLBETH et al.,
2016a), características geomorfológicas do estuário (HENRIQUES et al., 2017)
e variações nas condições ambientais locais (PASSOS et al., 2016). O estudo
recente de Henriques et al. (2017) merece um destaque pois foi o primeiro a
incluir barreiras biogeográficas como variável explicativa da distribuição
funcional das assembleias ictiícas. De fato, os autores mostram que existe uma
vasta amplitude de fatores que estão diretamente relacionados com a
estruturação funcional dos estuários, tais como variações de salinidade e
produtividade, tamanho do ecossistema estuarino, conectividade hidrológica
com áreas adjacentes, entre outros.
Contudo, embora características relacionadas com a divisão das regiões
biogeográficas marinhas (correntes oceânicas, variação climática, e etc

(SPALDING et al., 2007) – assim como a existência de filtros ambientais – ex.:
variação em salinidade, produtividade e etc. – sejam fatores importantes para a
estruturação das assembleias ictiícas, um componente que em muitos estudos
é negligenciado é a própria história evolutiva das espécies. A história filogenética
das espécies pode ter uma forte relação com as funções desempenhadas nos
ecossistemas (FLYNN et al., 2011), e em muitos casos atributos importantes
para a montagem e interação das assembleias são usualmente conservados
durante a história evolutiva das espécies. Sendo assim, para uma melhor
compreensão dos fatores estruturantes de comunidades de peixes estuarinos é
necessária uma análise que englobe diferentes escalas de tempo e espaço, além
da inclusão de análises filogenéticas na tentativa de elucidar se a estrutura
funcional destas assembleias é produto da história evolutiva das espécies, de
filtragem ambiental ou uma conjunção de ambos.

2.4. Diversidade filogenética
A diversidade filogenética ganhou espaço em estudos ecológicos
principalmente no início da década de 1990 com a crescente necessidade de se
estabelecer prioridades para a conservação (CIANCIARUSO; SILVA; BATALHA,
2009; MAY, 1990). Tal abordagem incorpora em suas análises as relações
filogenéticas das espécies, partindo da premissa que comunidades com
espécies filogeneticamente mais distintas são mais biodiversas que aquelas que
possuem espécies com parentescos próximos (MAGURRAN, 2004; WILLIAMS;
HUMPHRIES; VANE-WRIGHT, 1991). Particularmente, esta análise reconhece
que árvores filogenéticas refletem as diferenças fenotípicas, genéticas e
comportamentais entre diferentes linhagens evolutivas (TUCKER et al., 2017).
Sendo assim, espera-se que extinções de espécies não-aparentadas gerem uma
maior perda de informação filogenética na comunidade do que a extinção de uma
espécie com parentescos próximos, fazendo com que a identificação de áreas
com maior diversidade filogenética seja uma estratégia eficaz para a
conservação das espécies e dos ecossistemas como um todo (MOUQUET et al.,
2012; POLASKY et al., 2001).

No geral, as medidas de diversidade filogenética se mostram bastantes
eficientes na compreensão dos processos de estruturação de comunidades,
permitindo que as interações que levam a coexistência de espécies sejam mais
bem compreendidas (WEBB et al., 2002). Isso deve-se, principalmente, ao fato
de que tais interações podem ser resultado de uma variedade de fatores,
incluindo os processos evolutivos passados e contínuos (CHASE, 2003; WEBB
et al., 2002). No entanto, embora sua aplicabilidade seja abrangente, tal
ferramenta ainda é pouco utilizada, principalmente no ramo da zoologia, onde
existe uma grande escassez de informações sobre a diversidade filogenética de
comunidades naturais (CIANCIARUSO; SILVA; BATALHA, 2009).
Um dos grandes desafios, por exemplo, é a definição das diferentes
características entre espécies que pode explicar padrões de estruturações de
comunidades (MOUQUET et al., 2012). Embora diversos trabalhos tenham
utilizado a diversidade filogenética para identificar os processos ecológicos que
determinam padrões de distribuição e diversidade de espécies (JETZ et al.,
2012), Tucker et al. (2017) discute que o uso de análises filogenéticas em
ecologia de comunidade e em estudos de conservação ainda é bastante
subestimado. Por exemplo, a integração de análises filogenéticas com
abordagens funcionais parece ser de extrema importância para a compreensão
de regras de montagem de comunidades, principalmente porque as relações
entre atributos funcionais, hábito alimentar e funções desempenhadas pelas
espécies podem ser produto das afinidades filogenéticas entre espécies (DINIZFILHO et al., 2011; PAVOINE; BONSALL, 2011). De fato, a diversidade
filogenética tem sido até mesmo utilizada como um proxy em estudos de ecologia
funcional utilizando a similaridade/dissimilaridade entre espécies como
ferramenta para identificar funções (MOUQUET et al., 2012; WEBB et al., 2002).
Estudos que combinam abordagens funcionais e filogenéticas têm
mostrado alto potencial para identificação e priorização de espécies-chave, e
para predições de respostas e da suscetibilidade das comunidades biológicas
frente as mudanças globais (LAVERGNE et al., 2010; THUILLER et al., 2011),
fornecendo informações cruciais para a conservação de ecossistemas e

espécies. Além disso, a união de ambas as abordagens tem permitido a
identificação dos processos de estruturação de assembleias, mostrando que
filtros ambientais e a história biogeográfica podem atuar de formas distintas na
distribuição de diferentes grupos (LEIBOLD; ECONOMO; PERES-NETO, 2010).

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3. CAPÍTULO I: Assessing tropical coastal dynamics across habitats and
seasons through different dimensions of fish diversity1

Victor Emmanuel Lopes da Silva¶*; Marina Dolbeth¶¶; Nidia Noemi Fabré¶

Laboratório de Ecologia, Peixes e Pesca – Instituto de Ciências Biológicas e da

Saúde, Universidade Federal de Alagoas, Maceió, Brazil
¶¶

Interdisciplinary Centre of Marine and Environmental Research - CIIMAR,

Universidade do Porto, Matosinhos, Portugal

*Corresponding author: lopesdasilvavictor@gmail.com

Abstract
Coastal habitat mosaics are among the most productive ecosystems around the
globe, with many ecological and social-economic services provided. Their natural
challenging conditions have always been a subject of concern for ecologist and
conservationist, with a particular interest in understanding how its spatial and
temporal dynamics influence ecosystem functioning. In this context, we aimed to
assess tropical coastal dynamics using an integrative approach, measuring the
different facets of fish diversity across space (habitats) and time (seasons). Three
different estuarine systems and their adjacent areas in the southwestern Atlantic
were monthly sampled between July 2017 and June 2018, in a sampling design

Artigo publicado na revista Marine Environmental Research (Qualis A1, percentil 91%) em

agosto de 2021. DOI: 10.1016/j.marenvres.2021.105458

that encompassed three different coastal mosaics with three habitat types
(mangroves, seagrass and sandy beaches), and both seasons of the studied
region (dry and rainy). Taxonomic, phylogenetic, and functional diversity were
then evaluated with equivalent diversity measures to allow comparisons between
them. Different patterns of species occurrence and distribution were found
between habitats and seasons, which resulted in different effects on the
abundance-weighted diversity dimensions. Although taxonomic diversity of
habitats was greater during the rainy season (p=0.03), a seasonal increase in
phylogenetic diversity was only observed in the sandy beach habitat (p=0.04). In
contrast for the functional diversity, no significant differences were found among
habitats in both seasons (p=0.15), indicating high levels of redundancy. Our
results showed that patterns in the occurrence and abundance of tropical fish
species among habitats that comprise a coastal mosaic have different effects on
distinct diversity dimensions. More precisely, for tropical coastal systems with
marked seasonality, both habitats and season appear to play a synergic role in
the maintenance of ecosystem functioning by enhancing functional and
phylogenetic redundancy.

Keywords: biodiversity dimensions; Fish Ecology; tropical estuaries

3.1. Introduction
Identifying priority habitats for conservation has always been one of the
main goals of ecologists and conservationists worldwide (Wilson et al., 2006; Xu
et al., 2019). The increasing number of threats to species and greater impacts on
ecosystems have stimulated the development of different and complex
prioritization strategies to identify areas of interest for protection and conservation
(Pereira et al., 2012). However, despite all the work done, indicators still show
huge losses of biodiversity and ecosystem services across many scales (Butchart
et al., 2010; Velazco et al., 2019), with current extinction rates and habitat
degradation often compared to the five previous mass extinction events in the
last 600 million years (Stork, 2010).
According to Ceauşu et al. (2015), many factors play a significant role in
the loss of species and ecosystem services. Nevertheless, one major issue lies
in how current methodologies to prioritize conservation measurements are
designed and implemented. To date, most conservation approaches are still
typically based on one single component of biodiversity (Doxa et al., 2016),
neglecting its multidimensional concept that includes species, evolutionary
entities, functional traits and genetic diversity of taxa that inhabit a particular
region (Mazel et al., 2014). So, identifying successful strategies for ecosystems’
conservation implies embracing all biodiversity facets since their protection is
critical for maintaining the ecosystems’ functions and their essential services to
humans (Pollock et al., 2017). Nevertheless, the poor understanding of how
diversity dimensions are related to each other may result in conservation actions
proposed only through species-based indicators, which encompass species
richness and their vulnerability, but neglect their evolutionary and functional
information (Brum et al., 2017; Ouchi-Melo et al., 2018).
In coastal areas, for example, only a few recent studies have used
integrative approaches to analyze different diversity components (Dolbeth et al.,
2016; Henriques et al., 2017b; Mérigot et al., 2017). The high structural
complexity of these areas makes them one of the most intricate and productive

ecosystems on earth, providing multiple ecological and economic services, such
as their well-established nursery function for many species (Elliott and Whitfield,
2011; Nagelkerken et al., 2000). The planning and management of coastal
ecosystems have always been complex due to their challenging natural
conditions and great structural complexity (Blaber and Barletta, 2016). For
instance, habitat diversity found within these areas creates a coastal ecosystem
mosaic that is often credited as a critical component of higher productivity levels
and unique diversity profiles (Eggleston et al., 1999; Ferreira et al., 2019;
Nagelkerken et al., 2015; Sheaves, 2009). Each habitat that comprises the
coastal mosaic has its own dynamics and may have different roles for species in
the same community (Nagelkerken et al., 2015). However, the effects of this
habitat heterogeneity on ecosystem functioning and filtering mechanisms are still
poorly understood (but see Dolbeth et al. 2013, 2016), especially when
considering seasonal changes (Blaber and Barletta, 2016).
In tropical regions, for example, seasonality driven by rainfall regimes
tends to cause pronounced changes in environmental conditions and habitats’
structure of coastal areas (Passos et al. 2016), having a direct impact in the
shaping and structuring of fish assemblages. The greater inputs of freshwater
and sediments during rainy months modify productivity levels and environmental
conditions, creating additional seasonal changes in salinity, turbidity and
dissolved oxygen levels, which affect species and habitats (Barletta-Bergan et
al., 2002; Neto et al., 2014). In seagrass beds, their total coverage and biomass
tend to decrease with higher rates of rainfall and greater water turbidity (Koch et
al., 2007), which may cause a few fish species to migrate to adjacent areas in
their search for shelter (Nagelkerken et al., 2015). Estuarine and coastal sandy
beaches’ dynamics also change seasonally, with stronger wave action during the
rainy season that produces a constant remineralization process of organic matter
and makes a greater quantity of nutrients in the water column available, attracting
new species to this habitat (Santana et al., 2013).
Few studies have shown that seasonal changes in species composition
appear not to affect the functioning of these areas due to high functional

redundancy among fish species (da Silva and Fabré, 2019; Dolbeth et al., 2016).
Yet, these did not consider habitat-specific approaches nor how diversity
dimensions relate to each other through space and time to understand their
consequences on ecosystem functioning. Therefore, the present study aimed to
understand the relationship between diversity dimensions of fish assemblages
across habitats and seasons of costal mosaic systems, to provide subsidies for
effective management and conservation actions for species and the ecosystem
as a whole. Specifically, we conducted an integrative approach to assess the
individual and synergic effects of temporal and spatial changes on species
composition, phylogenetic lineages, and the functional diversity of fish species of
three tropical coastal mosaics and their main habitats.

3.2. Materials and methods
3.2.1. Study area, sample design and fish survey
Sampled areas were chosen based on their ecological and socioeconomic
importance for the region (Oliveira and Kjerfve, 1993; Paulino et al., 2020). Three
distinct systems of the southeastern Atlantic region were included in this study
(Fig. 1). The region is characterized by a tropical, semi-humid climate with two
well-defined seasons driven by rainfall: a dry season between October and April,
and a rainy season from May to September. The first two sampled areas are
located within one of the most important marine protected areas (MPA) of Brazil
– the Área de Proteção Ambiental Costa dos Corais (APACC), with 400,000 ha
of extension that host approximately 120 km of mangroves, sandy beaches, coral
reefs, and other ecosystems. The third habitat mosaic is located on the MundaúManguaba Estuarine Lagoon Complex, one of the most productive estuarine
systems in northeastern Brazil (Oliveira and Kjerfve, 1993).
All three areas have a variety of habitats within their extensions which
present distinct habitat configurations (Fig. 1). Among them, three typical habitat
types were sampled during the study period: mangroves, seagrass beds and

sandy beaches. Previous studies have analyzed features of these habitat types
individually throughout the region, showing that despite being displayed in
different habitat configuration in sampled systems, each habitat type has a
specific dynamic, with only small changes in environmental conditions occurring
from one system to another (Azevedo-Farias et al., 2021; Barros and RochaBarreira, 2014; da Silva et al., 2018; Paulino et al., 2020; Teixeira, 1997).
Mangrove sites were set in regions close to the estuaries’ banks covered with
mangrove forest dominated by Rhizophora mangle, Avicennia schaueriana, and
Laguncularia racemose. Seagrass stations (mainly comprised of Halodule
wrightii) were all selected in relation to their proximity to the estuaries’ mouths.
Sandy beach stations were all established in the shallow waters adjacent to the
estuaries’ mouth (mean depth ≤ 1.5 m).
Two sampling stations per habitat type were set in each area, resulting in
18 sampling stations that were surveyed monthly from July 2017 to June 2018.
In each sampling station, we conducted two standardized surveys per month
using a beach seine 12 m long and 3 m high with a mesh size of 12 mm and
opposite knots, comprising a total of 438 samples. Each sampling procedure
lasted for five minutes to minimize impacts on local communities (De Araujo et
al., 2008) and all collected fishes were taken to the laboratory for identification at
species level following regional taxonomic keys.

Figure 1. Study area, showing the three sampled estuarine systems: Manguaba
river estuary (A), Santo Antônio river estuary (B) and Pontal estuary (C).
Sampling stations are represented according to habitat type: mangrove (▲),
seagrass beds (●) and sandy beach (■).

3.2.2. Functional traits and species phylogeny
A combination of seven traits that describe well-known functions
performed by fish species was selected for this study (see Table 1 for information
on traits). Selected traits are mainly related to fish diet and movement, having a
solid relationship with species performance, such as detection and capture of
food items, swimming efficiency, and metabolic allocation of energy in the body
(Henriques et al., 2017b). Information was mainly retrieved from published

datasets (Beukhof et al., 2019) and online databases such as FishBase (Froese
and Pauly, 2020). For species that were not included in these databases, we
searched trait information on available literature.

Table 1. Functional traits used to estimate the functional diversity of fish
species along the sampled systems.
Trait

Ecological meaning

Reference

Maximum body size

Reflects position in the food web,

Henriques et al., (2017b)

metabolic rates, dispersal ability,
mobility and home range
Body shape

Indicates swimming performance,

Ribeiro et al., (2016)

and patterns in habitat use
Habitat association

Relates to the use of water-

Beukhof et al., (2019)

column, and adaptations to
habitats
Salinity preference

Reflects the physiological ability

Henriques et al., (2017b)

to deal with osmotic stress in
brackish estuarine waters
Trophic guild

Relates to the position in the food

Henriques et al., (2017b)

web, and shows the influence of a
species on abundance of others
Feeding mode

Reflects feeding strategies and it

Floeter et al., (2018)

is also associated to species diet
Reproductive guild

Indicates dispersal ability,

Lefchech &Duffy, (2015)

colonization potential, and
population growth

Phylogenetic analyses of species were carried out based on the current
taxonomy of fishes (Betancur-R et al., 2017). A total of 100 trees were retrieved
using the package “fishtree” in the software R statistics (Chang et al., 2019),
which provide access to sequences, phylogenies, fossil calibrations and
diversification rate estimates for ray-finned fishes from the Fish Tree of Life

website (https://fishtreeoflife.org). All 100 phylogenetic topologies were used to
build a final Majority-Rule Consensus Tree using the package “phytools” (Revell,
2020).

3.2.3. Data analysis
Differences in species composition between ecosystems and among
habitats and seasons were tested by permutational analysis of variance
(PERMANOVA), considering a 3-way mixed design with habitats (with 3-levels)
nested in estuaries (with 3-levels) and crossed with seasons (with 2-levels)
(Anderson et al. 2008). Significant results were further investigated by a post-hoc
test using the function “pairwise.adonis” in the pairwiseAdonis package (Martinez
Arbizu, 2020). The dimensions of diversity were then evaluated for each habitat
and season with equivalent diversity measures to allow comparisons between
them (de Bello et al., 2009). Fish taxonomic diversity was estimated through the
Simpson’s index (D’), whereas the phylogenetic and functional diversities were
assessed by Rao’s quadratic entropy (RaoQp and RaoQf). All indexes were used
for partitioning diversity into their α and β components, considering all sampling
sites in each habitat and season. The partitioning of diversity assumed an
additive relationship between the α and β components, with α representing the
within-community of each site, and β-diversity evaluating the degree of change
in species composition among communities (Lande, 1996; Whittaker, 1972).
Differences in the α-component of all dimensions between habitats and season
were evaluated using the Scheirer-Ray-Hare extension of the Kruskal-Wallis test
(Sokal and Rohlf, 1995).
Additionally, we performed principal coordinate analyses (PCoAs) using
species data to provide specific typologies of each diversity dimension for
habitats and seasons (Weithoff, 2003). As each diversity dimension considers
different data types, PCoAs were carried out using distinct similarity matrix for
each dimension. For the taxonomic space, a Bray-Curtis distance was applied to

a species-abundance matrix, which included the total abundance of species in all
samples per habitat and season. The phylogenetic space was produced from the
reconstructed phylogenetic topology of species using the cophenetic distance
(Munch and Stefanou, 2019; Sobral et al., 2016), and for the functional space,
we used the Gower distance in a species-traits matrix, which incorporated data
of all species and traits (Pavoine et al., 2009). The first two PCoA axes were used
to create bidimensional spaces for each diversity dimension, and spaces were
used to identify species and/or groups responsible for significant changes across
habitats and seasons.
All diversity measures were carried out within the R software (R Core
Team 2012), using the ‘Rao’ function of de Bello et al. (2010).

3.3. Results
A total of 2,668 individuals, distributed in 86 species of 30 families, were
collected during the study period. In terms of species richness, the most
representative habitat during the dry season was the seagrass (42 species),
followed by mangroves (36) and sandy beaches (29). This pattern shifted in the
rainy season, with sandy beach areas (44) being richer than seagrass beds (40)
and mangroves (34). Although all three areas had a similar species composition
(Table 2, PERMANOVA, p>0.05), different patterns of species occurrence and
distribution were found between habitats and seasons. For instance, species
composition was significantly different among habitats during the dry season, with
each habitat having its own pool of species (Table 2, PERMANOVA, p=0.01). In
the rainy season, however, sandy beach and seagrass habitats shared a similar
species composition (post-hoc test, p=0.53) which was significantly different from
the one found in mangrove areas (post-hoc test, p=0.01).
The seasonal and spatial patterns on species richness also resulted in
different effects on the abundance-weighted diversity dimensions. Although αtaxonomic diversity of all habitats was greater during the rainy season in

comparison to the dry season (Fig. 2a, Scheirer-Ray-Hare test, p=0.03), a
seasonal increase in α-phylogenetic diversity was only observed in the sandy
beach habitat (Fig. 2b, Scheirer-Ray-Hare test, p=0.04). In contrast for the αfunctional diversity, no significant differences were found among habitats in both
seasons (Fig. 2c, Scheirer-Ray-Hare test, p=0.15). When diversity was
partitioned, the β-component of taxonomic diversity was consistently greater than
the α-component, indicating a high turnover of species in all habitats and seasons
(Fig. 3). However, these changes in species composition did not greatly impact
the β-phylogenetic and β-functional components of diversity (Fig. 3),
demonstrating high phylogenetic and functional redundancy among species for
all habitats.

Table 2. Three-way permutational analysis of variance (PERMANOVA) with
1,000 permutations for estuarine fish species data. The analysis was carried out
considering a mixed design with habitats nested in estuaries and crossed with
seasons.
Source

Pseudo-F

Ecosystem

0.851

0.425

1.124

0.219

Habitat

1.753

0.876

2.315

0.001

Season

0.705

0.704

1.980

0.004

Habitat (Estuary)

2.903

0.725

1.917

0.001

Habitat ×

1.555

0.518

1.369

0.013

Season

Figure 2. Variability in the α-component (abundance-weighted) of each diversity
dimension of fish species for habitats and seasons of three tropical estuaries.
The * represents a statistically significant difference between seasons.

A few insights into these relationships could be assessed by analyzing the
position of studied species in the taxonomic, phylogenetic and functional spaces
(Fig. 4). In seagrass beds, there were seasonal changes in species composition

that resulted from both the occurrence of species in the rainy season that were
typically common to mangrove and sandy beaches habitats (i.e., Mugil curema
and Diapterus aurautus) and the addition of new marine species that were unique
to this habitat (i.e., Acanthurus coeruleus and Archosargus rhomboidalis). For
sandy beach areas, the increase of α-taxonomic and α-phylogenetic diversity
during the rainy season was caused by the occurrence of species with a more
estuarine habit, such as Trinectes paulistanus, Symphurus tessalatus, Mugil liza
and Cathorops spixii, as well as the occurrence of species that were unique to
the seagrass beds during the dry season.

Figure 3. α and β components of the three diversity dimensions of tropical fish
assemblages among habitats and seasons of three estuarine systems.

Figure 4. Taxonomic (A), phylogenetic (B) and functional (C) spaces occupied by
fish assemblages of three tropical estuarine systems across different habitats
(mangrove = red; seagrass = green; sandy beach = blue)) and seasons (dry =
sun symbol; wet = rain symbol).

3.4. Discussion
Habitat diversity within tropical coastal areas has always been credited as
a key component of the higher taxonomic diversity profile of these ecosystems
(Eggleston et al., 1999; Ferreira et al., 2019; Nagelkerken et al., 2015). However,
the effects of habitat heterogeneity on ecosystem functioning and filtering
mechanisms are still poorly understood, primarily due to the highly complex
dynamics of habitat mosaics. Our results add to the current knowledge of
estuarine and coastal ecology by showing that patterns in the occurrence and
abundance of tropical fish species have different effects on distinct diversity
dimensions. More precisely, for tropical systems with marked seasonality, both
habitats and season appear to play a synergic role in the maintenance of
ecosystem functioning by enhancing functional and phylogenetic redundancy.

3.4.1. Species composition among coastal habitats and seasons
Overall, despite differences in the distribution of habitats and in the
morphology of studied systems, habitat configuration had no significant effect in
structuring fish assemblages, with a similar specie composition being found in all
three sampled systems. Although it would be expected that habitat configuration
would play a significant role in shaping biological communities, studies have
shown that this effect is weaker at smaller scales and often independent of
system geo-morphology (Dorenbosch et al., 2007, 2004). However, distinct
pattern of habitat use by species was observed for each season. During the dry
season, habitats had their own species composition, with significant differences
between assemblages depending on the characteristics of each habitat. In this
season, habitats have distinct environmental conditions, being able to maintain
their own individual features and dynamics (Sales et al., 2016). Therefore,
environmental filtering selects a different set of species depending on individuals’
physiological

adaptations,

such

osmoregulatory

capacity

and

diet

requirements (Barletta et al., 2005). For example, sandy beach and seagrass

areas tend to have higher and more stable salinity levels than mangroves during
the dry season months (da Silva et al., 2018). These conditions are more suitable
for species with preference for higher salinity environments, such as marine
straggler fishes (da Silva and Fabré, 2019; Potter et al., 2015) that find additional
food sources and shelter in these areas. Since salinity is a key structuring factor
of coastal fish assemblages, its great variability among habitats favors the
presence of some species while limiting the occurrence of others (Barletta, 2004;
Hajisamae and Yeesin, 2014).
On the other hand, the rainy season was characterized by changes in
species composition that caused an increase in α-taxonomic diversity for all
habitats and enhanced similarity among them. During the rainy season, tropical
estuarine habitats typically receive great inputs of freshwaters and sediments,
which extend the estuarine condition to all habitats and the coast (Longhurst and
Pauly, 1987). This process called “estuarization” alters productivity levels and
environmental conditions, such as salinity, turbidity and dissolved oxygen
(Krumme et al., 2012; Neto et al., 2014; Passos et al., 2016), affecting the
habitats’ structure and their fish assemblages (Sales et al., 2016). For instance,
seasonal changes in species composition of seagrass habitats can be associated
with the life cycle of tropical seagrass species, highly sensitive to variations in
water physical-chemical parameters (Barros and Rocha-Barreira, 2014).
Seasonal fluctuations in turbidity and salinity can cause seagrass loss and
decrease its total biomass, changing habitat features and availability, which will
inevitably affect fish species (Koch et al., 2007; Preen and Marsh, 1995).
Moreover, the estuarization of costal habitats enhanced by rainfall appears
to cause a temporary spatial homogenization, allowing changes in species
composition by facilitating the transit of existing species among habitats, as well
as the occurrence of new species in the same area. This assumption can be
supported by the similarity in species composition of seagrass and sandy beach
areas during the rainy season in all three sampled areas. The seasonal reduction
of seagrass biomass caused by greater rainfall rates reduces habitat complexity
and increases structural similarity to sandy beach areas, enabling the selection

of a similar set of species in both habitats. In addition, their dynamics suffer
similar pressures with intensifications of rainfall and freshwater supply, such as
decreases in salinity levels and greater wave actions that promote a constant
organic matter remineralization (Lacerda et al., 2014; Rodrigues and Vieira,
2013). Furthermore, another evidence of habitat homogenization by estuarization
is the occurrence of a few estuarine species that were typically found in mangrove
habitats inhabiting the sandy beaches and seagrass beds during the rainy
season, even though mangroves were able to maintain their own species
composition during both seasons.

3.4.2. Relationship between diversity dimensions throughout the estuarine
dynamics
Although rainfall regime appears to play a significant role in structuring
tropical fish assemblages among estuarine and coastal habitats, the great
species turnover (high β-taxonomic diversity) found in our study was followed by
a trait-convergence pattern. Specifically, we found that species’ functions were
similar for all habitats (low β-functional diversity), regardless of the increases in
taxonomic diversity and changes in species composition. High functional
redundancy along with great diversity of species are typically credited as key
components of resilience and stability (Baptista et al., 2015; Casatti et al., 2015),
as ecosystems are able to maintain key functions even in the face of species
migrations or extinctions (Teichert et al., 2017). However, there is more to the
concept of redundancy than just assuming that species are functionally similar,
with many authors arguing that a subtle level of complementarity may be hidden
behind an apparent redundancy (Blüthgen and Klein, 2011). For instance, great
levels of niche differentiation among redundant species have been shown to
provide a portfolio effect within the estuarine ecosystem by promoting stable
coexistence of competitive species and maximizing resource use (da Silva and
Fabré, 2019).

While the mechanisms behind this niche differentiation are still poorly
understood, the phylogenetic history of species appears to be closely associated
with this diversification (Blüthgen and Klein, 2011; Elmqvist et al., 2003). In our
results, for example, functional diversity of sandy beaches remained stable
despite an increase in both, the taxonomic and phylogenetic diversity during the
rainy season, even with the addition of phylogenetically distinct species. This
result again shows the prevalence of functionally redundant species among
estuarine and coastal habitats and illustrates how phylogenetic lineages may play
a significant role in maintaining that functional redundancy. Although an increase
in the diversity of functions is expected with the rise of phylogenetic diversity
(Cadotte et al., 2010), species in the same functional group (a set of taxa that
perform a similar function) may differ in the way they perform a particular role
depending on life history features (Elmqvist et al., 2003). Indeed, it is expected
that the presence of phylogenetically distinct species in the same functional group
ensures the continuity of functions even when faced with disturbances, by
providing a certain degree of complementary between species (Jonsson et al.,
2002). Therefore, it is possible that the addition of fishes with a more estuarine
habit in sandy beaches during the rainy season may have enhanced redundancy
by increasing niche differentiation among assemblages.

3.4.3. Limitations, current concerns, and implications for conservation
Although we acknowledge that our study may have some limitations due
to the use of only one sampling gear to estimate species composition, the
presence and dominance of juveniles and small-sized fishes throughout the
coastal habitats in this region often result in similar diversity profiles among
different applied sampling methods (Henriques et al., 2017a; Vasconcelos et al.,
2015). The main purpose of our study was to retrieve a representative sample of
fish assemblages that have a significant contribution to the functioning of coastal
habitat mosaics, and as each studied habitat is mainly used by juveniles and

small-sized species as feeding areas and shelters, we believe that our study
covers a significant portion of species found in the area.
Our study suggests that habitats and seasons are all involved in a synergic
process that is directly linked to the maintenance and management of ecosystem
functioning. More precisely, we found that both habitats and seasons have a
significant role in structuring the three dimensions of fishes’ diversity, with a clear
seasonal pattern that appears to enhance redundancy of functions among
habitats. Consequently, conservationists should use integrative approaches that
take in consideration both factors when defining management actions in order to
conserve tropical estuarine and coastal systems as a whole. Nevertheless, it is
important to highlight that there are many current threats to the ecological integrity
of these environments, which can put this dynamics at risk (Blaber and Barletta,
2016). Climate change, for example, has great potential to increase rainfall in
these areas at unprecedent rates, especially during the dry season, which would
impact freshwater runoff and sediment supplies and eventually cause a
homogenization of ecosystems (Bernardino et al., 2015; Marengo et al., 2010).
Although a temporary homogenization appears to be a key component of
estuarine ecosystem functioning by enhancing habitat connectivity and
facilitating species movements, the permanent homogenization would impact the
individual integrity of habitats, by changing habitat features and conditions and
affecting species that inhabit these areas (Gartner et al., 2013). For example,
estuarine-dependent fishes tend to use different habitats as they grow to
complete their life cycle. Thus, a permanent homogenization would affect these
species dynamics and interfere in their development process (Nagelkerken et al.,
2015, 2008).
Furthermore, the increasing number of threats posed by human-induced
impacts are also of great concern, especially for the tropical region where
estuaries and coastal areas are suffering unprecedented levels of anthropogenic
pressures (Blaber and Barletta, 2016). River damming has reduced water and
sediment flows, changing productivity levels and affecting estuarine habitats’
structure (Lacerda et al., 2007). Urbanization of nearby areas has changed the

overall estuarine landscape, causing species loss and reducing fishery
production (Pereira et al., 2010). In addition, habitat degradation in these
ecosystems has been greater than ever, with the ongoing transformation of
mangrove areas into shrimp farms, the shrinking of seagrass coverage due to
poor water quality and increasing beach pollution (Arthington et al., 2016). Our
results showed how important the seasonal dynamics and habitat diversity are
for coastal areas. So, conservation actions should focus on the integrated
protection of all habitats that comprise the coastal mosaic, such as sandy
beaches, mangroves and seagrass beds, to sustain the complexity of inshore
coastal areas that are highly productive for coastal fisheries and fundamental to
maintain coastal livelihoods.

3.5. Acknowledgements
This work is part of the Long-Term Ecological Research – Brazil site PELDCCAL (Projeto Ecológico de Longa Duracão – Costa dos Corais, Alagoas)
funded by the Brazilian National Council for Scientific and Technological
Development – CNPq (#441657/2016-8), the Brazilian Coordination for the
Improvement

Higher

Education

Personnel

–

PELD/CAPES

(23038.000452/2017-16) and the Research Support Foundation of the State of
Alagoas – FAPEAL (#60030.1564/2016). V. da Silva received a scholarship
provided by Coordination of Improvement of Higher Education Personnel–
CAPES; N. Fabré was funded by the Brazilian National Council for Scientific and
Technological Development – CNPq (#311785/2018-2); and M Dolbeth was
supported by the Portuguese Foundation for Science and Technology (FCT)
investigator contract (IF/00919/2015), subsidized by the European Social Fund
and MCTES (Portuguese Ministry of Science, Technology and Higher
Education), through the POPH (Human Potential Operational Programme) and
partly by Portuguese national funds within the scope of UIDB/04423/2020 and
UIDP/04423/2020.

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4. CAPÍTULO II: Relative importance of habitat mosaics for fish guilds in
the northeastern coast of Brazil2

Victor Emmanuel Lopes da Silva1, Ivan Oliveira de Assis1, João Vitor CamposSilva2, Gustavo Vasconcelos Bastos Paulino3, Nidia Noemi Fabré1

Laboratory of Ecology, Fishes and Fisheries – Institute of Biological and Health

Sciences, Federal University of Alagoas, Maceió, Brazil
2

Faculty of Environmental Sciences and Natural Resource Management,

Norwegian University of Life Sciences, Ås, Norway
3

Laboratory of Molecular Diversity – Institute of Biological and Health Sciences,

Federal University of Alagoas, Maceió, Brazil
Corresponding author: lopesdasilvavictor@gmail.com
V.E.L.S.: http://orcid.org/0000-0002-7473-9591 (ORCID-iD)
I.O.A.: http://orcid.org/0000-0001-8703-9722 (ORCID-iD)
J.V.C-S.: https://orcid.org/0000-0003-4998-7216 (ORCID-iD)
G.V.B.P.: https://orcid.org/0000-0003-2825-3133 (ORCID-iD)
N.N.F.: http://orcid.org/0000-0002-4954-2236 (ORCID-iD)

Artigo publicado na revista Regional Studies in Marine Science (Qualis A3, percentil 67%) em

dezembro de 2021. DOI: 10.1016/j.rsma.2021.102145

Abstract
The identification of patterns in habitat use by fish guilds may provide an
integrated perspective of coastal mosaics. Thus, we used multivariate analyses
to assess the relative importance of habitat types for fish guilds based on density
and species composition throughout a seasonal event in the northeastern coast
of Brazil. Our results showed a great variability of responses found for each
functional group, with species composition of guilds that are estuarine-related
being affected by habitat types (p=0.001) and seasons (p=0.008), whereas the
facultative estuarine users showed no significant relationship with both variables
(p=0.95). Specific habitat association patterns were not found for guilds, though
solely estuarine species (p=0.041) and marine straggler fishes (p=0.027) were
related to environmental conditions that varied greatly with seasonality (i.e.,
rainfall and salinity rates), indicating that temporal changes in the region allow
species from different guilds to explore the whole coastal mosaic at different
scales of space and time. For this reason, we highlight that the integrated
protection of beaches, mangroves and seagrass compose an imperative strategy
to sustain the complexity of inshore coastal areas that are highly productive for
coastal fisheries and fundamental to maintain coastal livelihoods.

Keywords: seagrass, mangrove, reef fishes, coastal fisheries

4.1. Introduction
Fishes are among the most diverse and dynamics groups within the
estuarine and coastal biota (Elliott et al. 2007), with assemblages being mainly
comprised of marine, freshwater, and brackish species that spend at least one
part of their life cycle in those areas. These estuarine and coastal species are
one of the main components of ecosystems’ functioning and resilience (Baptista
et al. 2015; da Silva and Fabré 2019), as they perform a wide range of functions
throughout their life history cycle, including the control and the transport of
organic matter between different environments (Lebreton et al. 2011). Hence, it
is not a surprise that ecologists have always tried to understand the drivers and
patterns of temporal and spatial occurrence of fishes in these ecosystems
(Barletta-Bergan et al. 2002; Henriques et al. 2017; da Silva et al. 2018).
However, studies describing how fish species use estuaries and coastal
zones are often challenging due to the highly complex dynamics of these areas.
For instance, the constant changes in the environmental conditions and
productivity levels of these areas tend to create a wide range of responses from
species in the same assemblage due to distinct physiological limitations, such as
specific osmoregulation mechanisms (Whitfield et al. 2012; Telesh et al. 2013)
and different dietary requirements (Whitfield 2017). This variability of responses
along with other factors such as the great structural complexity found within have
a direct impact on how species use the whole coastal space (Gillanders et al.
2003; Wasserman and Strydom 2011).
Indeed, the structural complexity of coastal areas has always been one of
their main features, being well represented by the great diversity of habitat types,
which may include mangroves, seagrass beds, saltmarshes, mudflats, and
coastal sandy beaches (Pihl et al. 2007). Each one of these habitat types has its
own characteristics and dynamics, creating a highly complex mosaic that shapes
assemblages in many different ways, having distinct influences on ecosystem
functioning (Pihl et al. 2007). For example, the nursery role of seascapes has
been recently re-evaluated using a spatial perspective, and authors showed that

the nursery value of habitats that comprise the coastal mosaic may vary between
species and throughout fish development (Nagelkerken et al. 2015). In tropical
regions, though mangroves and seagrass beds have always been credited as
fundamental areas for fishes (Mumby et al. 2004), many studies have shown that
species which are dependent on these habitats may also use other environments
(i.e., sandy beaches and mudflats) throughout their life history (Gillanders et al.
2003; Vasconcelos et al. 2010; da Silva et al. 2018). Indeed, the diversity of
habitat types appears to enhance the effectiveness of coastal areas as nurseries,
since only a few species are confined to a single nursery ground, with mobile
species connecting adjacent habitats through migrations to seek shelter and/or
food resources (Nagelkerken et al. 2008; Nagelkerken et al. 2015).
Thus, the coastal habitat mosaic concept (Sheaves 2009) emerged as a
more developed approach to evaluate the functioning of these ecosystems by
incorporating the linkages among habitat types and the different stages of fishes’
life cycle (Barbour et al. 2014; Nagelkerken et al. 2015). According to this
concept, species migrate between adjacent areas as they grow, with the
individual response of fishes depending on their relationship with habitats
(Barbour and Adams 2012). In other words, from a spatial perspective, there may
be a considerable variability in the value of habitat types for different species in
the same community, as each habitat has its distinct features and dynamics, thus
contributing disproportionally for distinct parts of the assemblage (Nagelkerken
et al. 2015). Although this habitat mosaic concept has been largely applied to
explain use and movements of single populations, for example, the migratory
patterns of Lutjanidae, Haemulidae, Carangidae and other species with
commercial value (Honda et al. 2013; Murray et al. 2018; Reis-Filho et al. 2019),
a community perspective of this concept is still poorly explored.
Part of this lack of information based on community studies might be due
to the many challenges faced by ecologists when trying to describe habitat use
for the whole fish biota. Comparisons of fauna composition among different
habitat types are very difficult (Nagelkerken et al. 2000), and the high dynamism
of ecosystems makes the development of such studies even harder. In the

tropics, for instance, seasonality driven by rainfall regimes causes not only
changes in fish assemblages, but also in habitat’s structure (Passos et al. 2016),
with seagrass coverage decreasing and sandy beach dynamics drastically
changing from one season to another (Koch et al. 2007; Santana et al. 2013). A
comprehensive understanding of how fish assemblages use coastal mosaics
should take in consideration all these factors, since this type of information is
required for the proper management and conservation of ecosystems and
species (Sheaves et al. 2014; Potter et al. 2015).
In this context, one of the easiest and most effective strategies to evaluate
habitat usage might be through the classification of species into guilds based on
their functional attributes (Elliott et al. 2007). The guild approach provides a more
comprehensive overview of species, allowing us to assess their ecological and
functional role in ecosystems as it is often derived from species’ morphology,
feeding habit, reproductive mode, or habitat use (Elliott et al. 2007; Potter et al.
2015). For example, the estuarine-use functional guild proposed by Elliott et al.
(2007) and later developed by Potter et al. (2015) has been successfully used to
understand spatial and temporal changes of fish assemblages (Ferreira et al.
2019), as well as to identify changes in the food web structure and energy flow
of estuarine systems (Harrison and Whitfield 2008). This is possible because the
categorization of species into guilds is based on many biological information
regarding physiological adaptations and migratory patterns (Elliott et al. 2007).
Nevertheless, habitat-specific studies using this guild approach are still rare in
the current literature (Aguilar-Medrano et al. 2020), resulting in information gaps
that are extremely concerning as habitat loss and degradation of costal habitats
are increasing, especially in tropical regions (Blaber and Barletta 2016).
The identification of patterns in habitat use of fish guilds may provide an
integrated perspective of coastal mosaics. Thus, the aim of this work was to
assess the relative importance of habitat mosaic types for fishes, based on
density and guild's composition, during a seasonal event in the northeastern
coast of Brazil. We hypothesized that changes in the density of individuals and
species composition of guilds would be associated to habitats and seasons. Our

data not only will expand the current knowledge regarding the habitat use
patterns of fish assemblages in tropical regions but will also provide a more
integrated perspective that recognizes the value of the entire coastal habitat
mosaic.

4.2. Material and methods
4.2.1. Study area and sample design
This study was conducted in three coastal areas located in the northeastern coast
of Brazil in the southeastern Atlantic (Fig. 1), characterized by a tropical, semihumid climate with two well-defined seasons: a dry season from September to
February, and a wet season between March and August. The Manguaba river
(9°9′28″S; 35°17′42″W) and Santo Antônio river estuaries (9°24′18″S;
35°30′25″W) are located within one of the most important marine protected areas
(MPA) of Brazil – the Área de Proteção Ambiental Costa dos Corais (APACC).
The APACC is the largest coastal MPA in the region with 400,000 ha of extension,
hosting about 120 km of mangroves, sandy beaches, and coral reefs. The third
sampled area has a bar-built conformation (Levinson 2010) and is located on the
Mundaú-Manguaba Estuarine Lagoon Complex (9°39′57″S; 35°44′6″W), which is
one of the most productive coastal systems in the northeastern Brazil (Oliveira
and Kjerfve 1993).
In each area, six sampling stations were established along its extension,
with two stations per habitat type (mangrove, seagrass, and sandy beach),
resulting in a total of 18 sampling points (Fig. 1). Mangrove stations were located
in regions close to the estuary’s banks covered with mangrove forest dominated
by Rhizophora mangle, Avicennia schaueriana, and Laguncularia racemose (da
Silva et al. 2018). In the Manguaba river and Santo Antônio river estuaries,
seagrass stations were located in beds (mainly represented by Halodule wrightii)
nearby the estuaries’ mouths, while in the Pontal estuary, stations were set in
beds found inside the channels’ system that builds the estuarine complex. All

sandy beach stations were established in the shallow waters (mean depth ≤ 1.5
m) adjacent to the estuaries’ mouth.

Fig. 1 Location of sampling sites for each habitat type: mangrove (▲), seagrass
beds (●) and sandy beach (■) in the Manguaba river estuary (A), the santo
Antônio river estuary (B) and the Pontal estuary (C).

4.2.2. Fish surveys and environmental information
From July 2017 to June 2018, we conducted monthly surveys covering the
wet and dry seasons. Before fish sampling, we recorded the environmental
conditions of each station (i.e., salinity, temperature, dissolved oxygen, and pH)

with a Hanna HI 9828 multi-parameter water quality portable meter. After that,
we conducted two standardized surveys in all sampling stations, using a beach
seine 12 m long and 3 m high with mesh size of 12 mm and opposite knots. A
total of 432 hauls were conducted for five minutes each in order to minimize
impacts to local fish communities (de Araujo et al. 2008), with the initial and final
geographic coordinates hauls recorded to estimate the sampled area (m2). All
collected fishes were taken to the laboratory and identified to species level
following regional taxonomic keys (i.e. Figueiredo and Menezes 1978; Menezes
and Figueiredo 1985). The identified species were later classified into their
respective estuarine-use functional guilds (Potter et al. 2015), based on
published data⁠ (Table 1). We also retrieved monthly data on rainfall (in mm) for
each estuary from the Alagoas State Secretariat for the Environment and Water
Resources

(http://www.semarh.al.gov.br/)

represent

the

component

seasonality in our study, and measured the distance of each sampled habitat
from the estuary’s mouth, using its coordinates recorded during sampling
procedures.

Table 1 Estuarine-use functional guilds used to classify fish species collected in
the present study following Potter et al. (2015)
Guild

Ecological characterization

Solely estuarine (SE)

Species which their lifecycle occurs only in estuarine
environments

Estuarine and marine
(E&M)

Species that can complete their lifecycle in either estuaries
or in the marine environment

Marine estuarine
dependent (MED)

Species whose juvenile individuals mandatorily requires
estuarine shelters during his first life stages

Marine estuarine
opportunist (MEO)

Species that occasionally may enter in estuarine areas,
generally using these environments as alternative nursery
areas, but may vary the distribution in adjacent areas

Guild

Ecological characterization

Marine straggler (MS)

Species that may enters estuaries sporadically in fewer
numbers than MEO and are more common in areas which
salinity do not variate considerably

4.2.3. Data analysis
Fish densities of identified guilds were estimated for each haul as the total
number of collected individuals in the guild divided by the product of the swept
area and the seine size (m2) (Johnson et al. 2008). Variability in overall density
of fish species was evaluated by a three-way ANOVA using guilds, habitats, and
seasons as factors. To do so, datasets were previously log-transformed (log n+1)
to reduce data aggregation and meet the assumptions of a parametric test.
Normality and homoscedasticity of residuals were then analyzed by the ShapiroWilk and Levene’s tests, respectively.
Furthermore, Bray–Curtis similarity matrices were constructed from the
density data (#/m2) for each guild and used to evaluate the effect and relative
importance of habitat types and seasons on guilds’ composition by two-way
permutational multivariate ANOVAs (PERMANOVAs). The PERMANOVA is a
nonparametric distance-based ANOVA that uses permutation procedures to test
hypotheses and works by assigning components of variation (COV) of differing
magnitudes to the main factors and interactions between them. The greater is the
COV, the stronger is the influence of a particular factor or interaction term on the
structure of the data (Anderson 2017).
To further investigate patterns identified through the PERMANOVAs
analysis, a similarity percentage analysis (SIMPER) was later carried out to
identify species that were responsible for the dissimilarity between factors in
guilds that had a significant effect. We also carried out a non-parametric BEST
procedure with the Spearman’s rho rank correlation to identify whether or not
guilds’ composition could be explained by environmental conditions (Peterson et
al. 2013). This approach uses the “bioenv” function from the “vegan” package to

search for the best possible combination of environmental variables that gives a
correlative explanation for the composition of guilds (Clarke and Ainsworth 1993).
Finally, the function “envfit” from the ‘vegan’ package was used to assess
impacts of environmental factors on guild composition. This function performs an
overlap between vectors representing environmental factors and NMS ordination
plots, while testing for statistical significance with 999 random permutation tests
(Smith et al., 2017). All statistical analyses were carried out in the R statistics
software using the vegan package at a significance level of p<0.05 (R Core Team
2013).

4.3. Results
A total of 2,542 individuals, from 86 species and 30 families, were
collected. Species were classified into five estuarine-use functional guilds
(EUFG), with the marine straggler guild being the most representative in terms of
species richness (22 species), followed by the marine estuarine opportunists,
with 19 species, the solely estuarine and the estuarine and marine guilds (both
with 17 species each), and the guild with less representants in terms of species
was the marine estuarine with only 11 species.
Overall density of individuals varied greatly between the EUFGs (Table 2,
three-way ANOVA, F=22.63, p=0.001), but the solely estuarine and the marine
estuarine dependent guilds had the highest values registered throughout the
study period (Fig. 3). Moreover, though habitat types and season had individual
effects in the overall density of individuals, neither an interaction between them
(F=0.897, p=0.411), nor a relationship with guilds was found (F=1.061, p=0.394).
In fact, a similar pattern in the density of individuals among guilds and across
habitat types was found for both seasons (Fig. 2).

Table 2 ANOVA results for the variability in the overall density of individuals
across estuarine-use functional guilds, habitats, and seasons
Variable

Sum of Squares

F-value

Guild

52.95

22.636

0.000

Habitat

8.03

6.866

0.001

Season

4.71

8.054

0.005

Guild × Habitat

6.47

1.384

0.211

Guild × Season

2.17

0.927

0.451

Habitat x Season

1.05

0.897

0.411

Guild × Habitat × Season

4.95

1.061

0.394

Fig. 2 Variability in the density of individuals of identified estuarine use functional
guilds across habitats and seasons. Plot also shows rainfall data (in mm) for each
month to highlight differences between seasons. SE – solely estuarine; E&M –
estuarine and marine; MED – marine estuarine dependent; MEO – marine
estuarine opportunist; MS – marine straggler

In relation to guilds’ composition, each EUFG showed a distinct
arrangement of species in relation to spatial and temporal variables (Table 3).
Habitat type had a significant effect on the structuring of the guilds that show a
certain degree of dependency with the estuarine environment, such as the solely
estuarine (PERMANOVA, Pseudo-F=3.37, p=0.001), the estuarine and marine
(Pseudo-F=, p=0.016) and the marine estuarine dependent guilds (PseudoF=1.85, p=0.006). Seasons showed a similar pattern, being also associated to
EUFGs that are dependent on estuaries, except for the marine estuarine
dependent guild (Pseudo-F=1.16, p=0.221). Additionally, an interaction between
habitat types and seasons was also found for the solely estuarine species
(Pseudo-F=-2.5, p=0.034). On the other hand, the species composition of marine
estuarine opportunist and marine straggler individuals showed no significant
relationship with habitats and seasons, even though the marine stragglers
species were significatively correlated to the distance of habitat types from the
estuary’s mouth, as well as to changes in rainfall and salinity rates (Fig. 3, Table
4, BEST procedure, ρ=0.255, p=0.027).
To better understand the effects of habitat types and seasons on the
composition of EUFGs, we analyzed the usage pattern of species for each guild.
In the solely estuarine guild, though species tended to use the three available
habitats, seasonal changes in the density of species shaped the overall structure
of the guild. For example, Sphoeroides testudineus (responsible for 35.1% of total
dissimilarity, SIMPER) was the most abundant species during the wet season in
all habitat types but especially in the sandy beach area, whereas the second most
abundant species, Atherinella brasiliensis (15%) had the highest values
registered during the dry season for all three habitat types (Table S1). The
occurrence and abundance of species in this guild were also correlated to
habitats’ distance from estuary’s mouth, and a set of environmental variables –
rainfall, pH, turbidity – that varied greatly throughout the estuarine dynamics (Fig.
3, Table 4, BEST procedure, ρ=0.291, p=0.041).

Table 3 PERMANOVA results for the density of estuarine-use functional guilds,
obtained through the Bray–Curtis similarity matrix, showing the partitioning of
multivariate variation and tests by habitats and seasons, as well as their
interaction. SE – solely estuarine; E&M – estuarine and marine; MED – marine
estuarine dependent; MEO – marine estuarine opportunist; MS – marine
straggler
Estuarine-use functional guild
Source

df
F

E&M
F

MED
F

MEO
F

MS
F

Habitat

3.37 0.001 1.51 0.016 1.85 0.006 1.03 0.134 1.25 0.11

Season

1.81 0.008 1.57 0.033 1.16 0.221 0.91 0.326 1.28 0.134

Habitat
×
Season

-2.5

0.034 -2.2

0.687 -1.9

0.698 -1.4

0.475 -1.5

0.959

For the estuarine and marine guild, species showed preference for a
particular habitat, such as the mugilids Mugil liza and M. rubrioculos which were
only found in the sandy beach areas. Even when species used more than one
habitat, a clear habitat preference was found. For instance, Lycengraulis
grossidens (26.8%) had the highest density values registered in the sandy
beaches, whereas Diapterus rhombeus (13.7%) was more common to mangrove
areas. In the marine estuarine dependent guild, species, such as Eucinostomus
gula (24%), Mugil curema (17.4%), and E. argenteus (11%) used all three habitat
types in both seasons, but the highest densities were recorded in the dry season
with a slightly decrease occurring during the wet season (Table S1).

Table 4 Multivariate correlations between the environmental variables and
estuarine-use functional guilds, displaying the top model from the BEST output
for each guild, as well as its strength (ρ) and significance (p-value). SE – solely
estuarine; E&M – estuarine and marine; MED – marine estuarine dependent;
MEO – marine estuarine opportunist; MS – marine straggler
Guild

Best model

Correlation (ρ)

p-value

Rainfall + pH + Turbidity + Dist.Mouth

0.291

0.041

E&M

Temperature + Dissolved oxygen

0.123

0.214

MED

0.099

0.924

MEO

Rainfall + pH + Turbidity

0.192

0.629

Rainfall + Salinity + Dist.Mouth

0.255

0.027

Fig. 3 Non-metric multidimensional scaling (NMS) ordination plots showing guild
composition in relation to environmental factors.

4.4. Discussion
The results reported herein reinforce the importance of coastal mosaics
for both, species composition and overall density of tropical fish species,
highlighting that the relative importance of habitat types has seasonal variation
for ecological guilds. Specifically, we found that the habitat mosaic along with the
seasonal changes that occur throughout the coastal dynamics have different
influences on distinct species found within the same assemblage, expressed by
the great variability of responses found for each analyzed guild.
Marine estuarine dependent and solely estuarine species showed the
greatest densities of individuals in all habitat types during both seasons, which
was not a surprise as these guilds are typically reported as the main components
of estuarine and coastal fish assemblages (Mumby 2006; Nagelkerken et al.
2008; Ferreira et al. 2019). Species within these guilds have their life cycle strictly
related to the estuarine ecosystem, using a variety of habitat types at different
stages of their life cycle (Potter et al. 2015). For instance, the marine estuarine
dependent species, represented by Mugilidae, Lutjanidae and Gerreidae taxa
(Nagelkerken et al. 2008; Igulu et al. 2014), mostly use mangrove habitats as
shelters and seagrass beds as feeding areas during the juvenile phase (Blaber
2007; Vasconcelos et al. 2010; Schrandt et al. 2015), whereas solely estuarine
individuals use those areas to complete their whole life cycle, typically inhabiting
a variety of available habitats as they grow (Potter et al. 2015). Either way, for
both guilds, estuarine and coastal habitats make up an essential component of
species life history, helping to support substantial species populations.
Another possible explanation for the great abundance of individuals of
solely estuarine and marine estuarine dependent guilds throughout the whole
study period is that species within these guilds often have physiological and
morphological adaptations that allow them to support the challenging conditions
of these areas (Matthews et al. 2010). For example, high plasticity in diet (Rueda
2002; Contente et al. 2010), and wide salinity tolerance (Elliott et al. 2007) are
two main features that species in these guilds possess, assisting their

permanence in estuarine environments even when changes in environmental
conditions or productivity levels occur. In contrast, species that are not
considered obligate users of estuarine environment (i.e. marine estuarine
opportunist and marine stragglers), tend to lack these adaptations, making their
abundance very limited (da Silva and Fabré 2019), and typically occurring in
these areas for a short period of time (Ferreira et al. 2019; Macedo et al. 2021).
Habitats had a significant effect on species composition of guilds with a
certain degree of dependency on estuarine systems, however, the absent of a
significant effect of the interaction between habitat types and guilds on the overall
density of individual shows no signs of a single habitat association pattern per
guild. Although it would be expected that guilds would be linked to a specific
habitat due to distinct habitat features (da Silva et al. 2021), the seasonal
conditions of tropical regions may explain why this preference pattern was not
observed. The great inputs of freshwater and sediments during the wet season
create an estuarization process that extends the estuarine condition to the coast
(Passos et al. 2016), which, causes a seasonal homogenization of habitats during
the wet season that may trigger a spatial rearrangement of species in the whole
coastal landscape.
The strong effects of rainfall regimes on other conditions of tropical
regions, such as salinity, pH, dissolved oxygen, and turbidity, have been widely
described in literature, and are typically responsible for changes not only in
species composition, but also in habitats’ configuration (Chollett et al. 2007; Short
et al. 2007; McKenzie et al. 2016). For instance, a previous study conducted in
one of the studied estuaries described how rainfall affect the physical-chemical
components of the different habitats found within, where the salinity profile of
habitat types is driving by the great input of freshwater, and temperature and the
levels of dissolved oxygen are very similar among habitats during the wet season
(da Silva et al. 2018). These changes highlight rainfall as one of the main
structuring factors of estuarine and coastal fish assemblages in tropical regions,
with the habitat selection mechanisms of species being strongly influenced by
seasonal regimes (da Silva et al. 2018, 2021).

Moreover, coastal habitats have significant changes in their dynamics
during rainy months as a response to higher rainfall rates. Wave actions in beach
areas, for instance, tend to be stronger, producing a remineralization process of
organic matter that makes a greater quantity of nutrients available in the water
column (Lacerda et al. 2014). For tropical seagrass beds, rainfall regimes cause
substantial reductions of seagrass coverage and its total biomass (Koch et al.
2007), whereas mangrove areas typically have significant changes in turbidity
and dissolved oxygen levels (Barletta et al. 2005). Those fluctuations on habitat
features are often responsible for the reorganization of species in the estuarine
space (Elliott et al. 2007), either by forcing species to leave specific habitat types,
or attracting new species to them. This whole process might explain why
seasonality had an important effect on the species composition of guilds that
complete their whole life cycle in estuarine areas, such as the solely estuarine
species and estuarine and marine individuals.
On the other hand, there was no seasonal effects on species composition
of the marine estuarine dependent guild, neither a correlation with environmental
conditions was found, which may be associated to the life cycle of species in this
guild. Marine species that are estuarine dependent typically use estuaries and
coastal habitats as juveniles and remain in those areas until they are ready for
their recruitment (Potter et al. 2015). Thus, spending a considerable period of
time there, which could explain why this guild composition is not affected by
seasonal changes. For instance, in the tropics, many marine dependent fishes
spawn in the middle/end of the wet season, with pelagic eggs and larvae being
transported into estuaries and remaining in these areas until late dry season
(Rousseau et al. 2018).
The solely estuarine species was the only guild that had significant
changes associated to an interaction between habitat type and seasons, with a
significative correlation between this guild and rainfall and other environmental
variables that vary greatly with seasonality (pH and turbidity). These results
indicate that the coastal dynamics allows species in those guilds to use the whole
habitat mosaic at different scales of space and time. Indeed, studies suggest that

solely estuarine species perform constant migrations between different habitats
as they grow either to search for shelter and/or food, or to avoid the interaction
of adults with juveniles, which could affect the development process of these
individuals (Jones 1968; Bonin et al. 2015). Those spatial and temporal
segregations not only reduce species competition for resources, but also
increase the functionality of ecosystems allowing species to perform their
functions in different habitat types and seasons (Nyström 2006).
The absent of significant effects of habitat type and seasons on the marine
estuarine opportunist and marine straggler guilds can be related to their nondependency on estuarine environments. Fishes in these guilds are facultative
estuarine users, with many species occasionally find their way into an estuary
(Able 2005), either by being carried by tidal currents or intentionally entering the
estuarine habitats for a short period of time to feed. That makes their habitat
usage pattern very variable, with ontogenetic, annual, and cohort-specific scales
playing a significant role in their occurrence and abundance (Able 2005).
Nevertheless, in our study, the marine stranglers were associated to changes in
rainfall and salinity rates, as well as to the distance between habitat types and
the estuary’s mouth, with species being more abundant in sandy beach habitats,
which are closer to the estuaries’ mouth and where salinity rates are often higher,
especially during the dry season. Similar results were found in the Yucatan
peninsula, in the Gulf of Mexico, where these vagrant species where also
associated with areas with higher salinity profile and closer to the coast (AguilarMedrano et al. 2020). This result indicates that the pattern of habitat usage by
these species can be related to their physiological limitation, specifically their
osmoregulatory mechanisms. The understanding of this pattern of occurrence is
crucial, as those species play a significant role in the functioning of tropical
regions, as they increase niche differentiation among assemblages, enhancing
functional redundancy (da Silva and Fabré 2019).

4.5. Conclusion
Our findings highlight that both habitat type and seasons are important
structuring factors of the whole structure of coastal fish assemblages, especially
for those species that depend on these areas during one part of their life cycle.
Considering the vulnerability of estuarine and coastal habitats in tropical regions
and their importance for many fish species, protected areas should ensure the
whole habitat diversity of these areas in no-take zones, where the pressure from
human activities can be avoided. Mangroves and beaches are classical targets
of conservation strategies, mainly due their importance to human populations.
However, the preservation of these habitat types is always focused on each
environment as independent entities, not taking into consideration the mosaic
complex that they are part of. The perspective of the estuarine mosaic is a novel
tool that may be important to reconsider the limitations of conservation areas. For
this reason, the integrated protection of beaches, mangroves and seagrass
compose an imperative strategy to sustain the complexity of inshore coastal
areas that are highly productive for coastal fisheries and fundamental to maintain
coastal livelihoods.

4.6. Acknowledgments
This work is part of the Long Term Ecological Research – Brazil site
PELD-CCAL (Projeto Ecológico de Longa Duração -Costa dos Corais, Alagoas)
funded by the Brazilian National Council for Scientific and Technological
Development CNPq –(#441657/2016-8, #442237/2020-0), and FAPEAL Research Support Foundation of the State of Alagoas (#60030.1564/2016,
#PLD2021010000001) and by Coordination for the Improvement of Higher
Education

Personnel

CAPES-Brazil

CAPES

(#23038.000452/2017-16).

G.V.B.P., I.O.A. and V.E.L.S received a scholarship provided by Coordination of
Improvement of Higher Education Personnel– CAPES; J.V.C-S acknowledge the
Research Council of Norway for funding his post-doc position (#295650); and

N.N.F. was funded by the Brazilian National Council for Scientific and
Technological Development – CNPq (#311785/2018-2).

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5. CAPÍTULO III: Biogeographic patterns in the biodiversity dimensions of
estuarine fish assemblages from the Western Atlantic3

Victor E. L. da Silva1, Marina Dolbeth2, Nidia N. Fabré1

1Laboratório de Ecologia, Peixes e Pesca – Instituto de Ciências Biológicas e
da Saúde, Universidade Federal de Alagoas, Maceió, Brazil
2Interdisciplinary Centre of Marine and Environmental Research - CIIMAR,
Universidade do Porto, Matosinhos, Portugal

*Corresponding author:
lopesdasilvavictor@gmail.com

Artigo a ser submetido na revista Fish and Fisheries (Qualis A1, percentil 99%).

Abstract
Understanding how different biodiversity components are related across different
environmental conditions is a major goal in macroecology and conservation
biogeography. We investigated correlations among different dimensions of
estuarine fish diversity (species richness, phylogenetic and functional diversity)
along the three biogeographic realms of the Western Atlantic. We combined data
from 232 estuaries and 1216 species, which were characterized by seven
functional traits and by phylogenetic affinity. Our results provide new insights into
the relationship between environmental drivers and the dimensions of fish
diversity along the Western Atlantic. As expected, spatial scale had a significant
role in the effects of variables, with different combinations of factors having
unique relationships with dimensions at the macro (the whole Western Atlantic)
and meso (for each biogeographic realm) scales. Overall, estuarine fish diversity
dimensions were all correlated to estuary mouth width and sea surface
temperature, with wider entrances and warmer waters hosting the highest values
of SR, PD and FD. However, at smaller scales, arrangements in each dimension
varied according to distinct environmental features of regions.

5.1. Introduction
Current threats to biodiversity are mainly related to human activities and
the way they transform and impact the planet (Schlacher et al., 2016; Ripple et
al., 2017). With significant increases in human population around the globe,
natural resources have undergone overexploitation and continuously habitat loss
(Pinsky et al., 2011), resulting in faster habitat degradation processes and higher
extinction rates that are often compared to previous mass extinction events
(Stork, 2010). Unsurprisingly, this biodiversity crisis has widely encouraged the
development of different strategies to mitigate species loss, with the definition of
prioritization areas for conservation being one of the most implemented
approaches to date (Pereira et al., 2012). However, indicators show that we are
still facing unprecedent levels of decreases in biodiversity and ecosystem
services (Butchart et al., 2010; Velazco et al., 2019), with many issues related to
how conservation actions are designed and set. For instance, in aquatic
ecosystems, cryptic diversity of many taxa makes unclear how many species are
at risk, or whether these species are successfully protected by current strategies
(Cox et al., 2016). This, in part, results from conservation actions being mainly
proposed through species-based indicators (i.e. species richness, vulnerability
and endemism) which neglects the multidimensional concept of biodiversity
(Doxa et al., 2016).
Biological communities are products of complex evolutionary and
ecological processes, with the biodiversity concept going beyond the
identification and count of species in a particular region (Mazel et al., 2014).
Indeed, many studies have discussed that measuring only species richness may
result in significant loss of unique functional and evolutionary information, which
could affect the integrity and stability of assemblages and ecosystems (Doxa et
al., 2016; Brum et al., 2017; Xu et al., 2019). To address these limitation,
measures of phylogenetic and functional features of assemblages have emerged
as an important component of ecological studies, providing more detailed
information on assembly mechanisms and filtering processes (Petchey & Gaston,
2006; Teresa & Casatti, 2017). While phylogenetic diversity provides an

evolutionary picture of communities, by demonstrating the accumulated history
of species (Faith, 1992), functional diversity reflects the diversity of
morphological, physiological and ecological attributes found within (Violle et al.,
2007; Cianciaruso et al., 2009). Therefore, successful strategies for ecosystems’
conservation should embrace all biodiversity facets to guarantee the
maintenance of ecosystems’ functions and their essential services to humans
(Pollock et al., 2017).
However, though current studies have begun to unravel the complex
relationships between the different dimensions of diversity (Xu et al., 2019),
available knowledge is still limited and mostly based on restricted ecosystems or
groups (Bernard-Verdier et al., 2013; Brum et al., 2017). In estuaries and coastal
lagoons, for example, only few studies have used integrative approaches to
analyze what drives biodiversity dimensions in these areas (Teichert et al., 2018;
Hultgren et al., 2021), with conceptual gaps remaining as one of main obstacles
to fully comprehend these ecosystems dynamics. Estuaries are among the most
complex and productive ecosystems on earth, with many ecological and
economic services provided (Blaber & Barletta, 2016). These areas function as
nurseries for many taxa, which depend on these habitats for at least one part of
their life cycle (Beck et al., 2001; Nagelkerken et al., 2015). Among them, fishes
standout as one of the most diverse and dynamics groups within the estuarine
biota (Elliott et al., 2007), with assemblages being mainly comprised of marine,
freshwater and brackish species. These species are one of the main components
of estuaries’ functioning and resilience (Baptista et al., 2015; da Silva & Fabré,
2019), performing a wide range of functions, such as the control and the transport
of organic matter to coastal areas (Lebreton et al., 2011).
Global patterns in the richness (Vasconcelos et al., 2015), species
composition (Henriques et al., 2017a) and traits (Henriques et al., 2017b) of
estuarine fishes have been recently described, showing a possible divergence
between diversity dimensions, with biogeographic regions having a stronger
effect on traits than species richness (Henriques et al., 2017b). This observed
pattern may result from a variety of factors, such as different assembly processes,

unique filtering mechanisms and the evolutionary history of communities
(Bernard-Verdier et al., 2013), with spatial scales also playing a significant role in
the structuring of dimensions (Arnan et al., 2017). In the Western Atlantic, for
example, while dispersal limitations (i.e. hard barriers) and temperature filters
appear to act as structuring factors of fish assemblages (Henriques et al., 2017a),
trait composition in this region is more related to variables associated to the
connectivity between estuaries and the ocean (Henriques et al., 2017b). Although
we could expect that distinct environmental drivers would shape each dimensions
of diversity along the Western Atlantic, the great variability of environment
conditions throughout its extension, along with distinct sea geology configurations
makes the Western Atlantic a highly complex region, with three biogeographic
realms and more than 30 ecoregions being previously identified for its coast
(Spalding et al., 2007). Each region is characterized by distinct water temperature
profiles, or historical and broadscale isolation patterns that affect and select
species depending on their shared or unique evolutionary history (Spalding et al.,
2007). Therefore, each dimension might be affected by a particular set of
variables at different spatial scales.
Since the Western Atlantic represents an important hotspot of species
richness, hosting great numbers of species in estuarine systems (Vasconcelos et
al., 2015), it is crucial that we identify which factors drive the dimensions of
biodiversity along its extension. Thus, the present study aimed to investigate
biogeographic patterns in the dimensions of estuarine fish diversity throughout
the Western Atlantic, exploring the relationships between diversity and drivers at
different spatial scales. Two main hypothesis drove our study: (1) at the macro
scale (the whole Western Atlantic), all diversity dimensions would be related to
biogeographic variables (i.e. temperature profile), (2) for the meso scale (inside
the biogeographic realms), diversity dimension would respond differently to
analyzed variables, being more associated to environmental conditions of each
region.

5.2. Materials and methods
5.2.1. Estuarine fish assemblages’ dataset
We compiled information from estuarine systems and coastal lagoons
distributed along the Western Atlantic. The dataset was built using available
information from books, scientific papers, and research reports that presented a
list of fish species sampled from a particular estuarine system. Publications were
searched in Google Scholar using the search strings “estuary”, “fish” and the
name of each country located in the America continent, using both English and
the native language of the country (Portuguese, Spanish, or French). Each
publication was downloaded and analyzed following some criteria that were used
to standardize the data screening process: 1) the list of all species collected
during the sampling period had to be reported, thus, works presenting only the
most abundant species or species that contributed the most for the total biomass
were not included in the dataset; 2) sampling information (i.e., fishing gear)
should be available; and 3) studies carried out throughout estuarine gradients
(i.e. with sampling point in rivers or along the coast), were only accepted when
separate species list were given for each sampled environment, with only species
occurring in the estuarine area being included in the dataset. Species names
were checked and validated according to the current taxonomy of fishes using
the “rfishbase” package (Boettiger et al., 2012), and revised records were used
to build a presence/absence matrix. It is important to note that it was not the aim
of our study to produce an exhaustive sample, which would be practically
unachievable. Rather, we aimed to create a broadly representative and
geographically unbiased sample of estuarine fish species occurring across the
Western Atlantic.

5.2.2. Explanatory variables
For each estuary, we gathered data on variables that could potentially
reflect filtering mechanisms of species, phylogenetic lineages, and traits, such as
climatic conditions, estuary morphology and sea geology. Annual mean sea

surface temperature, mean salinity, dissolved oxygen levels, chlorophyll
concentration outside the estuary, and nearby current velocity were recovered
from the Bio-ORACLE website – https://www.bio-oracle.org – (Tyberghein et al.,
2012; Assis et al., 2018). Annual mean precipitation was retrieved from the
WorldClim database using the “sdmpredictors” package in the software R
statistics. Estuary area and mouth width were often available in the publications
used to build the species dataset, however, whenever this information was
absent,

measured

both

variables

using

the

Google

Earth

–

https://earth.google.com/web/ –. At last, continental shelf width was measured
using shapefiles in the QGIS software version 3.16 (QGIS.org, 2021).

5.2.3. Phylogeny and functional traits of fish species
To reconstruct a species-level phylogeny of estuarine fish present in the
Western Atlantic, we assessed the most current taxonomy of fish species
following Betancur-R et al. (2017). A total of 100 trees were retrieved from the
“fishtree” package in the software R statistics (Chang et al., 2019), which provides
access to sequences, phylogenies, fossil calibration and diversification rates for
ray-finned fishes, available in the Fish Tree Life website – https://fishtreeoflife.org
– (Betancur-R et al., 2017). All 100 phylogenetic topologies recovered were used
to build a final Majority-Rule Consensus Tree using the “phytools” package
(Revell, 2020).
Functional traits were selected based on their well-known relationship with
species performance in estuarine environments, such as prey detection and
capture, energy allocation in the body, swimming efficiency, and habitat use and
association (Henriques et al., 2017b). Overall, seven traits were chosen (Table
1), and we compiled a species-trait database with information retrieved from
online datasets and published data for all species (Beukhof et al., 2019; Froese
& Pauly, 2020). As removing species with missing data could affect final results,
thus, leading to misinterpretations (Nakagawa & Freckleton, 2008; Brum et al.,

2017), whenever information was not available for a particular species, we used
existing data for the closest species in the same genus or family.

Table 1 – Functional traits used to estimate the functional diversity of fish species
along the estuarine systems of the Western Atlantic
Trait

Ecological meaning

Reference

Maximum body size

Reflects position in the food web,
metabolic rates, dispersal ability,
mobility and home range

Henriques et al., (2017b)

Body shape

Indicates swimming performance,
and patterns in habitat use

Ribeiro et al., (2016)

Habitat association

Relates to the use of watercolumn, and adaptations to
habitats

Beukhof et al., (2019)

Salinity preference

Reflects the physiological ability
to deal with osmotic stress in
brackish estuarine waters

Henriques et al., (2017b)

Trophic guild

Relates to the position in the food
web, and shows the influence of a
species on abundance of others

Henriques et al., (2017b)

Feeding mode

Reflects feeding strategies and it
is also associated to species diet

Floeter et al., (2018)

Reproductive guild

Indicates dispersal ability,
colonization potential, and
population growth

Lefcheck & Duffy, (2015)

5.2.4. Diversity dimensions
Fish diversity dimensions were evaluated for each estuary using
equivalent diversity measures, to allow comparisons between future models. The
taxonomic component of diversity was expressed by species richness (SR),
taking into consideration the total number of species found in each estuary.
Phylogenetic diversity was assessed by Faith’s PD index (Faith, 1992), which

100

measures the extent of uniquely evolved characters among species using the
final Majority-Rule Consensus Tree created for our pool of species. Functional
diversity was evaluated using the dendrogram length functional diversity (FD),
proposed by Petchey & Gaston (2002), a non-abundance weighted diversity that
measures diversity at all hierarchical scales simultaneously, incorporating the
small functional differences between species (Petchey & Gaston, 2002).
Although FD and PD are expected to be correlated and have a significant
relationship with SR, many studies have shown that this relationship is rather
weak at broader scales (Arnan et al., 2017), with PD and FD covarying in different
ways along geographic and environmental gradients (Bernard-Verdier et al.,
2013; Purschke et al., 2013), thus being suitable for studies that cross
biogeographic regions.

5.2.5. Data analysis
Since one of the main purposes of our study was to identify drivers of fish
diversity dimensions at different scales, we used general linear models – GLMs
– to assess the effect of explanatory variables on dimensions using two
approaches: 1) modelling the whole fish assemblage dataset, including all
sampled estuaries and species; and 2) modelling each biogeographic realm
individually, considering the classification of Spalding et al. (2007). Before
analyzes, the existence of spatial autocorrelation was investigated by fitting
semivariogram models to the data using the “nlme” package in R statistics.
Variables were also checked for collinearity (r>0.7), and then standardized by
subtracting the variable mean to each value and dividing it by the variable
standard deviation.
Because several explanatory variables may influence the diversity
dimensions of fish species, a multi-model inference approach was used
(Burnham et al., 2011), taking into consideration the effect of all possible
combinations of variables on each dimension. We then used a model averaging
approach to reduce model selection bias and account for selection uncertainties

101

(Burnham & Anderson, 2002). The best set of models was chosen by the
corrected Akaike Information Criterion (ΔAICc<4), and the hierarchal partitioning
of explanatory variables included in each model was calculated to assess
individual effects of variables. Each selected model was tested for normality and
homoscedasticity. All analyzes were carried out in the software R statistics at a
significance level of p<0.05.

5.3. Results
A total of 232 estuarine systems and coastal lagoons were analyzed in our
study, with 1216 species being found in these ecosystems along the Western
Atlantic. The Tropical Atlantic realm hosted the highest number of species, with
49.3% of all species being found only in this region, and 25.7% being common to
other realms (Fig. 1). The Temperate Northern Atlantic had 16.6% of unique
species and 16.2% of shared species with other regions, whereas the Temperate
South America showed lowest species richness, with only 8.2% of exclusive
species and 16.2% of shared species (Fig. 1).
Several explanatory variables were correlated throughout the Western
Atlantic, with the significance and power of correlations varying across
biogeographic realms (see Fig S1 on supplementary information). Therefore,
more than 50 models were constructed with different sets of variables to avoid
collinearity. Overall variability in SR, PD and FD throughout the Western Atlantic
were positively correlated to estuary mouth width and sea surface temperature
(Fig. 2), indicating that systems with greater connectivity with the sea and warmer
waters host a greater number of species with phylogenetic and functional
divergence among them. Furthermore, continental shelf width also played a
significant role in shaping functional diversity, with estuaries located in regions of
narrow shelves having lower FD among fish assemblages.

102

Fig. 1 – Map of the Western Atlantic showing the location of the 232 estuarine
systems and coastal lagoons that were analyzed in the present study (A). The
plot also shows the number and percentage of unique and shared species for all
biogeographic realms with the representation of one of the most common species
that was unique in each realm (B). TNA – Temperate Northern Atlanti; TA –
Tropical Atlantic; and TSA – Temperate South America.

103

Across biogeographic realms, models for each diversity dimension varied
greatly in explanatory power and predictive performance (Table 2), with different
set of variables being selected for each realm (Fig. 3, see Table S1 for p-values
of variables included in the models). For the Temperate Northern Atlantic (TNA),
all three dimensions were positively correlated to mouth width, sea surface
temperature and shelf width, whereas chlorophyll concentration outside the
estuary had a negative effect on all dimensions (Fig. 3A). For the Tropical Atlantic
(TA), variabilities in SR and PD were positively correlated to estuary area and
dissolved oxygen levels, with both dimensions being negatively affected by
higher precipitation rates in the region. FD in this realm was only related to the
continental shelf width, with a positive relationship being found (Fig. 3B). In the
Temperate South America (TSA), precipitation and estuary mouth width were
related to all three dimensions, but chlorophyll concentration had only significant
effects on SR and FD (Fig. 3C).

Table 2 – Generalized Linear Models fitted to the variation of diversity dimensions
of estuarine fish species from the Western Atlantic, and its biogeographic realms:
total explained deviance (Exp. %), linear regression of observed and predicted
values (r2), total number of samples (n). Biogeographic realms: TNA –
Temperate Northern Atlantic, TA – Tropical Atlantic and TSA – Temperate South
America.
Mode
l fit

Total

TNA

TSA

Exp.
(%)

0.2
4

0.1
9

0.1
8

0.5
4

0.5
1

0.4
9

0.1
2

0.1
3

0.1
1

0.4
2

0.3
7

0.3
1

233

144

104

Fig. 3 – Model coefficient estimates (±95% confidence intervals) showing the
magnitude and direction of effects of explanatory variables on each diversity
dimension of estuarine fish species along the biogeographic realms of the
Western Atlantic: A) Temperate Northern Atlantic, B) Tropical Atlantic, and C)
Temperate South America. SR – species richness, PD – phylogenetic diversity
and FD – functional diversity. Blue dots and lines represent a positive effect, red
dots and lines show a negative effect, and gray dots and lines indicate no
significant effect found for the variable.

5.4. Discussion
Our results provide new insights into the relationship between
environmental drivers and the dimensions of fish diversity along the Western
Atlantic. As expected, spatial scale has a significant role in the effects of
variables, with different combinations of factors having unique relationships with

105

dimensions at the macro (the whole Western Atlantic) and meso (for each
biogeographic realm) scales. Overall, estuarine fish diversity dimensions were all
correlated to estuary mouth width and sea surface temperature, with wider
entrances and warmer waters hosting the highest values of SR, PD and FD. Both
variables have been previously highlighted in the works of Henriques et al.,
(2017a,b) as one of the main drivers of species and traits composition of estuaries
at a global scale. Temperature gradients impose suitable or unsuitable conditions
for species, selecting species and traits based on their physiological tolerances,
which appears to be related to the phylogenetic history of species as PD also
respond positively to this variable. In the same way, greater connectivity with the
sea allows the occurrence of marine species with dispersal ability and different
sets of traits that enhance FD in these areas. However, the magnitude and effect
size of explanatory variables varied greatly across biogeographic realms, with
distinct factors affecting diversity dimensions.
In the Temperate Northern Atlantic, for example, besides temperature and
mouth size, other variables had also significant effects on all three dimensions of
fish diversity, such as continental shelf width (positive effect) and chlorophyll
concentration (negative effect). The Temperate Northern Atlantic is characterized
by a clear temperature profile, with temperatures in the southern portion having
modest seasonality (Phlips et al., 2020) while varying greatly at the northern
region (Gobler et al., 2012). Temperature differences between regions are
responsible for filtering species composition, selecting specific settlement
mechanisms (Able et al., 2006) and tolerance ranges for each estuary (Morson
et al., 2019). This shapes not only the total number of species (SR) but also traits
(FD) that appears to be related to the evolutionary history of species (PD).
Another important structuring factors of estuarine biota in this realm were the
estuary mouth width and continental shelf width, which are directed related to the
connectivity between estuarine systems and the open sea, acting as regulators
of freshwater runoffs and saltwater inputs (Ohrel & Register, 2006), and
controlling fish migration and larval dispersion (Akin et al., 2003).

106

In the Tropical Atlantic, SR and PD showed the same patterns in relation
to explanatory variables, with both dimensions being positively affected by
estuary area and dissolved oxygen levels. Estuary size and area are typically
related to geomorphology, rivers runoff and entrance regimes, often having a
greater degree of marine influence, which could explain why both SR and PD
increased with total area (Harrison & Whitfield, 2006). Furthermore, larger
systems tend to have high structural complexity, mainly represented by the great
diversity of habitat types found within, such as mangroves, seagrass beds,
saltmarshes, mudflats, and coastal sandy beaches (Sheaves et al., 2014). Each
one of these habitat types has its own characteristics and dynamics, creating a
highly complex mosaic that shapes the estuarine biota and not only attracts a
greater number of species, but also distinct phylogenetic lineages with different
habitat selection mechanisms (Pihl et al., 2007; Larmuseau et al., 2011). The
positive relationship between SR and PD with dissolved oxygen levels was also
expected, as oxygen is required for aerobic metabolism, and is typically related
to higher diversity of prey items for estuarine fish species (i.e. macrobenthic
faunal) (Islam et al., 2013).
Additionally, precipitation was also a significant driver of SR and PD in the
Tropical Atlantic, with greater rainfall rates being negatively correlated to both
dimensions. While would be expect that regions with stronger rainfall regimes
would host greater numbers of species, since rainfall is typically associated to
increases in productive levels of estuaries (Krumme et al., 2012; da Silva et al.,
2018), recent studies have addressed how intricate seasonality may be for
tropical areas. For instance, throughout the Tropical Atlantic, rainfall frequency
and volume may create a process called “estuarization”, which is characterized
by the extension of estuarine conditions to the coastal ecosystem (Longhurst &
Pauly, 1987; Blaber et al., 1997; Barletta et al., 2003). This process, which has
been documented in many regions in the Tropical Atlantic realm, such as the
Guiana shelf (McConnell, 1962), the Gulf of the Mexico (Chittenden, 1976;
Yanez-Arancibia, 1985) and the Northeastern Brazil, creates a temporal corridor
that allows estuarine species to leave estuaries and inhabit adjacent coastal

107

areas, thus causing a temporal decrease in the number of species in the
estuarine zone. Nonetheless, even though it appears that this dynamic is a key
component of both ecosystems – enhancing the connectivity between estuarine
and coastal zones – (Passos et al., 2016; da Silva & Fabré, 2019), authors have
also discussed that future climatic changes may jeopardize the stability and
resilience of this process by intensifying rainfall regimes and producing a
permanent homogenization of both ecosystems, thus affecting their functionality.
Indeed, studies carried out in this region have already shown that narrow shelves
may facilitate the transit of estuarine species to coastal areas, enhancing the
functional diversity of coastal assemblages, but negatively impacting the
functional structure of estuaries (Passos et al., 2016). This process may also
explain why FD was positively correlated to continental shelf width, as
estuarization tends to be weaker at larger shelves (Lowe-McConnell, 1987).
On the order hand, precipitation was one of the main drivers of all diversity
dimensions in the Temperate South America, having a positive effect along with
estuary mouth width. Both variables can be linked to the connectivity between
the estuarine systems and the ocean, which have direct impacts on the
structuring of assemblages. Studies carried out along the Temperate South
America have shown a significant prevalence of marine species in the estuarine
fauna, with rare occurrence or total absence of freshwater species (Garcia et al.,
2001; Vilar et al., 2011). This not only results from the higher salinity profile that
estuaries have in these areas (i.e. Paranaguá estuarine complex), but also from
the close relationship between precipitation and productivity (Blaber & Barletta,
2016). At normal condition, rainfall regimes in this realm are associated to greater
productivity in estuarine areas by stimulating phytoplankton growth and
increasing photosynthetic efficiency (Vizzo et al., 2021). The growth in
productivity attracts marine species from coastal zone, rising the number of
species as well as the phylogenetic and functional complexity of these
ecosystems (Mouchet et al., 2013). In addition, the absence of a significant
relationship between temperature and diversity dimensions in this realm might be
unexpected as a great variability on the temperature profile occurs throughout

108

the whole realm, but it is important to acknowledge that only a small number of
estuarine systems in the southern portion of this region have been studied, which
may have masked the effect of this variable in our analyzes. Nevertheless, it is
important to highlight that latitude had also a significant effect on dimensions,
which can be related to the environmental conditions from the south portion of
this province which is very distinct from the north portion.
In conclusion, our study suggests that distinct environmental profiles
among biogeographic regions are drivers of change for the components of
estuarine fish diversity along the Western Atlantic, with dimensions responding
differently to environmental gradients depend on the spatial scale. Although at
broader scale diversity dimensions appear to have similar responses to variables
related to historical and isolation patterns (i.e. temperature and connectivity
between estuary and the sea), our results show that at smaller scales
arrangements in each dimension may vary according to distinct environmental
features of regions. This observed pattern is crucial to the planning and
management of estuarine ecosystems, which have been undergone unprecedent
levels of human-induced impacts. Our results highlight that conservation actions
should take in consideration regional features when designing and implementing
management strategies for species and ecosystems.

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118

6. DISCUSSÃO GERAL
Nosso estudo sugere que diferentes fatores influenciam a composição
específica e funcionalidade de ambientes estuarino-costeiros, evidenciando o
efeito da escala espacial na compreensão dos padrões que regem a
biodiversidade destes ecossistemas. A nível local, foi possível identificar que em
regiões tropicais ,a diversidade de habitats em ambientes costeiros em conjunto
com a sazonalidade atuam em um processo sinérgico, permitindo um rearranjo
espacial e temporal de diferentes conjunto de espécies, enriquecendo a
composição funcional e filogenética desses ambientes (DA SILVA et al., 2022;
DA SILVA; DOLBETH; FABRÉ, 2021). Tal padrão de ocupação temporal e
espacial diferenciada já havia sido evidenciado também em outras regiões
tropicais do Atlântico Ocidental (AGUILAR-MEDRANO; HERNÁNDEZ DE
SANTILLANA; VEGA-CENDEJAS, 2020), indicando que a existência de
mosaicos costeiros nesta região são de grande importância para o
funcionamento ecossistêmico destas áreas.
Contudo, a nível regional, diferentes combinações de fatores estão
relacionadas com as dimensões da diversidade de peixes nas escalas macro
(todo o Atlântico Ocidental) e meso (para cada domínio biogeográfico). No geral,
as dimensões da diversidade regional de peixes estuarino-costeiros foram todas
correlacionadas com a largura da boca do estuário e a temperatura da superfície
do mar, com entradas mais amplas e águas mais quentes apresentando os
maiores valores de diversidade taxonômica (DT), filogenética (DP) e funcional
(DF). Ambas as variáveis foram anteriormente destacadas nos trabalhos de
Henriques et al., (2017a,b) como um dos principais fatores estruturantes da
composição de espécies e traços na escala global. Os gradientes de temperatura
parecem atuar como um determinante da composição especifica regional destas
áreas, impondo condições adequadas ou inadequadas para um conjunto distinto
de espécies, selecionando as populações e suas características com base em
suas tolerâncias fisiológicas, o que parece estar relacionado à história
filogenética das espécies, pois DP também responde positivamente a essa
variável (HENRIQUES et al., 2017a, 2017b). Da mesma forma, a maior

119

conectividade com o mar permite a ocorrência de espécies marinhas com
diferentes conjuntos de características que potencializam a DF nessas áreas,
desempenhando um papel crucial na escala regional atuando como conectoras
entre a escala local e global pela sua capacidade de dispersão.
De fato, a nível local, nosso estudo evidenciou que esta conectividade
entre estuários e outros habitats costeiros é de extrema importância para a
manutenção da funcionalidade ecossistêmica, atuando principalmente no
incremento de redundância das funções chaves. Estudos prévios já haviam
identificado que a ocorrência de espécies marinhas de forma ocasional em
estuários e outros habitats costeiros aumentam a diferenciação de nichos (DA
SILVA;

FABRÉ,

2019).

Todavia,

resultados

apresentados

aqui

complementam tal informação indicando que tal ocorrência é resultado de um
efeito sinérgico entre a diversidade de habitats e os regimes sazonais que
permitem que diferentes conjuntos de espécies habitem os distintos habitats que
compõem os mosaicos costeiros ao longo da dinâmica natural desses
ecossistemas.
Contudo, é importante evidenciar que os padrões identificados podem
sofrer alterações diante do atual cenário que vivemos (MAHONEY; BISHOP,
2017). As mudanças climáticas, por exemplo, têm grande potencial para afetar
as variáveis que influenciam as diferentes dimensões da diversidade de peixes
nestas áreas, tais como temperatura da superfície do mar, níveis de clorofila e o
regime de chuvas. Nas provinciais temperadas, as mudanças na temperatura
dos oceanos podem atuar não apenas na criação de barreiras que limitem a
persistência de espécies locais, apresentando também grande potencial para o
surgimento de corredores térmicos que permitam a ocorrência de espécies de
outras regiões (DE QUEIROZ et al., 2018; PEÑA RIVAS; AZZURRO; LLORIS,
2013), alterando o pool de espécies regional e podendo modificar toda a
dinâmica ecossistêmica destas áreas.
Em regiões tropicais, um aumento das chuvas, especialmente durante a
estação seca, impactaria o escoamento de água doce e o abastecimento de
sedimentos, eventualmente causando uma homogeneização de habitats

120

estuarino-costeiros e interferindo na dinâmica identificada no nosso estudo
(BERNARDINO et al., 2015; MARENGO et al., 2010). Embora uma
homogeneização

temporária

pareça

ser

componente-chave

funcionamento do ecossistema estuarino, aumentando a conectividade do
habitat e facilitando os movimentos das espécies, a homogeneização
permanente impactaria a integridade individual dos habitats, alterando suas
características e condições, afetando as espécies que habitam essas áreas
(GARTNER et al., 2013). Por exemplo, nosso estudo demonstrou que peixes
dependentes de estuários tendem a usar diferentes habitats à medida que
crescem para completar seu ciclo de vida (DA SILVA et al., 2022). Assim, uma
homogeneização permanente afetaria a dinâmica dessas espécies e interferiria
em seu processo de desenvolvimento (NAGELKERKEN et al., 2008, 2015).
Sendo assim, considerando a vulnerabilidade dos habitats estuarinos e
costeiros ao longo do Atlântico, e sua importância para muitas espécies de
peixes, estratégias de conservação devem levar em consideração um conjunto
de variáveis de natureza local e regional. A perspectiva do mosaico de habitats,
por exemplo, é uma ferramenta que pode ser importante para reconsiderar as
limitações das áreas de conservação. Por esta razão, a proteção integrada de
diferentes habitats representa uma estratégia imperativa para sustentar a
complexidade das áreas costeiras, altamente produtivas para a pesca e
fundamentais para manter os meios de subsistência.

121

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123

8. ANEXOS
Supplementary information for
Biogeographic patterns in the diversity dimensions of estuarine fish
assemblages from the Western Atlantic
Victor E. L. da Silva1, Marina Dolbeth2, Nidia N. Fabré1
1

Laboratório de Ecologia, Peixes e Pesca – Instituto de Ciências Biológicas e

da Saúde, Universidade Federal de Alagoas, Maceió, Brazil
2

Interdisciplinary Centre of Marine and Environmental Research - CIIMAR,

Universidade do Porto, Matosinhos, Portugal
Supporting Information Content
Figure S1
Table S1

124

Fig. S1 – Pearson’s correlation for explanatory variables in the Western Atlantic
(A), and its respective biogeographic realms (B–D).

125

Table S1. Effect and significance of explanatory variables in each dimension of fish diversity for biogeographic realms of the Western
Atlantic.

Variable
Estuary area
Mouth width
Shelf width
Chlorophyll
Current velocity
Dissolved
oxygen
Precipitation
Salinity
Sea surface
temperature

SR
Ef.
+
+
-

p
0.092
0.009
0.046
0.022
0.409

0.965
0.851
0.000

TNA
TA
TSA
PD
FD
SR
PD
FD
SR
PD
FD
Ef.
p
Ef.
p
Ef.
p
Ef.
p
Ef.
p
Ef.
p
Ef.
p
Ef.
p
0.098
0.076 + 0.004 + 0.006
0.063
+ 0.017 + 0.021
+ 0.012 + 0.038 + 0.311
+ 0.353 + 0.013
0.078
0.198 + 0.006
- 0.041 - 0.015
0.312
0.697
0.615 - 0.018
0.052 - 0.035
0.438
0.526
0.397
0.155
0.949
+ 0.021 + 0.031
0.134

0.756
0.903
0.000

0.811
0.991
0.000

0.291
0.714
0.237

0.024
0.593
0.081

0.103
0.883
0.066

0.000
0.391

0.000
0.146

0.000
0.947