Jordana Rangely Almeida Santos de Oliveira

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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

JORDANA RANGELY ALMEIDA SANTOS DE OLIVEIRA

PLASTICIDADE INDIVIDUAL E INTERESPECÍFICA NA HISTÓRIA DE VIDA DE
ESPÉCIES DE MUGIL (TAINHAS) QUE CO-OCORREM EM AMBIENTES TROPICAIS:
IMPLICAÇÕES PARA O MANEJO E CONSERVAÇÃO.

MACEIÓ - ALAGOAS
Novembro/2024

JORDANA RANGELY ALMEIDA SANTOS DE OLIVEIRA

PLASTICIDADE INDIVIDUAL E INTERESPECÍFICA NA HISTÓRIA DE VIDA DE
ESPÉCIES DE MUGIL (TAINHAS) QUE CO-OCORREM EM AMBIENTES TROPICAIS:
IMPLICAÇÕES PARA O MANEJO E CONSERVAÇÃO.

Dissertação/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
Mestre/Doutor em CIÊNCIAS BIOLÓGICAS, área de
concentração em Conservação da Biodiversidade
Tropical.

Orientadora: Profa. Dra. Nídia Noemi Fabré

MACEIÓ - ALAGOAS
Novembro/2024

Catalogação na Fonte
Universidade Federal de Alagoas
Biblioteca Central
Divisão de Tratamento Técnico
O48p

Bibliotecária: Betânia Almeida dos Santos – CRB-4 – 1428
Oliveira, Jordana Rangely Almeida Santos de.
Plasticidade individual e interespecífica na história de vida de espécies
de Mugil (tainhas) que co-ocorrem em ambientes tropicais: implicações
para o manejo e conservação / Jordana Rangely Almeida Santos de
Oliveira. – Maceió, 2024.
183 f. : il.
Orientadora: Nídia Noemi Fabré.
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, 2024.
Bibliografia: f. 182-183.
1. Tainha(peixe). 2. Tainha – migração parcial . 3. Crescimento
sazonal. 4. Tainha – habitat – manejo e conservação. 5. Mugil – otólito.
I. Título.
CDU: 57:597.593

Folha de aprovação
Jordana Rangely Almeida Santos de Oliveira
Plasticidade individual e interespecífica na história de vida de espécies
de Mugil (tainhas) que co-ocorrem em ambientes tropicais:
implicações para o manejo e conservação.
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 Doutora em CIÊNCIAS
BIOLÓGICAS,
área
de
concentração
em
Conservação da Biodiversidade Tropical.

________________________________________________________________
Prof. Dra Nídia Noemi Fabré/UFAL
(orientadora)
Tese aprovada em 08 de novembro de 2024.

________________________________________________________________
Prof. Dr. Claudio Luís Santos Sampaio / UFAL

________________________________________________________________
Dra Alejandra V. Volpedo

________________________________________________________________
Dr. Francisco Marcante Santana da Silva / UFRPE

___________________________________________________________________
Dra Silvina Botta/ FURG
MACEIÓ - AL
Novembro / 2024

DEDICATÓRIA

Dedico esta tese aos meus amados, que foram meu alicerce e maior incentivo ao
longo de cada etapa desta jornada: Passos Jr., Leonardo Passos, Gabriel Passos, Rosa
Maria, Juarez Santos, Juliano Rodrigo, Mariana Lopes, Maria Eduarda Lopes e Isabela
Lopes. Vocês são a mais valiosa rede de apoio que eu poderia desejar. Mesmo
enfrentando minhas ausências durante o processo de pesquisa, estiveram sempre
presentes com amor e paciência, compartilhando comigo os desafios e as conquistas
dessa jornada. Essa vitória é, sem dúvida, também de vocês.

AGRADECIMENTOS
A Deus, toda a honra e toda a glória. Foi Ele quem me fortaleceu nos momentos
difíceis, iluminou meu caminho e me permitiu chegar até aqui.
A ideia do doutorado nasceu muito antes de eu ser aprovada na seleção. Lembrome da primeira vez que ouvi alguém dizer que eu seria doutora. Foi meu pai, em Foz do
Iguaçu, no ano de 2001. Ele me disse: 'Filha, invisto mais do que posso na sua educação
e sou muito criticado por isso. Mas seguirei adiante, porque mato um leão por dia para
garantir que você e seu irmão sejam doutores.' As palavras de um pai têm poder, e essa
foi uma verdadeira virada de chave na minha vida. Naquele momento, compreendi que
precisava honrar o sacrifício dos meus pais e retribuir todo o esforço que fizeram por mim.
Os anos se passaram, e a oportunidade finalmente chegou. No entanto, eu ainda
me perguntava se seria capaz de lidar com tantos desafios. Foi nesse momento que minha
mãe foi a minha maior incentivadora, sempre me encorajando a seguir em frente. Além
dela, o apoio incondicional do Passos Júnior foi crucial. Sua confiança em mim foi
essencial, assim como a compreensão dos meus filhos, Léo e Gabriel. Os três
mergulharam comigo nessa trajetória, enfrentando cada etapa ao meu lado, sendo meu
porto seguro, minha motivação diária e parte fundamental dessa conquista.
À minha orientadora, Dra. Nidia Noemi Fabré. Dizem que a relação entre orientador
e orientando é como um casamento, e o nosso já alcançou bodas de porcelana. São 20
anos de aprendizado e superação de desafios. A professora Nídia me ensinou muito mais
do que Biologia; ela abriu as portas do mundo para que hoje eu pudesse ser a professora
Jordana. Sua dedicação, apoio e ensinamentos foram fundamentais na minha trajetória,
e por isso sou imensamente grata.
Ao professor Vandick Batista, pelo acompanhamento, pelas ideias valiosas e, acima
de tudo, por me incentivar a refletir sobre cada etapa do processo. Obrigada por me
ensinar que sempre posso ir além, fazer mais e melhor, e por me mostrar a importância
de aproveitar ao máximo o tempo disponível para realizar um bom trabalho.
Ao meu orientador francês, professor Dr. Fabrice Duponchelle, por abrir as portas
do seu laboratório no Marbec da Université de Montpellier. Sua orientação foi essencial

para minha formação, ensinando-me sobre microbiologia e leitura de anéis de
crescimento, além de continuar me orientando, mesmo após meu retorno ao Brasil.
Ao Dr. Miller, da Universidade do Texas, cuja contribuição foi indispensável para a
realização da microquímica dos otólitos.
Aos meus amigos do LAEPP/LACOM/UFAL, é impossível expressar em palavras o
impacto que vocês tiveram na minha jornada acadêmica. Foram incontáveis
ensinamentos, debates e apoio incondicional de diversas formas. Meu respeito e gratidão
a cada um de vocês: Diogo, Reginaldo, Jessika, Erick, Victor, Daniele, Gilmar, Samantha,
Rafael, Aline, Fernando, Janaina, Morgana, Myrna, Mônica, Aninha, Matheus.
No meu primeiro dia de aula no PPG, minha amiga Morgana Macedo me disse:
"Jorda, o processo é difícil, mas quando Deus vê uma mãe nessa luta, Ele abre as portas
do céu e manda um anjo." E Ele realmente enviou: Matheus de Barros, um grande amigo
e coautor, sem o qual eu não teria conseguido chegar até aqui. Matheus, sua ajuda foi
inestimável, e sou imensamente grata por tudo.
Aos meus queridos amigos das noites mediterrâneas – Josy, Jardi, Naná e Beto –,
que tornam a vida mais leve, divertida e dinâmica, e que sempre acreditaram no meu
potencial. À minha grande amiga, irmã e comadre Cibele Tiburtino, por suas conversas
leves e conselhos que sempre me fazem sorrir e mantar a sanidade mental.
Às minhas primas Cristina Basílio, Daniele e Franciele Gonzales, que, mesmo a
quilômetros de distância, sempre torceram por mim.
À minha comunidade de fé, a Igreja Batista Betel, por me lembrar constantemente
que Deus está à frente de tudo. Por orar por mim em cada etapa e me ajudar em um dos
momentos mais difíceis durante todo esse processo.
Aos queridos familiares que me acolheram na Europa e tornaram possível um dos
meus maiores sonhos: fazer um intercâmbio junto à minha família. Paula, Beto, Hadassa
e Herbert, de Lisboa, vocês foram essenciais e têm minha eterna gratidão. Meus primos
queridos Márcia e Jesus, em Santa Pola, vocês fizeram muito mais do que eu poderia
sonhar, o nosso tempo juntos foi precioso, um presente.

Aos queridos professores da banca examinadora, que me acompanharam ao longo
do meu processo formativo: Alejandra V. Volpedo, Silvina, Silvina Botta, Claudio Luís
Santos Sampaio (Buia), Francisco Marcante Santana da Silva (Chico), Ladle Richard e
Ana Malhado. Obrigada por suas valiosas contribuições!
Ao professor Naércio Aquino Menezes, que há anos me ensinou a identificar as
tainhas, e ao professor Esteban Avigliano, cuja colaboração foi importante para a
realização da microquímica.
Ao IFAL, minha casa, por conceder a licença necessária para a realização da minha
tese e, mais do que isso, por oferecer suporte durante meu intercâmbio. Sou privilegiada
por trabalhar em uma instituição que valoriza a formação de seus servidores, e espero
retribuir à altura, incentivando também os meus alunos a buscarem sempre mais.
À FAPEAL, pela concessão da bolsa de pesquisa e pelos dois prêmios de
excelência acadêmica. Ao CNPq e à CAPES, pelo apoio financeiro.
Ao Programa Ecológico de Longa Duração da Área de Proteção Ambiental Costa
dos Corais Alagoas (PELD APACC-AL), que eu participei durante toda minha formação e
que agora continuo integrando como professora e pesquisadora.
Ao laboratório Misto Internacional (LMI) Tapioca (Tropical Atlantic Interdisciplinary
Laboratory on Physical, Biogeochemical, Ecological and Human Dynamics), pelo suporte
científico e financeiro importantes para o desenvolvimento desta tese e principalmente
para o intercâmbio para França.
Ao PPG-DIBICT e a todos que fazem parte dele, desde os professores que foram
fundamentais na minha formação até meus colegas, cujas discussões e momentos
compartilhados enriqueceram minha jornada. Cada troca de conhecimento e aprendizado
foi essencial para a conclusão deste processo.
Aos grandes mestres dos mares, os pescadores, que, com sua sabedoria e
experiência, me ensinaram na prática sobre as tainhas e os mistérios do mar. Sua
generosidade em compartilhar conhecimento foi essencial para esta jornada.
A todos que, de alguma forma, contribuíram para esta caminhada, meu mais
sincero e profundo agradecimento.

Àquele que é capaz de fazer infinitamente mais
do que tudo o que pedimos ou pensamos, de
acordo com o seu poder que atua em nós.
Efésios 3:20

RESUMO
A plasticidade individual e variabilidade interespecífica desempenham um papel crucial na
capacidade dos peixes de responder a mudanças ambientais o que influencia o ciclo de
vida, como crescimento e maturação sexual. Em espécies congenéricas e
morfologicamente semelhantes, esses mecanismos de plasticidade podem permitir a
coexistência, gerando divergências sutis nas características da história de vida. O objetivo
geral desta tese foi avaliar os traços de história de vida de forma interespecífica e a
plasticidade individual no uso do habitat de espécies de Mugil que co-ocorrem em
ambientes tropicais, verificando as implicações para o manejo e conservação. Para tanto,
indivíduos de três espécies de Mugil foram capturados em quarto estuários tropicais e os
seus otólitos foram utilizados, tanto para mensurar a idade quanto para fazer uma
cronologia química dos primeiros estágios de vida. A pesquisa foi estruturada em quatro
capítulos complementares que abordam diferentes aspectos da ecologia populacional e
pesca. No primeiro, foram discutidos mecanismos de coexistência entre as espécies,
relacionados a fatores abióticos. Verificou-se que M. curema é influenciada por fatores
como temperatura, oxigênio dissolvido e turbidez e ocupa três ambientes durante a
primeira fase do ciclo de vida enquanto M. rubrioculus é mais afetada pela variação na
salinidade e se restrige à parte externa do estuário e ao mar. Então, apesar de
filogeneticamente próximas, as duas espécies exibem diferentes padrões de uso do
habitat. O segundo capítulo investiga o crescimento polifásico alométrico em otólitos, que
se mostrou um bom indicador de eventos críticos do ciclo de vida, como a maturação
sexual. As espécies de Mugil exibiram diferentes padrões de crescimento e maturação,
sugerindo uma assincronia nos ciclos de vida que facilita a coexistência, sendo que M.
rubrioculus (K = 0,31) apresenta maior velocidade de crescimento e M. liza um
crescimento mais lento (K = 0,21), enquanto M. curema (K=25) é a espécie intermediária.
Foi observado que a velocidade de crescimento possui dois pontos de mudança ao longo
da vida, sendo o segundo associado a migração reprodutiva para o mar. No terceiro
capítulo, foi analisada a dependência estuarina e a plasticidade no uso do habitat. M. liza
foi a espécie que passou mais tempo na fase inicial de vida no estuário. Por outro lado,
M. rubrioculus, apresentou menor dependência estuarina. M. curema destacou-se pela
maior plasticidade individual no uso de habitats, exibindo maior migração parcial. O quarto
capítulo conclui que M. liza é a espécie mais vulnerável à pesca, com uma redução para
apenas 20% do estoque original. Essa vulnerabilidade pode ser relacionada à sua menor
plasticidade e maior permanência no estuário. O estudo destaca a importância de incluir
o Conhecimento Ecológico Local (LEK) no manejo sustentável das espécies, por meio de
uma abordagem participativa que envolva pescadores, gestores e cientistas. Assim,
conclui-se que a coexistência das espécies de Mugilidae é sustentada por complexos
mecanismos ecológicos, nos quais o uso do habitat e a plasticidade fenotípica
desempenham papéis cruciais. A gestão adequada desses recursos deve considerar a
variabilidade ambiental, as peculiaridades de cada espécie e as interações entre
diferentes agentes sociais, como pescadores, gestores e cientistas pesqueiros, para
promover a sustentabilidade dos estoques pesqueiros de forma horizontal e participativa.
Palavras-chave: trade-off. otólito. crescimento. migração parcial.

ABSTRACT
Individual plasticity and interspecific variability play a crucial role in the ability of fish to
respond to environmental changes which influence the life cycle such as growth and sexual
maturation. In congeneric and morphologically similar species, these plasticity
mechanisms can allow coexistence, generating subtle divergences in life history
characteristics. The general objective of this thesis was to evaluate interspecific life history
traits and individual plasticity in habitat use of Mugil species that co-occur in tropical
environments, verifying the implications for management and conservation. To this end,
individuals of three Mugil species were captured in four tropical estuaries and their otoliths
were used, both to measure age and to make a chemical chronology of the first stages of
life. The research was structured into four complementary chapters that address different
aspects of population ecology and fishing. In the first, mechanisms of coexistence between
species were discussed, related to abiotic factors. It was found that M. curema is influenced
by factors such as temperature, dissolved oxygen and turbidity and occupies three
environments during the first phase of its life cycle, while M. rubrioculus is more affected
by variations in salinity and is restricted to the external part of the estuary and to the sea.
Therefore, despite being phylogenetically close, the two species exhibit different patterns
of habitat use. The second chapter investigates allometric polyphasic growth in otoliths,
which has been shown to be a good indicator of critical life cycle events such as sexual
maturation. Mugil species exhibited different growth and maturation patterns, suggesting
an asynchrony in life cycles that facilitates coexistence, with M. rubrioculus (K = 0.31)
showing a higher growth speed and M. liza showing slower growth (K = 0.31) K = 0.21),
while M. curema (K=25) is the intermediate species. It was observed that growth speed
has two points of change throughout life, the second being associated with reproductive
migration to the sea. In the third chapter, estuarine dependence and plasticity in habitat
use were analyzed. M. liza was the species that spent the most time in the initial phase of
life in the estuary. On the other hand, M. rubrioculus showed less estuarine dependence.
M. curema stood out for its greater individual plasticity in habitat use, exhibiting greater
partial migration. The fourth chapter concludes that M. liza is the species most vulnerable
to fishing, with a reduction to just 20% of the original stock. This vulnerability may be related
to its lower plasticity and longer stay in the estuary. The study highlights the importance of
including Local Ecological Knowledge (LEK) in the sustainable management of species,
through a participatory approach that involves fishermen, managers and scientists. Thus,
it is concluded that the coexistence of Mugilidae species is sustained by complex
ecological mechanisms, in which habitat use and phenotypic plasticity play crucial roles.
The appropriate management of these resources must consider environmental variability,
the peculiarities of each species and the interactions between different social agents, such
as fishermen, managers and fisheries scientists, to promote the sustainability of fishing
stocks in a horizontal and participatory way.
Key-word: trade-off. otolith. growth. partial migration.

LISTA DE FIGURAS
Figura 2.1 - Espécies do gênero Mugil que coexistem em estuários tropicais. De cima para
baixo: M. curvidens, M. brevirostris, M. curema, M. rubrioculus e M. liza. Fotos: equipe do
Laboratório de Ecologia de Peixes e Pesca da UFAL.......................................................28
Figura 2.2 – Esquema representativo do ciclo de vida dos Mugil. Fonte: equipe do
Laboratório de Ecologia de Peixes e Pesca da UFAL......................................................30
Figura 2.3 - Micrografia eletrônica de otólitos sagittae de M. brevirostris, M. curvidens, M.
curema, M. rubrioculus e M. liza. Fotos: equipe do Laboratório de Ecologia de Peixes e
Pesca da UFAL.................................................................................................................33
Figura 2.4 - Otólitos sagittae inteiros de M. liza, M. curema e M. rubrioculus. Mostrando o
núcleo opaco (seta) e as sucessivas zonas translúcidas e opacas que formam os anéis de
crescimento. Fotos: equipe do Laboratório de Ecologia de Peixes da UFAL..................34
Figura 2.5 – Otólito sagitae de M. curema seccionado pelo isomet, emblocado em resina,
e posteriormente polido (A) e corado (B). Fotos: Jordana Rangely.................................35
Figure 3.1. Map showing the sampling points within the Mundau Lagoon, Northwestern
Atlantic……………………………………………………………………………………………66
Figure 3.2. Monthly variation in environmental parameters measured at different regions of
the Mundau Lagoon, Northwestern Atlantic……………………………………………….….69
Figure 3.3. Spatial and temporal variation in abundance (counts) of white and redeye
mullets at the Munda Lagoon, north-western Atlantic. The vertical axis shows the logtransformed means and two standard errors of mullet counts……………………………..70
Figure 3.4. Posterior predictive check for the Bayesian zero-inflated generalised linear
models fit to count data of white (top) and redeye (bottom) mullet species sampled at the
Mundaú Lagoon, north-western Atlantic. Individual data points represent observed
quantities and coloured lines are median model fits………………………………………...71
Figure 3.5. Influence of environmental parameters on the abundance of white and redeye
mullets within the Mundaú Lagoon, north-western Atlantic. Points represent Bayesian
posterior medians from the zero-inflated models and lines represent the 80% credible
intervals after 500,000 iterations. DO, dissolved oxygen…………………………………..73
Figure 3.6. Infographic illustrating the spatial-temporal movements of white and redeye
mullet M.curema and M. rubrioculus in the Mundaú Lagoon, north-western Atlantic……74
Figure 4.1. Map of the sampling locations in the tropical Southwestern Atlantic: Mundau
Lagoon (lower panel), and Santo Antonio River (upper panel)……………………………89
Figure 4.2. Sagitta otoliths from Mugil liza, M. curema and M. rubrioculus and their annual
growth rings…………………………………………………………………………….………..92
Figure 4.3. Size structures for the lebranche mullet M. liza, white mullet M. curema, and
redeye mullet M. rubrioculus caught in the study locations…………………………………95
Figure 4.4. Monthly marginal relative increment (MRI %) for the lebranche mullet M. liza,
white mullet M. curema, and redeye mullet M. rubrioculus caught in the study locations. A
posteriori multiple comparisons indicate significant differences in the month of February for
the lebranche and white mullets, and in August for the redeye mullet……………………...97
Figure 4.5. From top to bottom, for the lebranche mullet M. liza, white mullet M. curema,
and redeye mullet M. rubrioculus: relationship between otolith radius (OR)- mm) and total
length (TL), standardized residuals of the power regression between OR and TL,

polynomial fit of the relationship between OR and the allometric coefficient (b), and
relationship between the derivative of the polynomial model (b’) and OR………………..98
Figure 4.6. Length-at-age plots, von Bertalanffy growth curves fitted to back-calculated
lengths, age-converted SCPs from the polyphasic growth models and 95% confidence
intervals for the age at maturity (A50) for the three studied species. Note the different y-axis
scales because of significant size differences between lebranche mullet and the other
species…………………………………………………………………………………..……….99
Figure 5.1. Means and standard deviations (SD) of Sr:Ca (mmol.mol-1); in otoliths of Mugil
liza, M. curema and M. rubrioculus caught in estuaries of northeastern Brazil. See
Appendix for Sr:Ca ratios at the core vs whole transect profile…………………………..126
Figure 5.2. interspecific plasticity in relation to the use of coastal environments, in the first
phase of the life cycle (Rangely et al. 2023) GAM residues from the strontium ratio during
the first year of life……………………………………………………………………………..126
Figure 5.3. Variations in Sr:Ca ratios from core to edge of otoliths (birth-to-capture) of M.
curema, M. rubrioculus and M. liza, with colour representing corresponding age along the
ablation path. Red dotted lines are lower (5.0 × 10−3 ) and upper (7.4 × 10−3 ) bounds of
the estuarine zone. See Appendix A for individual plots of Sr:Ca ratios Data from LAICPMS…………………………………………………………………………………………..128
Figure 5.4. Relative frequency of individuals of each species (M. liza, M. curema and M.
rubrioculus) in each of the six habitat use categories……………………………………..129
Figure 5.1.1. – Microchemical profiles of otoliths of 52 Mugil curema from the Northeast
coast of Brazil. Red dotted lines are lower (5.0 × 10−3) and upper (7.4 × 10−3) bounds of
the estuarine zone. Data from LA-ICPMS………………………………………………….144
Figure 5.1.2. – Microchemical profiles of otoliths of 49 Mugil rubrioculus from the Northeast
coast of Brazil. Red dotted lines are lower (5.0 × 10−3) and upper (7.4 × 10−3) bounds of
the estuarine zone. Data from LA-ICPMS……………………………………………….…..145
Figure 5.1.3. Microchemical profiles of otoliths of 12 Mugil liza from the Northeast coast of
Brazil. Red dotted lines are lower (5.0 × 10−3) and upper (7.4 × 10−3) bounds of the
estuarine zone. Data from LA-ICPMS………………………………………………………146
Figure 6.1. Sampling locations of mullet in the Tropical Southwestern Atlantic: Santo
Antonio River (upper point) and Mundaú Lagoon (middle point) and Manguaba Lagoon
(lower point), Alagoas state, Brazil…………………………………………………………..152
Figure 6.2. Length frequency data of populations of three mullet species: Mugil rubrioculus,
M. curema and M. liza………………………………………………………………………….158
Figure 6.3. The top curves depict the LBB model’s fit to the length data, and the bottom
curves depict the LBB method’s prediction, where Lc denotes the length of 50% of the
individuals caught, L∞ is the asymptotic length, and Lopt is the length when the maximum
sustainable yield is achieved…………………………………………………………………159
Figure 6.4. Density distribution of fishers’ responses on Lopt (A) and L50 (B) values for the
three Mugil species. The red bars indicate the values estimated CSK (the LBB model) of
Lopt (A) and L50 (B). The distribution of responses given by fishermen for M. rubrioculus,
M. curema, and M. liza is represented by the colours blue, gray and green
respectively…………………………………………………………………………….………162

LISTA DE TABELAS

Table 3.1. Summary of posterior distributions for the random-effects zero-inflated model
parameters for predicting the abundance of M. curema and M. rubrioculus. 80% credible
intervals were selected according to criteria for hypothesis testing within a Bayesian
framework. Values highlighted in bold denote a “significant” effect. “Mullet” refers to the
coefficient for the abundance of the congeneric species affecting the other………..……72
Table 4.1. Output of the generalized linear models (GLMs) for the influence of rainfall and
condition factor on the annuli formation (IMR) for the three species………………………94
Table 4.2. Life history parameters and 95% confidence intervals obtained for the studied
species. A50 = age at first maturity, A95 = longevity, L50 = size at first maturity, L∞ = von
Bertalanffy asymptotic length, k = von Bertalanffy growth rate…………………………...104
Table 4.3. von Bertalanffy growth parameters for each studied species gathered from the
literature…………………………………………………………………………………………123
Table 5.1. Life history traits of stock assessments and respective questions used to assess
LEK………………………………………………………………………………………………156
Table 5.2. Outputs of the Length-Based Bayesian Biomass (LBB) for Mugil rubrioculus, M.
curema and M. liza. Quantities are displayed as medians and 95% credible intervals of
Bayesian posterior distributions. Z stands for total mortality rates (year-1), Lc stands for the
length at first capture, Lc_opt stands for the optimal length at first capture, K and L∞ are von
Bertalanffy growth parameters, B stands for current biomass, B0 stands for the virgin
Table 5.3. SWOT matrix composed of Positive vs negative points and internal vs. external
factors associated with overexploitation…………………………………………………….160
or unexploited biomass, BMSY stands for the biomass at the maximum sustainable yield,
and simple capture structuring indicators…………………………………………………...166

SUMÁRIO
1 Apresentação............................................................................................................. 17
Referências ................................................................................................................... 19
2 Revisão da literatura ................................................................................................. 21
2.1 História de vida ....................................................................................................... 21
2.2 Plasticidade individual em peixes ........................................................................ 22
2.3 Trade-off em peixes................................................................................................ 24
2.4 Mugilidae ................................................................................................................. 26
2.4.1 Reprodução e migração de Mugil ...................................................................... 29
2.4. 2 Crescimento, idade e microquímica de otólitos .............................................. 32
2.5 Pesca Artesanal ...................................................................................................... 38
2.5.1 Pescarias com dados limitados ......................................................................... 39
2.5.2 Conhecimento Ecológico Local (LEK).............................................................. 40
2.5.3 Pesca de tainhas ................................................................................................. 42
2.6 Referências ............................................................................................................. 45
3 Congeneric, sympatric tropical mullets respond differently to environmental
variability: insights into coexistence .......................................................................... 61
3.1 Abstract ................................................................................................................... 62
3.2 Introduction ............................................................................................................ 63
3.3 Materials and methods........................................................................................... 65
3.3.1 Study area and sampling .................................................................................... 65
3.3. 2 Data analysis ...................................................................................................... 66
3.4 Results .................................................................................................................... 69
3.5 Discussion .............................................................................................................. 73
3.6 Conclusions ............................................................................................................ 77
3.7 Acknowledgements ................................................................................................ 77
3.8 References .............................................................................................................. 78
4 Assessing interspecific variation in life-history traits of three sympatric tropical
mullets using age, growth and otolith allometry ....................................................... 85
4.1 Abstract ................................................................................................................... 86
4.2 Introduction ............................................................................................................ 87
4.3 Materials and methods........................................................................................... 89
4.3.1 Study area and sampling collection .................................................................. 89
4.3. 2 Otolith polyphasic allometric patterns ............................................................. 90
4.3. 3 Otolith macrostructure and age determination ............................................... 91
4.3. 4 Growth rate and asymptotic size ..................................................................... 93
4.3. 5 Hypothesis testing...............................................................................................93
4.4 Results .................................................................................................................... 94
4.5 Discussion ............................................................................................................ 100
4.5.1 Fine-scale variation in life-history explained by otolith allometry, age and
growth ......................................................................................................................... 100
4.5.2 Age and growth ................................................................................................ 103
4.5.3 Implications for fisheries management .......................................................... 105
4.6 Conclusions .......................................................................................................... 106

4.7 Acknowledgements .............................................................................................. 106
4.8 References ............................................................................................................ 107
5 Individual and interspecific plasticity in the life history of three sympatric mugil
species in tropical environments: implications for management and conservation
………………………………………………………………………………………………….117
5.1 Abstract ................................................................................................................. 118
5.2 Introduction .......................................................................................................... 119
5.3 Materials and methods......................................................................................... 121
5.3.1 Study area and sampling collection ................................................................ 121
5.3. 2 Otolith macrostructure..................................................................................... 122
5.3. 3 Microchemistry of otoliths ............................................................................... 122
5.3. 4 Fish ageing ...................................................................................................... 124
5.3. 5 Data analysis......................................................................................................124
5.4 Results .................................................................................................................. 125
5.5 Discussion ............................................................................................................ 129
5.5.1 Management and conservation of species .................................................... 132
5.6 Acknowledgements .............................................................................................. 133
5.7 References ............................................................................................................ 134
5.8 Appendix ............................................................................................................... 144
6 Joining data-limited stock assessment and traditional ecological knowledge to
inform tropical mullet management .......................................................................... 147
6.1 Abstract ................................................................................................................. 148
6.2 Introduction .......................................................................................................... 149
6.3 Materials and methods......................................................................................... 150
6.3.1 Sampling collection........................................................................................... 150
6.3.2 Conventional Scientific Knowledge (CSK) ...................................................... 152
6.3. 2.1 The length-based Bayesian biomass (LBB) assessment model ............... 153
6.3. 3. Local Ecological Knowledge (LEK) ............................................................... 155
6.3. 3.1 Data collection….............................................................................................155
6.3. 3.2 Data analysis …...............................................................................................156
6.4 Results .................................................................................................................. 158
6.4. 1 Conventional Scientific Knowledge (CSK) ..................................................... 158
6.4. 2 Local Ecological Knowledge (LEK)................................................................. 160
6.4. 3 Overlap between CSK and LEK ....................................................................... 162
6.5 Discussion ............................................................................................................ 163
6.5.1 Good (and Bad) Management Practices ......................................................... 165
6.6 Conclusions .......................................................................................................... 167
6.7 Acknowledgements .............................................................................................. 168
6.8 References ............................................................................................................ 168
7 Discussão geral ....................................................................................................... 178
7.1 Referências ........................................................................................................... 182

1 APRESENTAÇÃO
A história de vida de um organismo compreende o padrão de crescimento, a
diferenciação morfológica, a armazenagem de energia e a reprodução (Begon et al.,
2009, Rochet 2000). A variação no ciclo de vida frequentemente está correlacionada
com esses parâmetros, assim como, com o ambiente em que esse organismo se
desenvolve (Winemiller, 1989, Phillips et al., 2010). Considerando que os organismos
vivem em um mundo finito, o conceito de alocação limitada dos recursos durante o ciclo
de vida permite sustentar hipóteses sobre o destino dos recursos investidos pelo
organismo para uma dada atividade implicarará em tornam-se indisponíveis para outras
(Roff, 1992; Stearns, 1992; Ricklefs, 2003, Begon et al., 2007).
Sendo assim, a alocação de energia para reprodução e crescimento pode
influenciar o desempenho individual e consequentemente a dinâmica populacional (Roff,
1992; Stearns, 1992). Essa relação negativa entre dois traços da história de vida é
chamada de trade-off, e possui um ponto de inflexão de alocação, justamente quando o
indivíduo diminui ou cessa a alocação de energia para um dos traços e investe em outro,
como uma gangorra de alocação. A plasticidade individual também afeta a dinâmica
populacional, permitindo respostas adaptativas às mudanças ambientais por meio de
alterações na fisiologia e comportamento. (Begon, et al., 2007, Wooton, 1990).
Compreender a plasticidade individual e interespecífica da história de vida de
espécies de peixes do género Mugil é fundamental, principalmente se tratando de
espécies congenéricas que co-ocorrem em ecossistemas estuarinos. São espécies de
peixe estuarino-dependentes obrigatórias, que possuem uma área de criação (estuário)
e uma área de reprodução (mar) (Able, 2005, Fowler et al., 2016, Santana et al., 2018).
Dessa forma, essas espécies podem ter o ponto de inflexão do trade-off intimamente
relacionado ao uso de habitat e impactando o desempenho desses organismos. Se
partimos do pressuposto de que a estuarino dependência gera um ponto de inflexão no
ciclo de vida, já que o organismo sai da área de crescimento e parte para a área de
reprodução, seria o momento onde as espécies de Mugil sofrem o impacto do trade-off.
Quanto maior a estuarino-dependência, ou seja, quanto mais tempo eles passam no

estuário, maior é o pré ponto de inflexão e isso poderá se traduzir em maior tamanho.
Assim sendo, a estuarino-dependência poderá explicar diferenças interespecíficas no
crescimento das espécies, pois está relacionada com o pré ponto de inflexão, que
segundo Sousa e colaboradores (2015) é a etapa do ciclo de vida com investimento em
crescimento. Esse uso diferenciado de habitat, bem como traços de história de vida, pode
ser rastreados por meio dos otólitos, pois são estruturas conservativas que fornecem uma
cronologia química da vida do peixe, (Albuquerque et al., 2010; Avigliano & Volpedo,
2013)
Ressaltamos ainda a importância dos Mugilidae enquanto recurso pesqueiros,
visto que compõem 20% da captura no Brasil (MPA, 2011), o que os qualifica como
espécies cujo manejo e conservação é de interesse socio-econômico para o país, em
especial no Nordeste, onde coexistem pelo menos seis espécies do gênero (Menezes et
al., 2015, Neves et al. 2021) e todas são explotadas pela pesca, sendo conhecidas como
tainhas. Neste contexto, o objetivo geral dessa tese é avaliar os traços de história de
vida de forma interespecífica e a plasticidade individual no uso do habitat de espécies de
Mugil que co-ocorrem em ambientes tropicais, verificando as implicações para o manejo
e conservação. Para atingir esse objetivo geral, a tese foi organizada em quatro capítulos
independentes e complementares, cada um gerou um artigo científico.
Capítulo 01 - Objetivo: identificar padrões temporais e espaciais na distribuição de
M. curema e M. rubrioculus em ambiente tropical estuário do Atlântico Sudoeste.
Pergunta: qual é o papel da variabilidade ambiental na formação dos padrões de
distribuição destes peixes em um local escala? Hipótese: espécies congenéricas
morfologicamente semelhantes apresentam segregação temporal impulsionada por
diferentes respostas a fatores ambientais como mecanismo para permitir a coexistência.
Capítulo 02 – Objetivo: fornecer parâmetros de crescimento com base nas
relações comprimento-idade de três espécies de tainhas tropicais exploradas (M. curema,
M. liza, M. rubrioculus) e integrar informações de idade e crescimento polifásico
alométrico de otólitos e reprodução. Hipótese: (1) a alometria polifásica otolítica pode
com precisão prever a idade de maturação; (2) seguindo a teoria de história de vida, a
espécie menor e de crescimento mais rápido exibirá maturação mais precoce e mudança

na velocidade de crescimento em idades mais jovens, enquanto que a espécie de
crescimento mais lento apresentará maturação e alterações alométricas tardias.
Capítulo 03: Objetivo: Determinar a variabilidade individual na estuarinodependência para as espécies de Mugilidae relacionada a primeira fase do seu ciclo de
vida. Hipótese: A maior estuarino-dependência implica em uma menor plasticidade
individual nas estratégias de utilização de habitats estuarinos e costeiros por Mugilideos.
Capítulo 04: Objetivo: integrar Conhecimento Científico Convencional (CSK) e
Conhecimento Ecológico Local (LEK) como meio de promover a melhor gestão pesqueira
de tainhas. Especificamente, foi avaliado a situação dos estoques de três espécies de
tainha (M. curema, M. liza e M. rubrioculus). Além disso, empregamos LEK como método
complementar para reunir informações importantes sobre a história de vida e a pesca,
bem como identificar os pontos fortes, fraquezas, oportunidades e ameaças associadas
às pescarias estudadas.

REFERÊNCIAS
Able, K.W. 2005. A re-examination of fish estuarine dependence: evidence for
connectivity between estuarine and ocean habitats. Estuarine. Coastal and Shelf
Science 64, 5–17.
Albuquerque, C. Q.; Miekeley, N. & Muelbert, J. H. 2010. Whitemouth croaker.
Micropogonias furnieri, trapped in a freshwater coastal lagoon: a natural comparison of
freshwater and marine influences on otolith chemistry. Neotropical Ichthyology
(Impresso), v. 8, p. 311-320.
Avigliano, E. & Volpedo, A. V. 2013. Use of otolith strontium: calcium ratio as indicator of
seasonal displacements of the silverside (Odontesthes bonariensis) in a freshwatermarine environment. Marine and Freshwater Research, 64: 746-751
Begon, M.; Townsend, C. R. & Harper, J. L. 2009. Ecologia de Individuos a
Ecossistemas.
Fowler, A. M.; Smit, S. M., Booth D. J. & Stewart J. 2016. Partial migration of grey mullet
(Mugil cephalus) on Australia’s east coast revealed by otolith chemistry. Marine
Environmental Research. 119. 238-244.
Menezes, N. A.; Nirchio, M.; Oliveira, C. de & Siccharamirez, R. 2015. Taxonomic
review of the species of Mugil (Teleostei: Perciformis: Mugilidae) from the Atlantic South

Caribbean and South America, with integration of morphological, cytogenetic and
molecular data. Zootaxa 3918, 1–38.
Neves JMM, Perez A, Fabré NN, Pereira RJ, & Mott T (2021) Integrative taxonomy
reveals extreme morphological conservatism in sympatric Mugil species from the
Tropical Southwestern Atlantic. Journal of Zoological Systematics and Evolutionary
Research 59(1), 163–178.
Phillips, B. L., Brown, G. P., & Shine, R. (2010). Life‐history evolution in range‐shifting
populations. Ecology, 91(6), 1617-1627.
Ricklefs, R. E. 2003, A Economia da Natureza. Guanabara Coogan, 5° Edição. Rochet
2000
Roff, D. A. 1992. The evolution of life histories. Theory and analysis. Chapman and Hall,
New York.
Santana da Silva F. M.; Morizec, E.; Labonned, M.; Lessa, R. & Claviere, J. 2018.
Connectivity between the marine coast and estuary for white mullet (Mugil curema) in 2
northeastern Brazil revealed by otolith Sr:Ca ratio. Estuarine, Coastal and Shelf Science.
Sousa, M. F.; Fabré, N. N. & Batista, V. S. 2015. Seasonal growth of Mugil liza
Valenciennes, 1836 in a tropical estuarine system. Journal Of Applied Ichthyology, v. 31,
p. 627-632.
Stearns, S.C. 1992. The Evolution of Life Histories, Oxford University Press
Winemiller, K. O. 1989. Patterns of variation in life history among South American fishes
in seasonal environments. Oecologia 81, 225–241.
Wootton, R. J. 1990. Ecology of Teleost Fishes. Fish and Fisheries Series 1. Chapman
& Hall, London, 404.

2 REVISÃO DA LITERATURA
2.1 História de vida
A história de vida não é uma propriedade fixa que o organismo exibe, mas sim o
resultado de forças evolutivas de longo prazo acrescida das respostas imediatas de um
organismo ao ambiente no qual ele está inserido (Begon et al., 2007, Phillips et al., 2010).
A variação em um traço de história de vida, como crescimento, fecundidade ou
maturidade, está frequentemente correlacionada a variação em outro traço e com o
ambiente em que esse organismo ocupa, ou seja, é como um complexo conjunto de
traços co-evoluídos, que estão diretamente ligados ao fitness (Roff 1984, Ricklefs, 2003,
Stearns 1992, Rochet 2000).
Esses traços também variam em níveis biológicos, por exemplo, entre as espécies
(Winemiller & Rose, 1992) entre os indivíduos (Heins & Baker, 1987; Fowler et al., 2016)
e entre as populações (Soeth et al., 2019). A variação em uma característica de história
de vida pode ser vista de maneira diferente dependendo do nível organizacional biológico
de comparação. Comparar os traços de duas ou mais espécies e buscar entender as
diferenças entre eles, à luz dos ambientes que as espécies ocupam é imperativo
(Wooton, 1990; Devine et al., 2012; Midway & Peoples, 2019).

Nesse sentido, os

principais traços de história de vida a serem analisados são: tamanho/idade na
maturidade, tamanho/idade máxima, taxa de crescimento e fecundidade (Winemiller,
1989).
O tamanho corporal, traço de história de vida mais evidente, é um indicador da
necessidade energética e superioridade inter e intraespecífica e, desta forma, é esperado
que indivíduos e/ou espécies maiores tenham acesso aos melhores recursos disponíveis,
como alimento e espaço (Letourneur, 2000). Combinando o tamanho corporal
(comprimento total) com a idade é possível avaliar o crescimento somático, outro
importante traço de história de vida. A estimativa dos parâmetros de crescimento é uma
importante ferramenta para avaliação da dinâmica de populações, e também essencial
para o entendimento dos eventos do ciclo de vida, aspectos comportamentais e a
conservação e manejo de espécies (Fabré & SaintPaul, 1998; Sousa et al., 2015). Nas

regiões tropicais, as taxas de crescimento são influenciadas pelo período sazonal, o
habitat ocupado pela espécie, as fases do ciclo de vida e os recursos alimentares
(Boujard et al., 1991, Lowe-McConnel, 1991).
O padrão reprodutivo pode ser conceituado como o conjunto de atributos que uma
espécie possui para obter sucesso reprodutivo e manter populações estáveis (Winemiller,
2005). Este padrão engloba: tamanho de primeira maturação, desenvolvimento gonadal,
tamanho do ovócito, tipo de desova e fecundidade (Vazzoler, 1996; Winemiller, 2005). A
reprodução está adaptada, principalmente, às condições ambientais e a pressão de
predação (Stearns 1976, Winemiller, 1989, Wilson et al., 2019). Por exemplo, o aumento
da disponibilidade de alimentos, ou seja, um ambiente que propicie um forrageamento de
qualidade, aumentou o crescimento, reduzindo a idade na maturidade e aumentando a
expectativa de vida reprodutiva do adulto para o peixe Salvelinus namaycush (Wilson et
al. 2018). Além disso, para muitos animais, a seleção sexual e/ou os custos reprodutivos
levam a taxas de crescimento diferenciais e/ou tamanhos corporais máximos divergentes
entre machos e fêmeas (Andersson 1994; Love et al. 1990).
No contexto dos peixes, a estimativa dos parâmetros de crescimento
frequentemente emprega a função de crescimento de von Bertalanffy (VBGF), e as
interações entre esses parâmetros são utilizadas como indicadores das estratégias de
história de vida (Beverton & Holt, 1957; Ricker, 1975). Por exemplo, espécies com taxas
de crescimento relativamente rápidas costumam ser caracterizadas por atingir a
maturidade sexual em idades e tamanhos reduzidos, o que se reflete em alta
produtividade reprodutiva, expectativa de vida curta e tamanho corporal máximo limitado
(Roff, 1984; Stearns & Crandall, 1984; Stearns, 1992). Dessa forma, a mesma espécie
pode apresentar diferentes padrões de crescimento em diferentes ambientes, por
exemplo, ambientes com maior ou menor disponibilidade de recursos, com maturidade
sexual sendo atingida em diferentes tamanhos ou em diferentes idades (Stearns et al.
1986). A maturação precoce pode resultar em populações densas de indivíduos
pequenos e incorrer em um custo na forma de redução da fecundidade futura (Williams
1966; Bertschy & Fox, 1999). A forma mais recomendada, de estimar o crescimento, por

causa da precisão, é por meio de estruturas rígidas como escamas, espinhos e otólitos,
pois são estruturas conservativas.
Muitas espécies de peixes realizam migrações para completar seu ciclo de vida,
pois os habitats necessários para reprodução, crescimento e alimentação muitas vezes
estão separados por vários quilômetros (Northcote, 1978). A migração, pode ser
conceituada como movimentos que resultam em uma alternância entre dois ou mais
habitats separados, com um eventual retorno ao habitat original, ocorre com
periodicidade regular e envolve uma grande proporção da população (Northcote, 1978).
Vários são os padrões migratórios conhecidos, como por exemplo: vertical ou horizontal,
descendente (para jusante, rio abaixo) ou ascendente (para montante, rio acima). A
migração também pode ser parcial, onde uma população é composta tanto por migrantes
quanto por residentes, possui implicações ecológicas e evolutivas (Swingland, 1984;
Chapman et al., 2011). Isso foi verificado por Fowler e colaboradores (2016), com a
espécie Mugil cephalus na costa leste Australiana, onde indivíduos que compõe a
população permanecem no mesmo ambiente de salinidade por longos períodos
(residentes), enquanto outros se deslocam regularmente entre ambientes de salinidades
diferentes (migrantes). Sendo assim, existe uma diversidade de fenótipos migratórios
entre e dentro das populações, podendo levar à sobrevivência diferencial através da
exposição a diferentes predadores, além da resiliência à pressão por pesca,
demonstrando plasticidade nesse comportamento.

2.2 Plasticidade individual em peixes
A plasticidade fenotípica representa a capacidade intrínseca de um determinado
ser vivo de expressar diferentes fenótipos em resposta a variações temporais ou
espaciais em seu ambiente biótico ou abiótico, e pode ser estudada a nível individual ou
populacional (Schlichting & Pigliucci 1998, Sultan 2003, Dingemanse et al., 2010).
Podendo ser aplicada a uma série de características fenotípicas expressas a nível
comportamental, fisiológico, morfológico ou do desenvolvimento (De Witt e Scheiner,
2004; Fusco e Minelli, 2010).

Essa adaptabilidade individual, que é um fenômeno

epigenético, pode ser desencadeada por diversas causas e, quando persistente ao longo

do tempo, pode ter implicações evolutivas significativas para a sobrevivência das
populações em ambientes dinâmicos (Nussey et al., 2007; Stamps, 2016). O estudo da
plasticidade fenotípica teve início com a elaboração das “curvas fenotípicas”, que
demonstram o gradiente de respostas fenotípicas de uma ou mais características
submetidas a variações de fatores ambientais, conhecidas como de normas de reação
(Woltereck, 1909, Sarkar, 2004). A norma de reação de uma característica fenotípica
morfológica, fisiológica, comportamental ou de história de vida pode ser representada
graficamente em coordenadas cartesianas, que facilitam a compreensão desse conceito.
A plasticidade do desenvolvimento em peixes é particularmente pronunciada em
suas respostas às flutuações ambientais (Karjanailen et al. 2016). Por exemplo, a taxa
de crescimento, a idade na maturidade e a fecundidade são altamente influenciadas pela
temperatura e pela disponibilidade de alimentos (Stearns, 1977). Os peixes têm a
capacidade de ajustar seu crescimento e o momento de atingir a maturidade sexual em
resposta a mudanças na disponibilidade de recursos, na temperatura da água e em
outros fatores ambientais, o que os destaca como exemplos notáveis de plasticidade
fenotípica (Reed et al., 2010; Coulson et al., 2001). Essa capacidade adaptativa é
essencial para sua sobrevivência e reprodução em ambientes que são variáveis e muitas
vezes imprevisíveis. Nesse sentido, a variação temporal no clima pode impactar o
desempenho individual, os padrões e a intensidade da seleção natural e as interações
dependentes da densidade, conduzindo a mudanças físicas no habitat e alterando a
distribuição e abundância das espécies interativas (Grant & Grant, 2002; Stenseth et al.,
2002).
Outro exemplo da alta plasticidade ambiental em termos de habitat, salinidade,
residência e movimento nos peixes, temos os juvenis de Centropumus paralelus (Daros
et al. 2016). Essa alta plasticidade nos primeiros estágios do ciclo de vida poderia permitir
maiores taxas de sobrevivência, uma vez que os sistemas de natação das larvas e póslarvas não estão totalmente desenvolvidos e elas flutuam passivamente nas correntes de
água durante o início de sua história de vida (Daros et al. 2016).
A plasticidade individual associada ao comportamento reprodutivo se torna mais
previsível com o envelhecimento do indivíduo (Nettle & Bateson, 2015; Fischer et al.,

2014), e com a redução da incerteza ambiental (Fawcett & Frankenhuis, 2015; Polverino
et al., 2019). Isso sugere que os custos dessa plasticidade podem ser mitigados,
correlacionados com a manutenção sensorial e regulatória necessária para uma alta
capacidade de resposta ao ambiente (DeWitt et al., 1998; Urszan et al., 2018). Portanto,
a capacidade de um organismo em se adaptar às mudanças ambientais é uma estratégia
fundamental para atenuar os efeitos das variações no ambiente, maximizando seu
desempenho (DeWitt et al., 1998; Urszan et al., 2018).
A compreensão das origens e das consequências dessa plasticidade é crucial para
os estudos do comportamento de peixes e torna-se ainda mais urgente em contextos de
exploração populacional, nos quais a pesca seletiva com base no tamanho pode alterar
a história de vida das espécies (Wilson et al., 2019). Pois as populações naturais sob
regime de exploração, como no caso da pesca, geralmente enfrentam algum tipo de
restrição nas características fenotípicas desejadas (Allendorf e Hard, 2009). Como
exemplo temos a diminuição do tamanho médio de captura dos peixes expostos a
sobrepesca de exemplares de maior tamanho (Law, 2000; McClenachan, 2009). O que é
relevante considerando que a adaptação das populações em escalas de tempo ecológico
e evolutivo é fornecida pela evolução genética e também pela plasticidade fenotípica.

2.3 Trade-off em peixes
A teoria da história de vida preocupa-se com trade-offs estratégicos com relação
à alocação de energia entre várias funções biológicas e os efeitos desta alocação na
dinâmica populacional (Roff, 1992; Stearns, 1992; Arendt, 1997, Begon et al., 2007).
Segundo o conceito de trade-off, os recursos destinados para uma atividade tornam-se
indisponíveis para outras atividades, dessa forma um trade-off é uma relação negativa
entre duas características da história de vida, como uma gangorra de alocação de
recursos (Roff, 1992; Stearns, 1992; Begon, et al., 2007).
O trade-off entre o crescimento e reprodução é um dos mais importantes
estudados (Roff et al., 2006; Tsikliras et al., 2007; Roff & Fairbairn, 2007), já que são
processos complementares (Wooton, 1990). Sendo assim, um indivíduo, ao aumentar
sua alocação de energia para atividades reprodutivas, tenderá a diminuir sua

sobrevivência/ou taxa de crescimento corporal, diminuindo, consequentemente, seu
potencial para a reprodução no futuro. O aumento da reprodução conduzirá ao tamanho
reduzido e consequentemente uma diminuição no Valor Reprodutivo Residual - VRR
(Begon et al., 2007). O VRR combina a sobrevivência futura esperada com a fecundidade
futura esperada, levando em conta a contribuição de cada indivíduo para as futuras
gerações (Begon et al., 2007).
Tsikliras e colaboradores (2007) testaram o trade-off entre a taxa de crescimento
e a fecundidade dentro de uma única população de Sardinella aurita. Foi concluído que
a fecundidade individual está negativamente relacionada com taxa de crescimento
específico individual, demostrando que S. aurita, com a idade, aloca cada vez menos
energia para o crescimento e mais para a reprodução e que essa alocação relacionado
ao crescimento determina a fecundidade presente, sendo a fecundidade reduzida com o
custo de crescer mais rápido. Isso indica que qualquer aumento no crescimento está
associado a uma diminuição no número de descendentes. Consequentemente, a
reprodução é trocada por maior crescimento.
Levando em consideração as diferenças observadas nos padrões de crescimento
e desova devido à idade, indivíduos mais jovens parecem investir sua energia adquirida
em seu próprio crescimento, enquanto indivíduos mais velhos a investem na desova
(Tamura et al., 2019). A seleção nas taxas de crescimento via trade-off entre
sobrevivência à maturidade sexual e longevidade para Xiphophorus multilineatus foi
estudada, e demostrarou um custo de crescimento mais rápido para os juvenis, tendo
assim longevidade reduzida na idade adulta (Weinstein et al., 2019). Também foi
observada uma relação negativa entre a taxa de crescimento das primeiras idades para
as fêmeas, suportando ainda mais um custo de longevidade para um crescimento mais
rápido.
Outro exemplo de plasticidade de crescimento é o da truta, Salvelinus namaycush,
na América do norte da América, resultando da adaptação local e trade-offs, que
impulsionam a variação em características associadas ao crescimento ao longo do ciclo
de vida (Wilson et al., 2019). Para essa espécie, a alocação reprodutiva foi explicada pela
evolução dos trade-offs com mortalidade e outros traços de história de vida. Um trade-off

entre crescimento e mortalidade tem sido detectado para algumas espécies e apoia
fortemente a hipótese de que a taxa de crescimento mais rápida pode não sempre ser
ideal (Mangel & Stamps 2001).

2.4 Mugilidae
Os peixes da família Mugilidae estão distribuídos nas regiões tropical e subtropical
de todos os continentes, principalmente nas águas estuarinas e marinhas costeiras, onde
são conhecidos popularmente como tainhas, curimã e paratis (Thomson, 1997; Harrison,
2002, Menezes, et al., 2015). Essa família é constituída por 17 gêneros e 72 espécies,
sendo que sua taxonomia tem sido amplamente discutida e é bastante problemática,
principalmente devido ao fato de serem muito semelhantes morfologicamente (Nelson,
2006, Menezes et al, 2010; Menezes et al., 2015). Na América do Sul, até o presente,
foram identificadas oito espécies de Mugilidae, todas do gênero Mugil, são elas: M.
brevirostris Ribeiro, 1915; M. curema Valenciennes, 1836; M. curvidens Valenciennes,
1836; M. incilis Hancock, 1830; M. margaritae Menezes, Nirchio, Oliveira & Ramirez; M.
rubrioculus Harrison, Nirchio, Oliveira, Ron & Gavíria, 2007; M. trichodon Poey, 1875 e
M. liza Valenciennes, 1836 (Menezes et al., 2015). Sendo que em Alagoas foram
identificadas apenas cinco linhagens mitocondriais de Mugil (figura 1).
Apesar dos mugilídeos compreenderem um complexo de espécies estuarinas
morfoecologicamente similares, sua história evolutiva é notavelmente longa e distintiva.
Este gênero se destaca por sua diversificação ao longo de milhões de anos, sem uma
divergência morfológica e ecológica pronunciada (Neves et al., 2020). Mugil curema e M.
rubrioculus são exemplos de espécies que divergiram há cerca de 23 milhões de anos, e
apesar

disso,

conservadorismo

mantêm
extremo

uma

notável

nesta

semelhança

característica,

morfológica,

possivelmente

sugerindo

influenciado

por

similaridades no uso do habitat e traços de história de vida (Neves et al., 2020).
O ciclo de vida dos indivíduos do gênero Mugil possuem uma influência sazonal,
marcada pela pluviosidade nos ambientes aquáticos tropicais (Lowe-McConnell, 1991;
González Castro et al., 2009). Nesses ambientes duas estações sazonais são definidas,
são elas: seca e chuvosa (Figueroa & Nobre 1990). Na estação chuvosa, o fluxo de água

doce que entra nos estuários aumenta a produtividade biológica e disponibiliza alimento,
afetando assim todos os níveis da cadeia trófica, aumentando os teores de clorofila-a
favorecendo o crescimento e a sobrevivência dos peixes da região estuarina (Grego et
al., 2004, Robins et al., 2006, Gillson, 2011).
O uso do estuário e dos habitats marinhos adjacentes pode ser compreendido
como um continuum para os peixes do gênero Mugil o grau de dependência é obrigatório,
pois eles passam pelo menos uma fase do seu ciclo de vida nesse ambiente, com grande
relevância nos fluxos de matéria orgânica entre esses habitats (Able, 2005; Lebreton et
al., 2011). São necessários novos estudos que incorporem o papel das variáveis bióticas,
como por exemplo: o padrão de uso do estuário pelas coortes de desova e a variação
anual na abundância de peixes. Dessa forma, será possível melhorar a compreensão do
significado funcional e do grau de dependência estuarina dessas espécies (Simenstad et
al., 2000; Able, 2005). A explotação simultânea dos Mugilidae é devido ao fato de ocorrem
em simpatria e apresentando segregação temporal e espacial (Ibáñez Aguirre, 1993;
Albieri et al., 2010, Mai et al., 2018). Essa segregação se dá, por exemplo com diferentes
períodos de desova entre as espécies, com ocupação de áreas com alta salinidade ou
menor salinidade. Então, de forma geral, não ocupam o mesmo nicho ecológico
simultaneamente (Ibáñez Aguirre, 1993; Albieri et al., 2010, Mai et al., 2018).
Segundo Menezes e colaboradores (2015) As espécies do gênero Mugil
apresentam variações morfológicas distintas, permitindo sua diferenciação taxonômica.
M. brevirostris possui corpo fusiforme, cabeça curta e larga, focinho arredondado e
escamas grandes, enquanto M. curema é mais robusto, com faixa prateada, focinho
pontiagudo e escamas menores. M. curvidens diferencia-se pelos dentes curvados bem
desenvolvidos, corpo menos robusto, nadadeira dorsal mais alongada e um sulco bem
definido entre os olhos. M. rubrioculus tem olhos avermelhados, corpo esbelto e boca
menor. M. liza destaca-se pelo corpo fusiforme e otólitos com bordas irregulares, sendo
a espécie mais divergente do grupo em análises morfológicas e genéticas (figura 1).

Figura 1 - Espécies do gênero Mugil que coexistem em estuários tropicais. De cima para
baixo: M. curvidens, M. brevirostris, M. curema, M. rubrioculus e M. liza. Fotos: equipe
do Laboratório de Ecologia de Peixes e Pesca da UFAL.

Os Mugilídeos de forma geral são considerados detritivoros, convertendo energia
potencial dos detritos em energia aproveitável para outros níveis tróficos (YañezArancíbia, 1976). Dessa forma, apresentam um importante papel ecológico e econômico
para as regiões onde ocorrem. Os indivíduos de M. curema habitam principalmente
regiões estuarinas de fundo com lodo e águas turvas e os juvenis são encontrados em
praias arenosas, próximo aos estuários (Vieira & Scalabrin, 1991). M. curema possui uma
alta capacidade de adaptação alimentar, sendo considerada detritívora, iliófaga,
herbívora, onívora, fitófaga e zooplanctófaga (Franco & Bashirullah, 1992).

2.4.1 Reprodução e migração de Mugil
Em termos gerais, o ciclo reprodutivo das espécies estuarino-dependentes, como
os Mugilidae, é caracterizado por uma fase de maturação gonadal nos estuários,
configurando uma história de vida bipartida, sendo classificados como catádromos.
Durante a época reprodutiva, os peixes adultos empreendem uma migração em direção
às águas marinhas costeiras para a desova, com os ovos e as larvas sendo dispersos
pelos processos oceanográficos físicos até os estuários, onde as larvas em estágio
avançado estabelecem-se e desenvolvem-se como juvenis (Moore, 1974). Após a
metamorfose, os juvenis permanecem nos estuários para completar seu desenvolvimento
e, à medida que amadurecem, participam na migração reprodutiva, encerrando o ciclo
(Vieira & Scalabrin, 1991) (Figura 2). Então, em sua maioria, as tainhas utilizam os
estuários como berçários, aproveitando as condições favoráveis, como o influxo de
nutrientes e os habitats estruturados, para seu desenvolvimento durante os primeiros
anos de vida (Santana et al., 2018).

Figura 2 – Esquema representativo do ciclo de vida dos Mugil. Fonte: equipe do
Laboratório de Ecologia de Peixes e Pesca da UFAL.

No entanto, os Mugilidae do gênero Mugil possuem uma alta variabilidade
intraespecífica e interespecíficas nos padrões de migração (Chang et al., 2004; Chang &
Iizuka, 2012; Ibáñez-Aguirre et al., 2012; Avigliano et al., 2015; Fowler et al., 2016). Esta
variação no uso do habitat estuarino indica um comportamento migratório mais complexo
que o previsto inicialmente para tainhas (Fowler et al., 2016; Mai et al., 2018). Dessa
forma, M. curema está associada a águas de alta salinidade podendo ser classificada
como marinho migrante sub-categoria marinha estuarina-oportunista. Já M. liza está
associada a águas menos salinas, devendo ser classificada como marinha migrante subcategoria estuarina dependente (Mai et al., 2018). Mugil cephalus, uma das espécies
mais estudadas desse gênero, apesenta uma migração diádroma parcial, possuindo uma
diversidade considerável na história migratória entre os indivíduos (Fowler et al. 2016).
Não há estudo que analise esse traço de história de vida para as demais espécies do
gênero.
Os Mugilidae, em sua maioria, são peixes gonocóricos e de alta fecundidade
(Alvarez-lajonchere, 1982; Fazli et al., 2008). Essa fecundidade está relacionada com o
tamanho do peixe, assim, indivíduos com 32 cm de comprimento total possuem cerca de
1.082.200 ovos e 2.632.000 ovos foram encontrados em indivíduos com 54 cm de
comprimento total, conforme descrito por Lawson e Jimoh (2010) para a espécie M.
cephalus. A maturidade sexual em mugilídeos ocorre entorno de 3-4 anos nos machos,

e as fêmeas alcançam entre 4-5 anos, e o tamanho total de maturidade sexual depende
da espécie, no caso de M. liza na Baía de Sepetiba, o tamanho varia de 55 a 57 cm
(Okumus & Basçmar, 1997).
Em seu estudo sobre M. curema, Santana e colaboradores (2018) observaram que
os indivíduos analisados nascem em áreas de salinidade características do estuário,
onde eles se desenvolvem até aproximadamente um ano de idade, quando migram para
áreas de maior salinidade até atingir a maturidade sexual (3 anos) no mar. Após a desova
ocorrer, os indivíduos de M. curema podem permanecer no mar ou retornar ao estuário
até a próxima desova. O período reprodutivo de Mugil curema ocorre de diferentes formas
e de acordo com a distribuição geográfica, muitas vezes com ocorrência de dois picos
reprodutivos (Marin et al. 2003).
No Atlântico Ocidental subtropical M. liza, apresenta desova única e
desenvolvimento oocitário sincrônico em dois grupos, ou seja, a cada período de
reprodução evidenciam-se dois lotes de ovócitos dentro dos ovários, o dos ovócitos do
estoque de reserva e aquele dos ovócitos que serão eliminados no período de desova
(Vieira & Scalabrin, 1991; Sousa et al., 2015). Já M. curema apresenta desova parcial,
desenvolvimento oocitário assincrónico, consistindo na liberação de apenas parte dos
oócitos por vez, em lotes (Santana et al., 2018).
Ibáñez e colaboradores (2012) observaram que M. cephalus e M. curema na costa
do México podem desovar tanto em águas marinhas quanto em ambientes estuarinos.
Nos que desovam em ambientes marinhos os ovos são transportados para ambientes
costeiros estuarinos.

Foi verificado que a migração reprodutiva para o mar de M.

cephalus ocorre no inverno e de M. curema na primavera, evidenciando a segregação
temporal e espacial que ocorre quando duas espécies intimamente relacionadas são
simpátricas (Mai et al., 2018).
O processo reprodutivo e a abundância das espécies de Mugil estão sujeitos a
interferências negativas decorrentes do aquecimento global, considerando que a
temperatura da superfície do mar constitui o principal fator que limita a distribuição
geográfica dessas espécies, e os ambientes estuarinos e costeiros marinhos são
altamente sensíveis às mudanças climáticas (Hung & Shaw, 2006; Lan et al., 2014). Além

disso, o aumento do nível do mar e a acidificação dos oceanos, ambos associados ao
aquecimento global, podem impactar os habitats costeiros, reduzindo a disponibilidade
de alimentos para os indivíduos e, consequentemente, afetando sua capacidade de
sobrevivência e crescimento. É importante ressaltar que o período de adaptação da
tainha a essas mudanças ainda não é completamente compreendido, o que pode resultar
em uma menor disponibilidade desse importante recurso em um futuro próximo
(Rijnsdorp et al., 2009; Durand & Whitfield, 2016).

2.4.2 Crescimento, idade e microquímica de otólitos
Os otólitos são estruturas mineralizadas, acelulares, formadas por carbonato de
cálcio (97-99%), em sua maioria sob forma de aragonita, embutido em uma matriz
proteica, denominada otolina (Campana & Neilson, 1985, Campana 1999, Cousseau,
2010). Eles estão localizados no aparelho vestibular do ouvido interno de peixes ósseos
e estão presentes em três pares: sagittae, lapilli e asterisci (Thresher, 1999; Popper et
al., 2005). Em Perciformes, os sagittae são os mais utilizados para diversos estudos, por
serem os mais fáceis de remover e localizar, além de possuírem o maior eixo de
crescimento e a maior massa (Secor et al., 1992; Thresher, 1999).
As estruturas otolíticas são altamente conservadoras, não sofrendo reabsorção e
permanecendo intactas ao longo da vida do peixe (Tuset et al., 2008). Elas representam
as primeiras estruturas calcificadas a se formarem nos estágios embrionários ou larvais
(Domingues & Hayashi, 1998). Sendo a forma dos otólitos de cada espécie única (figura
3), é possível até a identificação da espécie pela sua morfometria (Dahl et al. 2024). Mas,
como essa forma sofre influência de um componente genético e também há uma
variabilidade hormonal e ambiental (fatores como sexo, idade, dieta, temperatura da
água, profundidade, tipo de substrato, salinidade e fonte de alimento), a forma dos otólitos
pode ser utilizada para diferenciação de estoques pesqueiros (Moralles-Nin et al. 1998,
Secor & Rooker, 2000, Ibañez et al. 2022).

Figura 3 - Micrografia eletrônica de otólitos sagittae de M. brevirostris, M. curvidens, M.
curema, M. rubrioculus e M. liza. Fotos: equipe do Laboratório de Ecologia de Peixes e
Pesca da UFAL.

O crescimento dos otólitos é caracterizado pela adição de camadas concêntricas
de carbonato de cálcio sobre uma base proteica, resultando em uma estrutura na qual
diferentes taxas de deposição de matéria orgânica e inorgânica ao longo do tempo se
traduzem em marcas com propriedades ópticas distintas, sendo elas opacas ou hialinas.
As opacas são zonas mais calcificadas, mais largas e escuras, que corresponde ao
período de crescimento rápido e as hialinas, também conhecidas como translúcidas, são
zonas menos calcificadas e mais estreita, período de crescimento lento, que juntas
formam um anel de crescimento (Panfili & Tomas 2001, Campana, 2004, Volpedo & Vazdos-Santos, 2015). Tais marcas são o resultado de uma interação complexa de fatores
endógenos e exógenos, como alterações no crescimento, flutuações na temperatura,
doenças, atividade reprodutiva, migração, disponibilidade e consumo de alimento, e
estresse ambiental (Campana, 2004). A contagem do número dessas marcas opacas e
hialinas (figura 4) é amplamente empregada para estimar a idade e o crescimento de

grande parte dos teleósteos (Rufino, 2004; Fabré & Saint-Paul, 1998). As primeiras
pesquisas utilizando essa abordagem foram realizadas em regiões temperadas, onde as
flutuações de temperatura entre verão e inverno são bem marcadas (Ricker, 1975).
Posteriormente vieram as pesquisas em regiões tropicais, que apresentam variações
sazonais, como períodos secos e chuvosos (Morales-Nin & Panfili, 2005, Sousa et al.
2015).

Figura 4 - Otólitos sagittae inteiros de M. liza, M. curema e M. rubrioculus. Mostrando o
núcleo opaco (seta) e as sucessivas zonas translúcidas e opacas que formam os anéis
de crescimento. Fotos: equipe do Laboratório de Ecologia de Peixes e Pesca da UFAL.

No entanto, durante o estágio inicial da vida, como a transição do estágio larval
para o juvenil e as mudanças ambientais que podem deixar marcas nos otólitos (Chang
et al., 2000), a validação da marca de idade pode se tornar confusa. Por exemplo, foram
registradas marcas nos otólitos de Mugil curema antes do primeiro ano de vida,
possivelmente correspondendo à mudança de habitat, do local de nascimento marinho
para a região estuarina (Santana et al., 2018). Nesse sentido, é fundamental validação,
ou seja, a determinação da periodicidade e época de formação dos anéis nos otólitos

(Campana, 2001, Green et al. 2009, Volpedo & Vaz-dos-Santos, 2015). Assim como
também é fundamental, anteriormente, a escolha da técnica de visualização de anéis,
por exemplo, se os anéis serão visualizados inteiros ou seccionados, se serão polidos ou
não, se é preciso aplicar alguma técnica de coloração para melhorar o contraste entre as
zonas opacas e hialinas (Figura 05) (Stevenson e Campana 1992).

Figura 5 – Otólito sagitae de M. curema seccionado pelo isomet, emblocado em resina,
e posteriormente polido (A) e corado (B) com azul de metileno. Fotos: Jordana Rangely.

Esses dados de crescimento desempenham um papel crucial em uma variedade
de cálculos essenciais para a ciência pesqueira, como por exemplo: longevidade, taxa
de mortalidade, modelos de avaliação de estoques, além da modelagem ecológica
(Sparre e Venema 1988, Beverton e Holt 1957, Methot e Wetzel 2013).
Durante um certo tempo de sua vida, o crescimento do peixe é acompanhado de
mudanças na forma do corpo, que são atreladas a mudanças anatômicas ou fisiológicas,
que são conhecidas como relações alométricas, (Begon et al., 2006). Da mesma forma,
os otólitos também podem apresentam alometrias morfométricas relacionadas com a
ontogenia (Volpedo & Echeverría, 1999; Pérez & Fabré, 2013). Diversos modelos podem
ser utilizados para identificar essa alometria, sendo um dos mais aceitos o proposto por
Huxley (1924). Esse modelo foi aplicado por Bervian e colaboradores (2006) que
identificaram pontos de mudança do crescimento ao longo do ciclo de vida do peixe,
indicativas de alocação de energia diferenciada, registradas em mudanças morfológicas
e morfométricas no otólito.

Além dessas informações trazidas pelo otólito também é possível gerar um perfil
da história de vida e obter informações sobre as características ambientais de cada
espécime por meio da microquímica de otólitos (Campana & Thorrold, 2001). Conforme
os peixes crescem, os otólitos incorporam em sua composição material proveniente dos
ambientes em que estão inseridos. Existem pelo menos 50 tipos de elementos presente
nos otólitos, entre eles: cálcio (Ca), carbono (C), oxigênio (O), nitrogênio (N), cloro (Cl),
enxofre (S), magnésio (Mg), sódio (Na), fósforo (P), estrôncio (Sr), potássio (K), lítio (Li),
manganês (Mn), cobre (Cu), cobalto (Co), cádmio (Cd), bário (Ba), chumbo (Pb), silício
(Si) e zinco (Zn) (Sturrock et al., 2012).
Alguns desses elementos, como o lítio, manganês, bário e estrôncio, apresentam
concentrações variadas para diferentes ambientes (marinho e estuarino) e estação (seca
e chuvosa), formando marcadores naturais que refletem o ambiente físico-químico e
consequentemente as mudanças sofridas pelo indivíduo durante o seu ciclo de vida
(Campana e Thorrold, 2001; Campana, 2005; Elsdon et al., 2008).
Dessa forma, a microquímica de otólitos fornece uma cronologia química da vida
do peixe, sendo uma técnica precisa e cada vez mais utilizada em pesquisas de alto
impacto, como por exemplo, em relação a migração (Thresher, 1999, Albuquerque et al.,
2010; Sturrock et al., 2012; Avigliano & Volpedo, 2013; Mai et al., 2019, Koochaknejad et
al. 2024), reprodução (Fowler et al., 2016; Avigliano et al., 2016), idade e crescimento
(Santana et al., 2018) e ontogenia (Walther et al., 2010), fornecendo informações para
responder questões ecológicas aplicadas em diferentes escalas temporais e espaciais,
que podem ser utilizadas para fins de gerenciamento e conservação de espécies de peixe
(Campana, 2005; Elsdon et al., 2008; Avigliano et al., 2016). Além disso, combinando a
análise dos elementos com os anéis de crescimento é possível um arquivo importante
que registra com organização temporal as informações do ambiente frequentado pelos
peixes, as mudanças ambientais e a exposição a poluentes em toda a ontogenia (Halden
& Frierich, 2008).
Pesquisas

recentes

indicam

potencial

desta

técnica

avaliar

estuarinodependência e uso diferenciado de habitat (Albuquerque et al. 2010, 2012,
Condini et al., 2016, Mai et al. 2019, Almeida et al. 2024), já que os ambientes estuarinos

passam por processos constantes de input e output de nutrientes que afetam, espacial e
temporalmente, os processos biológicos, físicos e químicos dos peixes (Elsdon &
Gillanders, 2005). A heterogeneidade química dentro dos estuários, devido às descargas
fluviais e antropogênicas, cria variabilidade espacial entre os ambientes estuarinos e
costeiros adjacentes, que podem ser quimicamente identificadas nos otólitos dos peixes
(Elsdon et al., 2008; Walther & Thorrold, 2009).
A variabilidade da concentração de Sr e Ba nos otólitos é principalmente devido à
composição química da água (Campana 1999, Wells et al. 2003). A concentração de Sr
está positivamente relacionada à salinidade enquanto Ba está negativamente relacionada
à salinidade, dessa forma, na região estuarina é encontrada uma menor concentração de
Sr e uma maior concentração de Ba em relação a região marinha, o que ficará registrado
no otólito dos peixes (Secor et al., 2001; Zimmerman, 2005; Labonne et al., 2009;
Tabouret et al. 2010; Avigliano & Volpedo, 2013).
Dessa forma, é possível verificar a conectividade entre a região marinha costeira
e o estuário para as espécies utilizando Sr e Ba. Por exemplo, para M. curema, a maior
salinidade na estação seca leva a uma maior assinatura Sr: Ba no otólito entre os
indivíduos gerados nesta temporada desde o nascimento até um ano de vida (Santana
et al. 2018). Por outro lado, a menor salinidade na estação chuvosa leva a uma menor
assinatura Sr:Ba no otólito entre os indivíduos gerados nesta temporada (Ibañez et al.
2012). Esta relação direta entre a salinidade e a relação Sr: Ba no otólito também foi
encontrada para M. liza (Callicó Fortunato et al., 2017).
A metodologia mais utilizada para análise microquímica dos otólitos nos dias atuais
é a ablação a laser e espectrometria de massas por plasma acoplado indutivamente (LAICP-MS) (Mai et al. 2014, Avigliano et al. 2015, Ferreira et al. 2023). Essa técnica
determina elementos traço de forma pontual sobre cortes de otólitos, em um raster que
vai do núcleo à borda do otólito (Volpedo & Vaz-dos-Santos, 2015). Sendo assim, segue
os seguintes passos: limpar com água MiliQ logo após sua extração, colocar os otólitos
em resina cristal epóxi, seccioná-los transversalmente através do núcleo, colar em lâmina
de vidro e submeter a LA-ICP-MS (Albuquerque et al. 2012, Avigliano et al. 2015).

2.5 Pesca Artesanal
Há uma crise global na indústria pesqueira nas últimas décadas (FAO 2022, Pauly,
2008, 2019). A estagnação vivida recentemente está principalmente ligada a um ligeiro
declínio na captura de pesca, que diminuiu 4,5 por cento em 2019 e 2,1 por cento em
2020, (FAO 2022). Esta queda deveu-se a vários fatores, incluindo grande exploração
dos recursos pesqueiros sem uma gestão adequada, os impactos do COVID-19, a
degradação ambiental e a questão do aquecimento global (FAO 2022, Paniagua &
Rayamajhee, 2024).
A pesca de pequena escala (SSF) vem recebendo crescente atenção internacional
por desembarcar cerca de 50% das capturas globais de pesca marinha e empregar cerca
de 51 milhões de pessoas ao redor do mundo, 90% das pessoas envolvidas na pesca,
muitas delas nos países mais pobres do mundo (FAO/ WorldFish Centro 2010, Mills et
al. 2011, FAO, 2018). Suas contribuições para a segurança alimentar e a redução da
pobreza, especialmente nos países em desenvolvimento, são cruciais para os Objetivos
de Desenvolvimento Sustentável da ONU (ODS) (FAO, 2015). Centenas de milhões de
pessoas em toda a cadeia de produção dependem dessa indústria para sua subsistência,
sendo ela uma força motriz econômica e social (Stobutzki et al., 2006 a,b; Hilborn et al.,
2020). Consequentemente, a SSF contribui diretamente para a segurança alimentar,
redução

pobreza,

nutrição

global,

emprego

melhoria

das

condições

socioeconômicas de grande parte da população (Batista et al., 2014). No entanto, essas
pescarias frequentemente carecem de dados históricos importantes, o que resulta na
falta de avaliação adequada e no subgerenciamento dos estoques pesqueiros (Stobutzki
et al., 2006 a,b; Hilborn et al., 2020).
No Brasil, a atividade pesqueira é regulamentada pela Lei Nº 11.959, de 29 de
junho de 2009, que dispõe sobre a Política Nacional de Desenvolvimento Sustentável da
Aqui-cultura e da Pesca, visando o desenvolvimento sustentável da pesca, o
desenvolvimento e a fiscalização da atividade pesqueira e o desenvolvimento
socioeconômico, cultural e profissional dos que exercem a atividade pesqueira. Neste
documento, a pesca comercial artesanal é “aquela praticada diretamente por pescador

profissional, de forma autônoma ou em regime de economia familiar, podendo utilizar
embarcações de pequeno porte” (Brasil, 2009).

2.5.1 Pescarias com dados limitados
A estatística global de pescarias existe desde 1950, em um esforço das Nações
Unidas de monitorar o desenvolvimento da economia mundial (Ward, 2004, Pauly, 2008).
No entanto a maioria das pescarias no mundo é considerada de “dados limitados”
(Costello et al., 2012), o que significa que há uma escassez de informações sobre a
dinâmica populacional das espécies, como comprimento máximo, idade, tamanho/idade
na maturidade e fecundidade (Walters & Martell, 2004). Essa limitação de dados impede
a definição de estratégias eficazes para o desenvolvimento sustentável da pesca,
utilizando os modelos de avaliação baseados em métodos convencionais, que utilizam
séries temporais de dados (Dowling et al., 2015, 2017, 2023). Para essas situações,
foram desenvolvidos os modelos de avaliação com dados limitados (DLMs), que
oferecem métodos alternativos focados em espécies com dados escassos. Os DLMs
podem ser divididos em modelos baseados em comprimento e modelos baseados em
capturas, ambos são utilizados para estimar o estado dos estoques de espécies e
desenvolver uma gestão pesqueira viável (Kuo et al., 2023). Esses modelos foram
testados, tanto em países desenvolvidos, quanto em desenvolvimento, fornecendo
estimativas comparáveis às das avaliações convencionais e oferecendo uma visão mais
abrangente dos estoques (Zhou et al., 2017, Sagarese et al. 2018, van Germet et al.,
2022).
Vários DLMs foram desenvolvidos, como: indicadores baseados em comprimento
(LBI; Froese 2004), razão potencial de desova baseada em comprimento (LBSPR;
Hordyk et al. 2015) e abordagem de biomassa bayesiana baseada em comprimento
(LBB; Froese et al., 2018). O LBB estima simultaneamente todos os parâmetros
relevantes com uma abordagem bayesiana da Cadeia de Markov de Monte Carlo
(MCMC), que é recomendado para quantificar a incerteza na avaliação dos estoques
pesqueiros (Magnusson et al., 2013, Froese et al., 2018). Este método relaciona as taxas
de história de vida dependente de comprimento e como essas taxas interagem para

produzir uma determinada distribuição de frequência de comprimento, fornecendo:
mortalidade natural, mortalidade por pesca, comprimento assintótico, comprimento na
primeira captura, comprimento ótimo, biomassa atual explorada e a biomassa
inexplorada, consequentemente o status do estoque. LBB pode ser modelado com traços
de história de vida então, primeiro ele estima o comprimento assintótico L inf, mas, se uma
boa estimativa de Linf está disponível a partir de um estudo independente anterior, este
valor pode ser introduzido, diminuindo assim a incerteza nos resultados do LBB (Froese
et al., 2018).

2.5.2 Conhecimento Ecológico Local (LEK)
Para se ter um entendimento completo do processo pesqueiro e um consequente
manejo adequado dos recursos, para além do status do estoque, é preciso considerar as
relações humanas (Marrul-Filho, 2003, Diegues, 2001). Para gerar um plano de manejo
adequado, é fundamental o ordenamento da atividade pesqueira, como um sistema
resultante de uma combinação complexa, que avalia e integra os efeitos das dinâmicas
ambiental, social, econômica, tecnológica e política, com vistas ao uso sustentável do
recurso (Marrul-Filho, 2003, Diegues, 2001, Beddington et al., 2007). No geral, a pesquisa
e gestão da pesca está mudando de foco para colocar a pesca em um contexto mais
amplo que coloca mais ênfase nas interações entre pessoas, poder, perturbação externa
e incerteza e dinâmica de governança mais ampla (Andrew et al., 2007, Jentoft 2007;
Mahon et al., 2008).
Neste contexto, surge o conceito de Conhecimento Ecológico Local (LEK), que
consiste em um conjunto de crenças e conhecimentos empíricos acumulados sobre o
ambiente (Berkes et al., 2000). Esse conhecimento é baseado principalmente nas
observações e experiências dos moradores locais, que possuem uma compreensão
profunda e abrangente sobre conservação, transmitidos culturalmente através de
gerações (Kohl & Yli-Pelkonen, 2005; Braga et al., 2018). O LEK tem sido amplamente
utilizado em estudos de pesca (Silver & Campbell, 2005; Grant & Berkes, 2007), pois os
pescadores podem fornecer informações específicas sobre as espécies, como tamanho,
abundância, hábitos alimentares e reprodutivos, além de dados históricos e

contemporâneos das capturas (Pauly, 1995; Grant & Berkes, 2007; Rasalato et al., 2010).
Portanto, o LEK pode ser utilizado para reconstruir ou complementar tendências de longo
prazo em populações fortemente exploradas ou em espécies mal avaliadas com baixa
biomassa (linhas de base históricas), além de melhorar o planejamento, as práticas de
conservação e detectar extinções (Saenz-Arroyo et al., 2005; Thornton & Scheer, 2012;
Leduc et al., 2021).
Morril (1967) foi um dos pioneiros em pesquisa etnoictiológica, descrevendo a
compreensão dos pescadores das Ilhas Virgens (“Cha-Cha”) sobre taxonomia, ecologia,
comportamento e toxidade dos organismos marinhos. Poizat e Baran 1997 observaram
que existe uma sobreposição das informações recolhidas dos pescadores (LEK) sobre a
distribuição espacial e temporal dos peixes com os resultados de um levantamento
ictiológico (CSK) em um estuário africano. Sáenz-Arroyo e Revollo-Fernández (2016)
notaram uma forte sobreposição de dados históricos de capturas com as memórias dos
pescadores no México. No Brasil, em Alagoas, Marques (1991) também observou uma
forte sobreposição de LEK e CSK ao analisar o conteúdo estomacal de bagre no
Complexo Estuarino Lagunar Mundaú Manguaba.
Os estudos que incorporam o LEK também trazem benefícios significativos para
os próprios pescadores. Por exemplo, fortalecem seus valores culturais, proporcionam
maior voz política e reconhecimento por parte dos gestores, auxiliam na resolução de
disputas de manejo, aprimoram o diálogo entre os pescadores e as agências de gestão,
promovendo uma gestão participativa e horizontal dos recursos pesqueiros (Ruddle 1995;
Berkes 1999).
Como exemplo de LEK aplicado a pesca das tainhas, temos o trabalho de Herbst
e Hanazaki (2014), que investigaram o conhecimento ecológico local dos pescadores ao
longo de um gradiente latitudinal no litoral de Santa Catarina, sobre o ciclo de vida da
tainha Mugil liza, dando ênfase aos aspectos migratórios, alimentares, reprodutivos e
comportamentais. Foi concluído que pescadores possuem um conhecimento detalhado
sobre o ciclo de vida da tainha e identificam variações intra e interanuais nas rotas
migratórias, e esse padrão precisa ser considerado no manejo da pescaria.

2.5.3 Pesca de tainhas
Essa gestão participativa é especialmente importante para espécies de Mugil, pois
são um dos recursos mais consumidos no Brasil, representando cerca de 20% da pesca
comercial, uma das maiores pescarias de Mugilideos do mundo (MPA, 2011). As
espécies mais abundantes nas capturas são M. liza e M. curema. Na região Sul do país,
M. liza é responsável pela mobilização de uma frota industrial de traineiras e frotas de
média escala como o emalhe anilhado, além de milhares de pescadores artesanais em
todas as regiões das lagoas e estuários (Vieira & Scalabrin, 1991). Já na região Nordeste
a pesca é artesanal, possuindo uma grande importância econômica, social e cultural, com
volume de captura muito mais baixo, porém existe a exploração simultânea de várias
espécies, sendo M. liza substituída por M. curema, que é a espécie mais capturada na
região (Santana da Silva, 2007).
As condições de mercado interferem nos desembarques, pois, dependendo da
época, o esforço de pesca é direcionado para peixes mais rentáveis, causando redução
nos desembarques de tainha (Steele & Bert, 1998, Mendonça & Machado 2010). Sendo
assim, as capturas de tainha mais baixas em alguns meses do ano e mais altas em
outros. Assim, as oscilações na produção devem-se principalmente ao aumento da
presença de pescadores em busca de melhores fontes de renda.
O comércio das ovas de Mugil é histórico no Brasil. Na região sul do país as
gônadas de M. liza são colhidas na época reprodutiva e exportadas como ‘Bottarga’ para
mercados internacionais. Essa pesca ocorre quando imensos cardumes estão em
direção norte, para se reproduzir, sendo um momento de grande vulnerabilidade para a
espécie, aumentando a sobrepesca. Esse comércio representa uma ameaça significativa
à conservação desta espécie, e a Instrução Interministerial Brasileira (MPA/MMA nº 7 de
2011) proibiu o desembarque de ovas de M. liza sem suas carcaças. Na região nordeste
esta prática histórica de consumo de ovas de Mugil também ocorre e é potencialmente
negativa para o manejo do estoque, uma vez que capturam os peixes durante o período
reprodutivo, especificamente antes da desova (Marques et al., 2005, Cascudo, 1984).
Esse comercio era intensificado no período da quaresma, onde a quantidade de Mugil
capturada era muito numerosas porque os pescadores procuram apenas as ovas, não

utilizando todos os peixes para alimentação. (Cascudo, 1984). Marques e colaboradores
(2005) relatam que uma cena comum era observar corpos de curimãs deixados às
margens da Lagoa Mundaú, pois a população local não conseguia utilizar todos aqueles
peixes, mas ovas necessárias para suprir o consumo tradicional da população local era
muito alto. Atualmente, as ovas de curimãs e tainhas ainda são um alimento tradicional
em Alagoas (Marques et al., 2005). No entanto, esta prática já não é comum como
antigamente, devido à baixa oferta pelo declínio drástico dos estoques em certa forma,
devido à consciência dos pescadores em face ao declínio do estoque, ou pela educação
ambiental conduzida por ONGs, escolas e academia (Santos & Sampaio, 2013; Siemer
& Knuth, 2001; Patterson et al., 2009).
Mugil liza foi recomendada para classificação como Quase Ameaçada (NT) sob a
recente revisão da IUCN no Brasil, e em 2004 a espécie foi classificada como
superexplorada

pelo

Ministério

Pesca

Aquicultura

Brasil

(IBAMA/ICMBIO/CEPSUL, 2007). Esse problema de sobrepesca para M. liza já foi
reconhecida pelo governo federal, que em 2015, instituiu o Plano de Gestão da Pesca da
Tainha. Já as outras espécies do gênero são considerados deficiente em dados pela
IUCN. Já que raramente são relatadas nas estatísticas, porque geralmente ocorre nos
desembarques da pesca artesanal. Então o seu rendimento é normalmente subestimado
nas estatísticas e também no número de embarcações registadas (Mendonça & Miranda,
2008; Mendonça & Machado, 2010).
Os Mugilideos são muito vulneráveis à atividade de pesca pois possuem
relativamente alta longevidade, maturação sexual tardia, são capturada em todos os
estágios da vida, e principalmente durante o período reprodutivo em cardumes (safra).
Apesar dessa importância para os desembarques, no nordeste do Brasil não existe plano
de manejo, nem período de defeso para este grupo (Sousa et al., 2015).
As tainhas possuem uma forte conexão com a história, a cultura e a economia de
Alagoas. Tanto é que sua relevância está eternizada na bandeira do estado, que exibe
três tainhas, representando não apenas a riqueza dos recursos pesqueiros, mas também
a importância da pesca artesanal para o sustento das comunidades costeiras. As tainhas
foram durante décadas o recurso pesqueiro mais importante do estado. Em 2005, a

produção de tainhas em Alagoas alcançou 1.766,4 toneladas, representando 18,1% de
toda a produção de pescado marinho e estuarino no estado (IBAMA, 2006). Em 2007, as
tainhas corresponderam a 13% dos desembarques pesqueiros totais, destacando sua
relevância para a economia local (IBAMA, 2007). Após 2007, as estatísticas oficiais sobre
a pesca de tainha em Alagoas tornaram-se escassas.
As pescarias na região são realizadas utilizando oito principais aparelhos de
pesca: rede de espera, rede de cerco, tarrafa, linha, arrasto duplo, a rede de caceia, a
rede de cerco e o arrastão de praia. Cada uma dessas técnicas resulta em capturas de
diferentes espécies de tainhas, além de incluir outras espécies da fauna acompanhante
associada

essa

atividade.

pesca

com

rede

cerco

concentra-se

predominantemente na captura de Mugil curvidens e M. curema, enquanto a rede de
espera e a linha são mais eficazes para capturar Mugil liza. Já a tarrafa é mais utilizada
para capturar Mugil curema e Mugil curvidens. Essa diversidade de métodos reflete a
adaptação das práticas de pesca às características comportamentais e ecológicas de
cada espécie (Torres et al. 2007; Rangely 2011).
A captura das tainhas nos rios, lagunas e no litoral sempre foi uma atividade
essencial, fornecendo alimento e renda para inúmeras famílias que dependiam
diretamente da pesca para sobreviver. Seu comércio movimentava mercados locais e
desempenhava um papel importante na identidade cultural de Alagoas, marcando
presença em pratos típicos e celebrações regionais (Cascudo, 1984; Marques et al.,
2005).
Preservar as tainhas vai além de garantir a continuidade da pesca; trata-se de
valorizar a história de Alagoas, suas tradições e o sustento das futuras gerações. O
cuidado com os ecossistemas costeiros, como estuários e manguezais, é crucial para a
sobrevivência das tainhas e para manter viva a ligação entre esse peixe icônico e o povo
alagoano.

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3 CONGENERIC, SYMPATRIC TROPICAL MULLETS RESPOND DIFFERENTLY TO
ENVIRONMENTAL VARIABILITY: INSIGHTS INTO COEXISTENCE
Jordana Rangely1,2, Matheus de Barros*3,4, Daniele Souto-Vieira1, Maria das Neves
Tayana S. C. Oliveira5, Victor E. L. da Silva1, Ivan Oliveira de Assis1, Nidia N. Fabré1
1Laboratório de Ecologia de Peixes e Pesca (LaEPP), Universidade Federal de Alagoas,

Maceió, Brasil.
2Instituto Federal de Educação, Ciência e Tecnologia de Alagoas (IFAL), Maceió, Brasil.
3School of Marine and Environmental Sciences, University of South Alabama, Mobile, AL,

USA
4Shelby Center for Ecosystem-Based Fisheries Management, Dauphin Island Sea Lab,

Dauphin Island, AL, 36528
5Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Aveiro, Portugal.

Artigo publicado: https://doi.org/10.1071/MF23108
RANGELY, Jordana et al. Congeneric and sympatric tropical mullets respond differently
to environmental variability: insights into coexistence. Marine and Freshwater Research,
v. 75, n. 9, p. NULL-NULL, 2024.

Abstract
Context: Disentangling mechanisms influencing the seasonal and spatial distribution of
fish is essential to understanding population dynamics. In the Southwestern Atlantic, the
sympatric mullets Mugil curema and M. rubrioculus are closely related and use habitat
similarly. However, which processes allows their coexistence is unknown.
Aim: We tested the hypothesis that the species exhibit different habitat use patterns that
are temporally decoupled to allow sympatry due to different responses to environmental
drivers. Methods: Bayesian zero-inflated models were used to unravel spatial and
temporal distribution patterns of those species in a Southwestern Atlantic lagoon.
Key results: The two species display different distribution within the estuary, being
spatially and temporally segregated, with M. curema mostly inhabiting inner portions and
M. rubrioculus inhabiting the outer estuary.
Conclusions: This decoupling in habitat use might be driven by distinct responses to
environmental variability: M. curema is influenced by factors such as temperature and
dissolved oxygen, while M. rubrioculus by variations in salinity. We suggest that the
studied species evolved divergent responses to environmental variation to allow
coexistence.
Implications: This study suggests that environmental factors drive the abundance of
mullets inside estuaries, and are therefore useful in predicting their spatial and temporal
distribution.

Keywords: ecology, fish, Mugil, habitat use, fisheries, salinity, estuary, temperature

Introduction
Mechanisms underlying the spatial co-occurrence of species have always drawn the
attention of ecologists (Dufour et al., 2015; Winston, 1995). Because sympatric
congeneric species tend to be ecologically similar, presenting similar habitat requirements
and feeding on roughly the same available resources (Schoener, 1974), insights into
which mechanism allows their coexistence are considered to be of great importance to
understand ecological differentiation and processes behind the structuration of biological
communities (Ackerly et al. 2006), as well as to provide useful insights to management
and conservation (Davidson-Watts et al. 2006; Di Bitetti et al. 2008; Jirapunpipat et al.
2009). Historically, many drivers of species coexistence such as habitat selection
(Davidson-Watts et al., 2006), trait divergence (Ackerly et al. 2006; da Silva et al. 2019)
and niche differentiation (da Silva & Fabré, 2019) have been identified. However, the
astonishing variability in strategies adopted by co-occurring species warrants a closer
species-specific examination of its drivers, especially when it comes to closely related and
commercially important species.
At a local scale, ecologically similar species are expected to exhibit morphological
differences, as well as spatial and/or temporal segregation in microhabitat and resource
use to reduce competition (Ackerly et al. 2006). However, for a few congeneric species,
these assumptions appear to be in contradiction. The family Mugilidae, for example,
contains a substantial number of co-occurring species, which are abundantly present in
estuaries and other coastal regions in tropical and subtropical regions (Blaber, 2000).
Despite showing highly conservative morphological features (Menezes et al. 2015) and
similar ecological traits such as feeding habits (Garcia et al. 2018), habitat requirements
have been demonstrated to significantly overlap between species (Ibáñez et al. 2012),
with factors such as temperature and salinity being able to influence their habitat use
patterns (Cardona et al. 2008; Lemos et al. 2021). However, there is scant evidence of
habitat partitioning in congeneric species as a mechanism to allow for coexistence through
changing niche amplitude (Garcia et al. 2018).
In the Tropical Western Atlantic, mullets are represented by the abundant and
commercially important genus Mugil, with eight species (Menezes et al. 2015). Out of

these, M. curema and M. rubrioculus are closely related and the most morphologically
similar species (Neves et al. 2020, 2021). M. curema and M. rubrioculus live in sympatry
and have very similar life cycles (Avigliano et al. 2021; Ibáñez et al. 2012; Menezes et al.
2015). Although data for M. rubrioculus is highly scarce in the literature (da Silva et al.
2017a), M. curema was previously suggested to be in a state of overfishing or population
decline (Mendonça and Bonfante, 2011), highlighting the need of gathering relevant
ecological information that may aid future management decisions.
Classical ecological niche theory states that species with similar ecological
requirements and life history need to partition resources to maintain coexistence, and
habitat heterogeneity plays a crucial role in niche differentiation (Jenkins et al. 2019;
Schoener, 1974). Recent studies revealed that M. curema and M. rubrioculus display
significant interspecific variation in some life-history traits such as length-at-age, maturity
and allometry, possible evidence of niche differentiation reflected on ecological traits
(Rangely et al. 2023). However, it is still not known how such species arrange themselves
spatially and temporally in relation to each other. The aim of this study was to identify
spatial and temporal patterns in the distribution of the white mullet M. curema and redeye
mullet M. rubrioculus in a tropical estuary of the Southwestern Atlantic. We addressed the
following question: what is the role of environmental variability in shaping the distribution
patterns of these fish at a local scale? We hypothesized that those morphologically similar,
congeneric species may exhibit some degree of spatial and temporal segregation driven
by different responses to environmental factors as a mechanism to allow coexistence.

Materials and methods
Study area and sampling
Sampling was executed in the Mundaú Lagoon, located in a tropical and semi-humid
region of the Southwestern Atlantic coast. The area has two well-defined seasons
characterized by rainfall patterns: a dry season from October to March and a rainy season
from April to September. There, eight sampling sites were placed to cover the whole
estuarine gradient: from the upper estuarine to the surf zone at the sea, with two sampling
points in each region (upper, middle, lower estuary, and sea) (Fig. 1). Each site was
monthly sampled from November 2013 to October 2014 with a 1000 m long and 3 m wide
seine net with 35 mm of mesh opening, a traditional local fishing gear usually utilized to
capture mugilids (Torres et al. 2007). This net was deployed in the water by artisanal
fishers using two small boats to enclose the sampling site for about 20 minutes, forming
a semicircle with a set of baited hooks attached at the end of the net. All sampling
procedures were executed systematically by the same fishing team to reduce potential
effects of different fishing skills. In this way, we could assume absolute count data
represents abundance since the effort was standardized. The two fishing sets from each
region are more than 1 km distant from one another, which ensures independence
between samples (e.g. de Barros et al. 2023). Two fishing sets per site/month were
deployed, which totals 96 sets for the whole year. More replication would be necessary to
obtain a more accurate picture of the spatial variability on mullet abundance, but we were
limited by logistical constraints such as the need for the tides to be below a certain level.
While our sampling is limited regarding the spatial variability in mullet abundance, we
argue the data is still sufficient to answer the main question posed in this study about how
environmental factors influence mullet abundances because of sufficient temporal
coverage. At each sampling point, the following physicochemical and environmental
variables were recorded in situ from water samples: temperature (∘ C), turbidity (NTU),
salinity (parts per thousand - ppt), dissolved oxygen (mg/l), conductivity (μmhos/cm), and
primary productivity (μg/l of chlorophyll a). Abiotic variables were recorded with a
Multiparameter Sonde (YSI 6600 V2). In addition, mean monthly rainfall (mm) for the
corresponding region was retrieved from http://www.semarh.al.gov.br/ (SEMARH, 2024).

Then, fish were identified in the laboratory by specialized taxonomic keys and processed.
Sampling and transport were authorized by the Biodiversity Information and Authorization
System - SISBIO (license number 56293-1).

Figure 1. Map showing the sampling points within the Mundau Lagoon, Northwestern
Atlantic.

Data analysis
Because of the high proportion of zeros in the mullet count data, log-transformation
was not effective in producing normally-distributed data. Then, we compared fish counts
with a non-parametric Mann-Whitney U test. Effects of environmental variability on the
abundance of M. curema and M. rubrioculus were modeled using Bayesian zero-inflated,
random-effects models with Monte Carlo Markov Chains (MCMC) algorithms. A zeroinflated model was considered the most appropriate after checking if a conventional
generalized linear model (GLM) was underfitting zeros in the R package “performance”

(Lüdecke et al. 2021). The number of iterations was set to 500K and 10K burn-ins in the
“r2jags” R package, an implementation of the JAGS (Just Another Gibbs Sampler) for the
R statistical software (Su and Yajima, 2012). A complete description of the modeling
framework is as follows:
Let Y = {yi, i = 1,…, N} be a N-dimensional variable denoting the counts of M. curema
and M. rubrioculus in the study area. We assume Y is generated by a mixture of two
distinct processes as follows:

𝜃 + (1 − 𝜃)𝑒 −𝜆 𝑓𝑜𝑟𝑦𝑖 = 0
𝜆 𝑦[𝑖] −𝜆
𝑝(𝑦[𝑖] ∨ 𝜃, 𝜆) = {
(1 − 𝜃)(
)𝑒 𝑓𝑜𝑟𝑦𝑖 > 0
𝑦!
where θ is the overall probability of observing zeros in the data. We model θ as a function
of covariates using the logit link:

𝜃=

𝑒 (𝛾0+𝛾[𝜅] 𝑋)
1 + 𝑒 (𝛾0+𝛾[𝜅]𝑋)

𝛾0 𝛮(0, 𝜎𝛾0 )
𝜎𝛾0 ℎ𝑎𝑙𝑓𝐶𝑎𝑢𝑐ℎ𝑦 (0,1)
𝛾[𝜅] 𝛮(0, 𝜎𝛾[𝜅] )
𝜎𝛾[𝜅] ℎ𝑎𝑙𝑓𝐶𝑎𝑢𝑐ℎ𝑦 (0,1)
where γ0 is an intercept and γk is a K-dimensional vector of coefficients for each k-th
covariate, while X represents a K x N-dimensional matrix of covariates. Coefficients follow
non-informative prior distributions centered at zero with half-Cauchy standard deviations.
For data points that are not zero, Y is assumed to follow a Poisson distribution with rate
parameter λ:

𝑌𝑃𝑜𝑖𝑠𝑠𝑜𝑛(𝜆)
𝜆 = 𝑒 (𝛽0+𝛽[𝜅] 𝑋)

𝛽0 𝛮(0, 𝜎𝛽0 )
𝜎𝛽0 ℎ𝑎𝑙𝑓𝐶𝑎𝑢𝑐ℎ𝑦 (0,1)
𝛽[𝜅] 𝛮(0, 𝜎𝛽[𝜅] )
𝜎𝛽[𝜅] ℎ𝑎𝑙𝑓𝐶𝑎𝑢𝑐ℎ𝑦 (0,1)
where β0 is an intercept and β[k] is a K-dimensional vector of coefficients for each k-th
covariate, and X is the same K x N-dimensional covariate matrix as in above. The
covariates included in the model are environmental data on salinity (ppt), temperature
(Celsius), Dissolved Oxygen (mg/L), turbidity (NTU), Chlorophyll concentration (mg/L),
and rainfall (mm), as well as the abundance of the other mullet (number of individuals),
and collection site (Figure 1). The coefficient for collection site is random, while the other
parameters are fixed for both count and presence-absence models. The resulting loglikelihood function for the Poisson Zero-inflated model may be then written as follows:

𝑙𝑜𝑔𝐿(𝛽, 𝛾) = ∑ log⁡
𝑦[𝑖]=0
(𝑋𝛾)
+ ∑𝑦[𝑖]>0[𝑦[𝑖] 𝑋𝛽 − 𝑒 (𝑋𝛽) − 𝑙𝑜𝑔(𝑦[𝑖] !)] − ∑𝑁
]
𝑖=1 log[1 + 𝑒

Posterior predictive checks were conducted by sampling from the posterior
predictive distributions for the models from both species and comparing these graphically
to the observed data. We evaluated all possible model combinations taking into
consideration the list of explanatory variables considered in this study and identified the
set of most adequate models according to the smallest BIC (Bayesian Information Criteria)
and DIC. Explanatory variables were previously examined for collinearity using the
Spearman’s rank correlation test at a threshold of r > 0.7 for highly correlated variables
(Dormann et al. 2013). If collinearity was detected, the models were executed separately
with each variable to examine their respective BIC and DIC values. Then, the variable that
generated a model with the lowest predictive error was selected for the general model,
while the other was excluded. As a result, only water conductivity was excluded because

of an expected high correlation with salinity (r = 0.78). For model diagnostics, MCMC chain
convergence was checked with the potential scale reduction factor, which compares
within and between-chain variances to test the null hypothesis of homogeneity of
variances of posterior distribution among parallel chains (Brooks and Gelman, 1998). The
models were considered to converge when the upper limit of the convergence diagnostic
is close to unity. Posterior predictive checks were executed by analysing model residual
distribution after comparing predicted and simulated data (Gelman et al. 2000). Effects of
explanatory variables were considered significant if 80% of the posterior distributions did
not overlap zero, following standard procedures that require defined criteria for hypothesis
tests within a Bayesian framework (Kruschke, 2021).
Results
All measured environmental factors varied spatially and temporally within the study
area. Temperature was at its highest (> 30 Celsius) during the dry season, and at its
lowest during the wet season (< 26 Celsius). The inner lagoon appeared to have hottest
temperatures, while the sea was colder. Expectedly, salinity was highest at the sea and
lowest at the upper and middle lagoon regions, and varied seasonally at all sampled
regions with peaks during the dry season. Turbidity was spatially similar, but peaked inside
the lagoon at the end of the wet season. Primary productivity was higher inside the lagoon,
at which there were peaks during the wet season. Finally, dissolved oxygen was the
lowest at the sea (Fig. 2).

Figure 2. Monthly variation in environmental parameters measured at different regions of
the Mundau Lagoon, Northwestern Atlantic.

A total of 1167 individuals were collected during the sampling period in 96 replicate
net hauls, with 985 being M. curema and 182 M. rubrioculus. Evidently, the white mullet
M. curema was far more abundant than the redeye mullet M. rubrioculus (Mann Whitney
U test, p < 0.0001). Even though, the species appeared to exhibit substantial differences
in their patterns of abundance within and outside the estuary, which also seems to vary
seasonally (Figure 3). Specifically, the white mullet is evenly distributed inside the estuary
and less abundant at the sea during the dry season. In the rainy season, the white mullet
is more abundant in the upper lagoon. The redeye mullet is much more abundant at the
sea than inside the estuary in the rainy season, while it seems to enter estuarine regions
with the advent of the dry season (Fig. 3).

Figure 3. Spatial and temporal variation in abundance (counts) of white and redeye mullets
at the Munda Lagoon, north-western Atlantic. The vertical axis shows the log-transformed
means and two standard errors of mullet counts.

According to the traceplots for the three MCMC chains and the potential scale
reduction factor, Bayesian zero-inflated model outputs showed full convergence to the
posterior for almost all model parameters after 500K iterations and 10K burn-ins. The
regression coefficient for temperature was the only parameter that exhibited slight signs
of non-convergence on the models for both species, possibly due to multiple local minima
on the negative log-likelihood profile. Posterior predictive checks show that the model for
M. curema can accurately predict the observed data, with a normal residual distribution.
The model for M. rubrioculus was not as good on predicting all the variation and spread
of the data, but still useful to describe its general trends (Fig. 4). In fact, after including all
variables and random effects in the models, predictive error (DIC statistic) was reduced
from more than 2000 to about 250 – 300 for both models. Posterior distributions and
credible intervals of model parameters show that the examined species exhibit different
responses to environmental variability. The abundance of the white mullet is positively
influenced by temperature and primary productivity, and negatively by dissolved oxygen,
turbidity, and rainfall. Conversely, abundances of the redeye mullet are only positively

influenced by salinity. Both species also seem to negatively respond to increased
abundance of their congeneric (Fig. 5, Table 1).

Fig 4. Posterior predictive check for the Bayesian zero-inflated generalised linear models
fit to count data of white (top) and redeye (bottom) mullet species sampled at the Mundaú
Lagoon, north-western Atlantic. Individual data points represent observed quantities and
coloured lines are median model fits.

Table 1. Summary of posterior distributions for the random-effects zero-inflated model
parameters for predicting the abundance of M. curema and M. rubrioculus. 80% credible
intervals were selected according to criteria for hypothesis testing within a Bayesian
framework. Values highlighted in bold denote a “significant” effect. “Mullet” refers to the
coefficient for the abundance of the congeneric species affecting the other.

Parameter
Probability of
Encounter
Temperature
Salinity
Turbidity

M. curema
Median
80% credible
estimate
interval
0.93
0.90 to 0.96

M. rubrioculus
Median
80% credible
estimate
interval
0.67
0.089 - 0.1

0.408
0.002
-0.035

0.286 to 0.545
0.115
-0.151 to 0.478
-0.036 to 0.042
0.072
0.044 to 0.104
-0.044 to 0.004
-0.029 to 0.018
0.026
Chlorophyll
0.034
0.026 to 0.041
-0.0014
-0.011 to 0.046
Mullet
-0.024
-0.012 to -0.047
-0.028 to 0.036
0.062
Dissolved O2
-0.11
-0.149 to -0.042
-0.153 to 0.065
Rainfall
-0.049
0.072
-0.001
-0.012 to 0.01
-0.077 to -0.01
80% credible intervals were selected according to criteria for hypothesis testing within a
Bayesian framework. Values highlighted in bold denote a ‘significant’ effect. ‘Mullet’ refers
to the coefficient for the abundance of the congeneric species affecting the other.

Fig 5. Influence of environmental parameters on the abundance of white and redeye
mullets within the Mundaú Lagoon, north-western Atlantic. Points represent Bayesian

posterior medians from the zero-inflated models and lines represent the 80% credible
intervals after 500,000 iterations. DO, dissolved oxygen.

Discussion
Current ecological theory states that sympatric, morphologically alike species with
similar life-history traits such as M. rubrioculis and M. curema (Rangely et al. 2023) are
expected to exhibit mechanisms to allow for coexistence and reduce overlap in resource
use that often result in subtle trait divergences (Holt et al. 1994; Porreca et al. 2017). Our
results suggest that the habitat use patterns of the studied species are spatially and
temporally decoupled (Figure 6) due to different responses to environmental variability.
Specifically, M. rubrioculus, driven by salinity, occupies outer estuarine reaches and the
sea, only penetrating inner estuarine areas during the dry season. M. curema is driven by
temperature, dissolved oxygen, chlorophyll, and turbidity, being able to occupy the inner
estuary.

Fig 6. Infographic illustrating the spatial-temporal movements of white and redeye mullet
M.curema and M. rubrioculus in the Mundaú Lagoon, north-western Atlantic.

Evolutionary responses to coexistence leading to niche differentiation can vary
considerably from mechanisms such as dietary mismatches and different life-histories to

distinct responses to varying environmental conditions (da Silva et al. 2017b; Rangely et
al. 2023; Ulrich and Tallman, 2021). The advent of different responses to abiotic factors
in sympatric species has long been acknowledged as an evolutionary tool that makes
each species have optimal competitive fitness in different environments, hence
contributing to ecological partitioning (Lombarte et al. 2000). Therefore, one of the
mechanisms that could have led to such decoupled life histories in tropical mullets is
character displacement, acknowledged as a common process when sympatric species
are found to differ in resource use (Goldberg and Lande, 2006). Ecological character
displacement can be explained as competition-induced differences in life-history traits
through phenotypic plasticity, causing differential selection to take place (Slatkin, 1980).
This process is a key driver of species diversity, also often associated with sympatric
speciation (Schluter and McPhail, 1992; Tyerman et al. 2008). Despite being previously
seen as relatively rare in nature because the presence of gene flow usually slows down
trait divergence, sympatric speciation is now acknowledged as one of the main
mechanisms leading to the formation of species with similar ecological requirements but
with fine-scale divergences due to the presence of assortive mating among individuals
with a particular trait (Barluenga et al. 2006; Bird et al. 2012; Jiggins, 2006). Therefore,
such process is thought to select individuals that perform better in certain environmental
conditions (see Johannesson, 2001 for a review on sympatric/parallel speciation and its
mechanisms). In fact, phylogenetic studies on the genus Mugil found that M. curema and
M. rubrioculus are the most closely related among tropical mullets, and their lineages have
diverged more recently (Neves et al. 2020, 2021), which supports the occurrence of
sympatric speciation.
Complex interactions between biotic and abiotic variables come into place to
explain variations in fish habitat use over time and space (da Silva et al. 2021, 2022). An
important density-dependent effect on fish populations is interspecific competition, which
can be particularly strong on sympatric, closely-related species and influences factors
such as growth and habitat use (Andersen et al. 2017; Hasegawa, 2016). As a response,
the overlap in niche between populations of competing species tends to decrease to
minimize competition (Johannesson, 2001; Lombarte et al. 2000). The white mullet M.

curema, ubiquitous inside the estuary, is a generalist predator able to adapt to various
prey community structures (Garcia et al. 2018), which is usually favored inside estuarine
regions due to the commonly higher diversity and abundances of potential prey in its
productive waters. Unfortunately, such information is not yet available for the redeye
mullet. Even so, we speculate that this species may present less variable feeding habits
and, consequently, a stricter ecological niche when compared to M. curema because of
the less variable spatial distribution found in this study. Then, an apparent resource
partitioning, apart from the evident spatial segregation, should be another mechanism
allowing such species to coexist (when and where they do), which was previously
observed in the study of Garcia et al. (2018) between M. curema and M. liza in a
subtropical estuary.
The spatial and temporal decoupling showed by the studied species follows
common dynamics of tropical coastal habitats. Estuaries are one of the most dynamic
systems among coastal habitats, with marked variations in environmental conditions due
to its connection with both terrestrial and oceanic systems (Macedo et al. 2023; Ram et
al. 2003). Accordingly, biological communities are highly affected by such considerable
environmental changes, including nekton (Jaureguizar et al. 2021; Childs et al. 2008).
Unlike temperate regions, where temperature variations control most environmental
changes and ecological cycles, nekton on tropical estuarine environments are usually
driven by seasonal variations in rainfall (wet/dry seasons) (da Silva et al. 2018; de Barros
et al. 2022; Macedo et al. 2021), which affect water mixing and nutrient dynamics on
estuaries (Burford et al, 2012; Medeiros and Kjerfve, 1993). The tropical rainy season
drives allochthonous entrances from upstream that increase primary productivity, reduces
salinity, dissolved oxygen and enhances water turbidity (Carrillo et al. 2009; Kress et al.
2002), while conditions in the dry season include the penetration of sea-like conditions
inside the estuary (Azhikodan et al. 2021). Our results suggest M. rubrioculus might be
more adapted to higher salinities (Figure 5), being mostly restricted to occupy areas
outside the estuary during the rainy season (Figure 3). Conversely, the advent of the dry
season allows this species to penetrate the estuary due to increased saltwater intrusion.
M. curema, not restricted by salinity, was evenly distributed inside the estuary during the

rainy season (Figure 2), where dissolved oxygen is lower, but turbidity and primary
productivity are higher. In the dry season, when M. rubrioculus can penetrate estuarine
regions, M. curema showed higher abundances on the upper estuarine region, which
could be attributed to effects of interspecific competition.
Mullets are an important fishery resource in South America, but few mullet stocks
are assessed in the region since those fisheries are artisanal and small-scale. With some
reports of overfishing (Mendonça and Bonfante, 2011) and increasing fishing pressure
due to population growth in the region (Blaber and Barletta, 2016), assessment and
management efforts will be vital to ensure the long-term sustainability of these resources.
Fisheries stock assessments primarily rely on abundance indexes to infer trends in the
population over time (Maunder and Punt 2004). However, raw abundance indexes often
do not reflect the true abundance since variations in the index can also reflect numerous
other factors such as sampling artifacts, variations in environmental conditions at the time
of sampling, and fishing behaviour (Maunder et al. 2006). Therefore, data standardization
(i.e. ‘removing’ the influence of factors other than abundance) is necessary for the index
to be used as a reliable indicator of population trends (Hinton and Maunder 2004). In our
study, we demonstrate that the abundances of M. curema and M. rubrioculus are
significantly impacted by variations in environmental conditions, which should therefore
be accounted for in future assessments. We also highlight the usefulness of modelling
frameworks that can handle overdispersed characteristics in the data such as zero
inflation, being therefore highly useful for species with patchy distributions. In fact, zeroinflated models have been extensively used in CPUE standardization procedures, and
produce reliable results when the right explanatory variables are accounted for (AlvarezBerastegui et al. 2018, Brodziak and Walsh 2013, Hiraoka et al. 2015).

Conclusions
The studied species showed significant spatial segregation in the Mundaú Lagoon
Estuary, which appears to be a result of divergent adaptation resulting in distinct
responses to environmental conditions between species. As a result, the white mullet,
which is more abundant, is substantially widespread inside the lagoon. Conversely, the

redeye mullet exhibits a remarkably low abundance inside the estuary, whereas it is much
more present at the sea, where salinity is at its highest. The inherent seasonality of tropical
estuaries appears to rearrange the species distribution within the different estuarine
regions. Management decisions towards improving mullet conservation and stock
productivity should incorporate the small-scale variability in spatial distribution assessed
here into future species distribution models. Further, the influence of predicted shifts in
abiotic parameters due to climate change on the studied species should be explored.

Acknowledgements
We would like to thank all members of the Laboratory of Ecology, Fish and Fisheries at
the Federal University of Alagoas. Special thanks to all fishers who helped with fish
sampling and to Mônica Albuquerque for making the infographic art. Sampling, transport,
and animal ethics approval were provided by the Brazilian Biodiversity Information System
(SISBIO) (#56293-1).

Declaration of funding statement
Data collection was partially funded by the State Funding Agency of Alagoas (FAPEAL)
and the National Council for Scientific and Technological Development (CNPq). N.N.F.
was funded by the Brazilian National Council for Scientific and Technological
Development – CNPq (#304433/2022-5).

Conflict of interest
The authors have no conflict of interest to declare.

Data availability statement
The dataset used for analyses in this study can be made available upon reasonable
request to the corresponding author.

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4. ASSESSING INTERSPECIFIC VARIATION IN LIFE-HISTORY TRAITS OF THREE
SYMPATRIC TROPICAL MULLETS USING AGE, GROWTH AND OTOLITH
ALLOMETRY
Jordana Rangely*1,2, Matheus S. F. de Barros3,4, Mônica D. Albuquerque-Tenório1,
Reginaldo Medeiros1, Richard James Ladle5, Nidia Noemi Fabré1
1Laboratório

de Ecologia, Peixes e Pesca (LaEPP) da Universidade Federal de

Alagoas (UFAL), Instituto de Ciências Biológicas e da Saúde
2Instituto Federal de Educação, Ciência e Tecnologia de Alagoas (IFAL)
3School of Marine and Environmental Sciences, University of South Alabama, Mobile,

AL, USA
4Shelby Center for Ecosystem-Based Fisheries Management, Dauphin Island Sea

Lab, Dauphin Island, AL 36528
5CIBIO-InBIO,

Universidade do Porto, Campus de Vairão, Rua Padre Armando

Quintas, 4485-661 Vairão, Portugal

Artigo publicado: https://doi.org/10.1016/j.fishres.2022.106577
RANGELY, Jordana et al. Assessing interspecific variation in life-history traits of three
sympatric tropical mullets using age, growth and otolith allometry. Fisheries Research, v.
260, p. 106577, 2023.

Highlights

• Validation of annuli deposition for three sympatric, tropical mullets is provided.
• Otolith allometry is integrated with age, growth and reproduction.
• Otolith allometry is a potential predictor of key life cycle events.
• The studied species adjust their life-history traits to allow for coexistence.
• Information provided here allows for further look into possible management
options.

Abstract
Life history theory predicts that organisms optimize their life-history traits according to
evolutionary context and environmental constraints. Sympatric estuarine-dependent fish
are intriguing subjects for studying life-history variation, as their traits are molded by their
complex habitat use and co-occurrence with ecologically similar species. In this study, we
investigated life-history traits of three tropical mullet species (Mugil curema, M. liza and M.
rubrioculus) using otolith age, growth, and allometry. Our results indicate that otolith
allometric patterns are useful predictors of specific life history traits: the faster-growing
species M. rubrioculus (K = 0.31) was characterized by earlier stanza changing points
(SCPs), with 0.8 years of life. In contrast, the slower-growing species, M. liza (K = 0.21)
was characterized by later changing points, 1.3 years of life. M. curema is intermediate (K
= 0.25), with 0.95 years of life. The first SCP may register juvenile movements between
estuarine and coastal habitats before the first year of life, and the second SCPs appear
to reflect the migration to the sea and age at maturation. More generally, our study species
exhibit fine-scale temporal differences in life cycle events that may be negatively related
to growth rates and body size that can be predicted by otolith allometry, as well as a
gradient of interspecific divergences in life-history traits. These are likely to be driven by
differences in their migratory behavior and habitat use that permit coexistence.

Keywords: fish, fisheries, Mugil, sympatry, estuarine-dependent, life cycle

1 Introduction
Life-history theory predicts that organisms make optimal decisions about how to
best allocate energy to mutually exclusive processes such as growth, reproduction and
migration (Marquet et al., 2014; Reiners et al., 2017; Winemiller, 2011). As a result, a
unique and optimal set of traits emerge that maximize fitness in the species' evolutionary
and ecological context (Stearns, 2015). Recent developments in life-history theory
suggest that a species’ life-history traits can be used to accurately predict its responses
to environmental constraints such as seasonality, abiotic variability and habitat use
(Perkin et al., 2016; Hitt et al., 2020).
Connectivity within a seascape is often conceptualized as the product of complex
interactions among different biophysical elements such as coastal and estuarine
ecosystems (Ray, 2005; Taylor et al., 1999, Macedo et al, 2021). Some opportunistic
marine or freshwater species utilize estuarine habitats for early growth or reproduction
(Able, 2005; Ray, 2005), despite the additional costs associated with osmoregulation
(Cardona, 2000). Among estuarine-dependent fish, the family Mugilidae (mullets) is one
of the most representative, with the genus Mugil being particularly pervasive in tropical
and subtropical coastal environments (Froese & Pauly, 2008; Menezes et al., 2015).
Mullets usually exhibit complex migratory behaviors, with particularly variable habitat use
patterns in different life cycle stages (Avigliano et al., 2021; Mai et al., 2018). According
to Avigliano et al. (2021), the most common habitat use pattern for mullets is estuarine
migratory, in which the estuary is vital at some point of their life cycle. Mullets typically use
estuaries as nurseries, where juveniles take advantage of the higher nutrient input and
structured habitats to rapidly develop in their first year(s) of life. After that, they typically
migrate to coastal seas, where reproduction takes place (Santana et al., 2018). In this
sense, mullets are potential model species for studying life-history traits because of their
complex migratory behavior, wide commercial importance, and a high degree of sympatry
(Ibáñez et al., 2022; Mai et al., 2018; Morado et al., 2021; Whitfield et al., 2012).

Fish otoliths, hard calcified structures located in their inner ear, have been widely
used by scientists due to their capacity to store information about a fish’s life history
(Campana, 2005; Miller et al., 2010; Schulz-Mirbach et al., 2019; de Queiroz et al., 2018).
As the fish grows, the otolith incorporates calcium and other elements, a process that is
usually controlled by environmental variation (Morales-Nin, 2000). As such, otoliths are
very useful in disentangling life-history traits such as age, growth and allometric patterns
(Bervian et al., 2007; Jakes-Cota et al., 2021; Medeiros et al., 2021; Xieu et al., 2021).
For example, Medeiros et al. (2021) described polyphasic allometric growth patterns in
otoliths of snook (genus Centropomus), finding that changes in allometric growth rates
are associated with critical events in their life cycle, such as age at maturity and sex
change. Such findings highlight a potential new, cost-effective, and practical tool for
evaluating critical aspects of fish life histories, potentially providing important baseline
information for management purposes. However, it is mandatory that such methodology
undergoes species-specific testing.
For estuarine-dependent species such as mullets, spending less time in estuaries in
the early years of their life may be related to faster growth rates, with faster-growing
species being able to migrate earlier because of reduced size-selective mortality risks
(Able, 2005; Ray, 2005). According to life-history theory, such fast-growing species may
reach sexual maturity earlier, but also attain smaller maximum sizes (Thorson et al., 2014,
2017). In this study, we aim to provide growth parameters based on length-at-age
relationships of three exploited tropical mullet species (Mugil curema – white mullet, Mugil
liza – lebranche mullet, Mugil rubrioculus – redeye mullet) to aid management of such
poorly studied resources. In addition, we integrated age and growth information with
polyphasic otolith allometry and reproduction to address the following hypotheses: (1)
otolith polyphasic allometry can accurately predict age at maturation; and (2) the studied
species exhibit a gradient in life-history parameters according to life-history theory.
Specifically, we hypothesize that the faster-growing and smaller species will exhibit earlier
maturation and change allometric growth patterns at younger ages, while the slowestgrowing species will exhibit late maturation and allometric changes. In addition, crucial

population parameters are provided for the first time for the extremely under-studied mullet
M. rubrioculus.

Materials and methods

2.1

Study area and sample collection
Sampling activities were carried out in two tropical Southwestern Atlantic estuaries;

Mundaú Lagoon, (9° 380 15′′ S 35° 460 20′′ W) and the estuary of the Santo Antônio river
(9º24’50”S e 35º30’24”W), Alagoas, Brazil (Figure 1). These areas exhibit a semi-humid
tropical climate, with rainy periods from March to August (rainfall 242.9 - 94.2 mm) and
dry periods between September and February (100.7 - 63.9 mm). Rainfall (in mm) was
recorded monthly based on data from the Brazilian National Weather Institute.

Figure 1. Map of the sampling locations in the tropical Southwestern Atlantic: Mundau
Lagoon (lower panel), and Santo Antonio River (upper panel).

Monthly samples were obtained for one year for the three species: white mullet in
2009-2010; lebranche mullet in 2011-2012, and redeye mullet in 2018. Different fishing
gear (e.g., gillnets, trawl, longline, casting nets, and hand line) was used to obtain
representative samples in terms of size composition, as certain gears tend to select
individuals of different sizes. Individuals were then taken to the laboratory, identified
following dichotomic keys by Menezes et al. (2015), and processed according to standard
fish sample processing procedures. Each individual was measured (total length (TL in cm)
and

individual

gonad

developmental

stages

were

assigned

macroscopic

examination. Gonad developmental stages were defined as immature, developing virgin,
mature, post-spawning and spent or resting (Vazzoler, 1996). Next, the otoliths were
removed and washed with distilled water and a 2% sodium hydroxide solution. In addition,
to visualize growth rings, the otoliths were decalcified by submersion in a 4% xylene
solution and read while submersed in a 70% ethanol solution. Each otolith was
photographed with a digital camera attached to a stereoscopic microscope and had its
radius (distance from the nucleus to the rostrum) measured with the aid of the ImageJ
software (Schneider et al., 2012).

2.2

Otolith polyphasic allometric patterns

The first step in fitting poly or multiphasic growth models is to validate the assumption
of non-linear growth patterns, which would take form of a non-random residual distribution
in a linear fit of the data (Bervian et al., 2006). For that, the relationship between otolith
radius (OR) and total length (TL) for the three species were analyzed by fitting the Huxley
(1950) power equation. The standardized residuals of the fitted power equation were
plotted against the explanatory variable (OR) and checked for non-random patterns by a
normality test. A non-normal residual distribution implies that the fitted model fails in
explaining a considerable amount of variation in the data.
Once non-linear growth patterns were identified, several power regressions with
invariant intercepts (a) for data grouped into size classes of 5 mm were fitted to extract
allometric coefficients (bsc, i.e. the b parameter in the Huxley power equation). These
allometric coefficients were plotted against the explanatory variable (OR) and a third-

degree polynomial model was fitted for the relationship between fish total length and
allometric coefficients (bsc) (Bervian et al. 2006). To determine the rate of change of the
allometric coefficients as the fish grows, the polynomial models were differentiated for
their first derivatives. Then, the inflection points for the polynomial fits (i.e. stanza changing
points (SCP) – when the rate of change for the allometric coefficient is equal to zero were
determined by plotting the first derivatives against OR observations. Finally, the SCPs
were transformed into predicted ages according to the best-fit growth model.

2.3

Otolith macrostructure and age determination

After decalcification with a 5% xylol solution, whole otolith ring demarcation patterns
were evaluated by quantitative methods to ensure robust growth ring identification and to
detect potential false marks. Quantitative evaluation was based on the distance from the
otolith core to each mark called, the radius of each ring. Each radii were evaluated for
conformation with a normal distribution (Shapiro-Wilk's test) and to check if the mean
radius of each mark decreased with increasing otolith size, under the assumption that the
growth rate decreases as the fish grows. A particular mark was considered false (and not
considered in further age estimation) if it did not follow these criteria.
After eliminating ‘false’ rings, otolith growth increments were identified by two
researchers in an independent, double-blind process (no prior knowledge of individual fish
morphometric characteristics that could bias age determination, as well as no knowledge
of which age the paired researcher attributed to the fish) (Jakes-Cota et al., 2021). The
otoliths were read under transmitted light at 10x magnification. Then, reading accuracy
was assessed by the coefficient of variation (CV) with a threshold of 10% (Allman et al.,
2014; Chang, 2011). To confirm the annual formation of growth rings, we utilized the
Marginal Increment Ratio (MIR) (Fabré & Saint-Paul, 1998), defined by the following
equation:

𝑀𝐼𝑅(%) =

𝑅𝑡 − 𝑅𝑛
∗ 100
𝑅𝑛 − 𝑅𝑛−1

where Rt is the otolith radius, Rn is the distance from the nucleus to the last growth ring,
and Rn-1 is the distance from the nucleus to the penultimate growth ring. We applied a
one-way analysis of variance (ANOVA) followed by the Tukey post-hoc test to check for
significant differences in the MIR between months, showing the periodicity of ring
formation. The month with significantly smaller MIR, as determined by a post-hoc Tukey
test, was considered as the month of ring formation.
Otolith macrostructures are the result of alternating periods of faster and slower growth
rates which are, in turn, a consequence of seasonal growth that is usually driven by
variations in environmental parameters. To investigate if seasonal tropical rainfall and fish
condition are related to fish growth, a generalized linear model (GLM) was used. MIR, the
response variable, was used as an indicator of seasonal growth rate (Fabré and SaintPaul, 1998; Hauser et al, 2018) and used as response variable, while condition factor and
monthly rainfall (mm) were considered explanatory. Here, condition factor was defined as
the ratio between the observed and predicted length, as defined by the previously fitted
least-squares length-weight relationships (Froese, 2006). Model assumptions such as
residual normality and homogeneity of variances were previously verified before accepting
test results.
A total of 953 otoliths (364 for M. curema, 380 for M. liza and 209 for M. rubrioculus)
were processed for age estimation (size ranges were 5 – 42.5 cm for the white mullet,
11.5 – 75 cm for lebranche mullet, and 8 – 39 cm for redeye mullet). Sagittal otoliths of
the three species after decalcification were characterized by a very dense opaque core,
followed by a large hyaline band and subsequently alternating growth rings. Following the
quantitative criteria of decreasing between-ring distances and unimodal fitting, the first
two rings were not considered to be annuli for all species (Figure 2).

Figure 2. Sagitta otoliths from Mugil liza, M. curema and M. rubrioculus and their annual
growth rings.

2.4

Growth rate and asymptotic size

We utilized the back calculation method to estimate fish length at previous ages
through correspondent growth ring measurements towards improving the accuracy of
length-at-age data. This is based on the relationship between otolith size and fish size,
using the radius of each growth ring as a proxy to calculate fish size at its respective age
(Morat et al., 2020). We used the back-calculation model from Morita & Matsuishi (2011),
which uses the following multiple regression model:

𝑇𝐿 = 𝛼 + 𝛽 ∗ +𝛾 ∗ 𝐴𝑔𝑒
where 𝛼 is the intercept, 𝛽 is the coefficient of variation for OR (otolith radius), and 𝛾 is
the coefficient of variation for fish age.
Then, the coefficients of the best-fit model are applied to the following equation:

−𝛼
𝑇𝐿𝑡 =
+
𝛽

(𝑇𝐿𝑐 +

𝛼 𝛾
+ ∗ 𝑡) ∗
𝛽 𝛽
𝑐

𝑡

−

𝛾
∗𝑡
𝛽

where TLt is the length at age t, TLc is the length at capture, ORt is the otolith radius at
age t, ORc is the otolith radius at capture, and 𝛼 , 𝛽 and 𝛾 are the coefficients obtained
by the multiple regression analysis.
Length-at-age data (observed and back-calculated) were utilized as input to estimate
the growth parameters of the three species by fitting the von Bertalanffy growth model
(VBGM) in the R package “FSA” (Ogle et al., 2021). It utilizes non-linear least-squares
regression analysis to search for optimal parameters such as k, L∞ and t0 and their
respective standard errors. The following equation define the VBGM:

𝐿𝑡 = 𝐿∞ (1 − 𝑒 −𝑘(𝑡−𝑡0 ) )
where Lt is the length at age t, L∞ is the asymptotic size, k is the growth rate and t0 is the
theoretical age when length is set to zero, i.e., the x-intercept.

2.5

Hypothesis testing

To test if otolith allometry can be used to accurately describe important life history
events in the three species, we first converted the SCPs to relative age according to the
best-fit von Bertalanffy growth model. We then utilized the R package “sizeMat” to
calculate the age at first maturity (A50) using the data on individual gonad developmental
levels for each species. Then, we verified if the A50 95% confidence intervals overlap with
any SCP. We also analyzed the 95% posterior distributions of growth parameters k and
L∞ and compared them between species. All statistical analyses were carried out with
predefined, fixed seed values to allow for reproducible results in the R software version
4.1.2.

Results
Lebranche mullet had the highest mean (31.41 ± 19.2 cm) and maximum total length

(75 cm), followed by white (28.5 ± 7.67 and 45 cm) and redeye mullet (27.08 ± 6.19 and
39.6 cm) (Figure 3). Age estimates ranged from 0 to 9 years for white mullet (only 4.78%
or error between readers), 2 to 8 years for lebranche mullet (6.37% error) and 1 to 10
years for redeye mullet (5.43% error).

The monthly marginal increment ratio (MIR%) variation confirmed that one annulus is
formed per year for each species. The smallest MIR values indicated that the hyaline zone
was formed in the month of February for both lebranche and white mullet (Tukey post-hoc
pairwise test, p < 0.0001 and p = 0.031, respectively). For the redeye mullet, ring
formation appears to take place in August (Tukey post-hoc pairwise test, p = 0.028)
(Figure 4). Generalized linear models indicated that the relative condition factor and
monthly rainfall are closely related to annuli formation. More specifically, we detected
significant positive influence of rainfall on the marginal increment ratio of lebranche and
white mullets. Condition factor was also positively related to the MIR for the white and
redeye mullets (Table 1).

Table 1. Output of the generalized linear models (GLMs) for the influence of rainfall and
condition factor on the annuli formation (IMR) for the three species
Specie

Effect

Estimate

Lebranche
mullet

Condition
factor
Rainfall
Condition
factor
Rainfall
Condition
factor
Rainfall

White mullet

Redeye mullet

t value

p value

-0.160

Standard
error
0.136

-1.178

0.24

0.00024
13.83

0.000115
5.115

2.098
10.4

0.0373*
0.005*

0.022
0.731

4.884
0.360

2.832
2.031

0.042*
0.043*

0.00019

0.053

0.004

0.99

Figure 3. Size structures for the lebranche mullet M. liza, white mullet M. curema, and
redeye mullet M. rubrioculus caught in the study locations.

According to the non-random residual distributions, the OR / TL relationship for all
three species showed polyphasic allometric growth (p < 0.001). As demonstrated by the
polynomial fit, there was significant variation of the allometric coefficient with increasing
otolith radius. Differential equations for the polynomial models, which denote the rate of
change for the fitted model as the independent variable changes, indicate two sequential
stanza changing points (SCPs) for the three species. The redeye mullet achieves the
SCPs at smaller ORs, while the lebranche mullet achieves it at larger ORs (Figure 5).
According to the length-at-age plots, the first SCPs take place at around one year of age
for all three species. However, the redeye mullet had the earliest (about 0.8 years),
followed by white (0.95 years) and lebranche mullets (1.3 years). Similarly, despite

occurring at roughly 3 years of age for the three species, the second SCP also exhibited
a similar gradient: approximately 2.7 for the redeye mullet, 3.1 for the white mullet, and
3.5 years for the lebranche mullet. According to the macroscopic gonadal maturation
models, the second SCP for the three species greatly overlapped with the age at
maturation, hence confirming our 1st hypothesis (Figure 6).
Not surprisingly, fitted growth parameters also show the same gradient pattern found
for the SCPs: the lebranche mullet was the slowest-growing (k = 0.21) and had the
greatest asymptotic length (L = 70.37), the redeye mullet was the fastest-growing (k =
0.31) and exhibited the smallest asymptotic length (L = 36.38), and the white mullet
exhibited intermediary growth parameters (k = 0.25, L = 39.45). The growth curves of the
three species were similar, but 95% confidence intervals did not overlap (Table 2 and
Figure 6).

Figure 4. Monthly marginal relative increment (MRI %) for the lebranche mullet M. liza,
white mullet M. curema, and redeye mullet M. rubrioculus caught in the study locations. A
posteriori multiple comparisons indicate significant differences in the month of February
for the lebranche and white mullets, and in August for the redeye mullet.

Figure 5. From top to bottom, for the lebranche mullet M. liza, white mullet M. curema,
and redeye mullet M. rubrioculus: relationship between otolith radius (OR)- mm) and total
length (TL), standardized residuals of the power regression between OR and TL,
polynomial fit of the relationship between OR and the allometric coefficient (b), and
relationship between the derivative of the polynomial model (b’) and OR.

100

Figure 6. Length-at-age plots, von Bertalanffy growth curves fitted to back-calculated
lengths, age-converted SCPs from the polyphasic growth models and 95% confidence
intervals for the age at maturity (A50) for the three studied species. Note the different yaxis scales because of significant size differences between lebranche mullet and the other
species.

101

Table 2. Life history parameters and 95% confidence intervals obtained for the studied
species. A50 = age at first maturity, A95 = longevity, L50 = size at first maturity, L∞ = von
Bertalanffy asymptotic length, k = von Bertalanffy growth rate.
Lebranche mullet
A50 (Years) 3.4 (3.2 – 3.5)
A95 (Years) 14 (13 – 15)
L50 (cm)
42.5
L∞ (cm)
70.37 (67.33 –
74.1)
t0
-0.26 (-0.21 – 0.29)
k
0.21 (0.19 – 0.22)

White mullet
3.1 (2.9 – 3.3)
13 (11.5 – 14)
28.4
39.45 (38.05 – 41.17)

Redeye mullet
2.5 (2.2 – 2.6)
10 (9 – 11)
24.6
36.38 (35.73 – 37.1)

-1.72 (-1.69 – -1.75)

-0.3 (0.27 – 0.33)

0.25 (0.23 – 0.28)

0.31 (0.29 – 0.33)

Discussion
This study is the first to combine data on age, growth, maturity, and polyphasic

allometric growth patterns. We also provide annuli validation and growth parameters for
three highly exploited mullet species, especially for the data-poor redeye mullet. On
joining data on age, growth and reproduction with allometry, we demonstrate that
polyphasic otolith allometric variation can be a powerful tool to understanding variation in
life-history traits in exploited fish, as well as providing insights on important events in their
life cycle such as age at migration and maturation. In addition, our results show significant
variation in life-history traits among species that follow the expected ecological theory
predictions, as stated in our second hypothesis: the fastest-growing species reached the
smallest asymptotic sizes and exhibited earlier changes in allometry and maturation, and
the slowest-growing showed larger sizes and later changes in allometric patterns and
maturity. Multiple implications for management of such data-poor species can be drawn
from our results, such as the use of the new parameters in further population and
ecosystem models, and the potential use of otolith allometric variation as a cost-effective
tool for untangling important species traits.

4.1. Fine-scale variation in life-history explained by otolith allometry, age and growth

102

Our results indicate that the fastest-growing species (redeye mullet) changes its
allometric growth patterns earlier (around 0.8 years), followed by the white mullet (at
roughly 0.95 years) and the lebranche mullet, the slowest-growing, at 1.3 years of age.
The second change in allometry for the three species highly overlapped with ages at
maturity (Figure 6). Such results can be considered evidence that polyphasic allometric
growth in fish otoliths can be a suitable indirect indicator of crucial life cycle events such
as sexual maturation and ontogenetic habitat shifts. The same has been observed in
protrandic hermaphroditic fish, where sex changes are reflected in allometric shifts
(Bervian et al., 2006.; Carvalho et al., 2015; Hashiguti et al., 2019; Medeiros et al., 2021).
We also show that sympatric Mugil species may have temporally asynchronous life cycles
to allow coexistence and, more generally, show how life-history traits can vary among
congeneric, sympatric species. This asynchrony is likely to be an evolutionary response
that increases fitness of ecologically similar co-occurring species exposed to roughly the
same environmental conditions (Chang and Iizuka, 2012; Scott and Johnson, 2010).
As mullets exhibit complex, estuarine-dependent life cycles that are largely
constrained by local factors (da Silva et al., 2018), it is to be expected that their growth
pattern shows a substantial amount of geographical variation (Hegarty et al., 2022). We
verified that otolith allometric growth patterns of the studied species appear to show
disparities that possibly reflect time-sensitive dynamics of their first year in estuarine
nursery habitats. The fastest-growing species (redeye mullet) showed the first allometric
growth stanza (SCP1) earlier, followed by the white mullet and the lebranche mullet, the
slowest-growing. Understanding which cyclic biological process would cause changes in
allometric growth in the juvenile phase is warranted.
Santana et al. (2018), when analyzing otolith microchemistry for the white mullet,
suggests that this species appears to remain in the estuary after recruitment, until
reaching around one year of age. Avigliano et al. (2020) evaluated the estuarine
dependence of white mullet in the Santo Antônio River and found that 81.5% of individuals
have an otolith microchemical profile that corresponds to marine-estuarine opportunistic
habits. In explanation, these authors highlight the high mobility of juveniles between
coastal habitats such as mangroves and lagoons. Therefore, it is worth speculating that

103

the SCPs showed in our results register the first migration from the estuary to the sea.
Such movements between the different seascape habitats in the first year of life are also
potentially recorded in otoliths as non-annual macrostructures. These are discarded in
age estimates (see materials and methods and Figure 2) and might be related to
physiological stress. Similar conclusions were reached by Hsu and Tzeng (2009) and
Chang et al., (2000), who found multiple concentric rings around the core region of the
otolith before the first annulus in Mugil cephalus. They suggest that the possible causes
of these ‘false rings’ could be ontogenetic events, such as metamorphosis from larval to
juvenile stage and abrupt changes in environmental factors (Chang et al. 2000).
The life cycle of tropical estuarine-dependent fish species is heavily influenced by the
marked seasonality in rainfall of these regions (da Silva et al., 2021, 2022; Macedo et al.,
2021). The tropical rainy season is a crucial driver of increased biological productivity (de
Barros et al., 2022), which may affect key physiological processes such as seasonally
varying growth rates and deposition of calcium carbonate in otoliths (Efitre et al., 2016;
Gabriela et al., 2021). Relationships between biological metrics and rainfall were also
observed in this study, where ring formation of the lebranche and white mullets appeared
to be strongly influenced by the monthly precipitation. Similarly, Basilone et al. (2020) also
detected an association of the marginal relative increment in fish otoliths with body
condition index, which was true in this study for the white and redeye mullets. Such
relationship could indicate an indirect effect of seasonal spawning activity on annuli
formation, which can be associated with the physiological stress and intense energy
during spawning activity, momentarily reducing the fish condition (Andrade et al., 2013).
Other than rainfall and spawning, other factors such as temperature can also influence
annuli deposition even in tropical fish (Cappo et al., 2000; Caldow and Wellington, 2003).
In this sense, asynchronism in ring formation between some of the studied species may
be a result niche partitioning to reduce interspecific competition related to reproduction or
resource acquisition, as has been observed in other sympatric fish (Fakoya and Anetekha,
2019; Simon et al., 2012). Also, considering that the redeye and white mullets are
phylogenetically closer (Neves et al., 2020), it is to be expected that they should also

104

exhibit higher degrees of niche overlap and therefore need to evolve temporally decoupled
life cycles.
The second change point in allometry (SCP2) highly overlaps with ages at maturity in
the three studied species. For the lebranche and white mullets, several studies have
shown that sexual maturity is reached at sea, where spawning events take place (Moore,
1974, Santana et al., 2018, Mai, 2019, Ibáñez et al., 2012, 2016; Ibañez and GallardoCabello, 1996). In our study, the three species exhibited the second stanza around the
third year of life. In addition, they coincided with the change in annual growth rate as
shown by switching annuli patterns in the otoliths (wider rings for thinner rings) and the
occurrence of double marking (false double ring). Ibañez (2016) described similar age
patterns in mugilids to those found in our work.

4.2. Age and growth
The estimated growth parameters for the lebranche and white mullets all lie well within
the expected range observed by other similar studies (Table 7). Generally, the literature
shows that the lebranche mullet is consistently slower-growing and attains larger
maximum sizes, as well as a higher longevity (Alvarez-Lajonchere, 1981; Garbin et al.,
2014). However, it should be stated that larger, older individuals were possibly missed by
our sampling gears, with the maximum observed age for the lebranche mullet in our study
being of only 7 years. As such, despite being considerably similar to other studies (Table
7), the growth parameters for this species, especially the asymptotic length, should be
considered with caution. Thus, further work in the region might be needed to advance
biological knowledge and address possible uncertainties on population parameters of
lebranche mullet. Parameters for the white mullet show that this species grows faster, but
still attains considerably old ages (maximum observed age of up to 11 years in Santana
et al., 2009), with a reasonably good fit to the data (Figure 6). Despite being an important
component of many regional fisheries (in situ observations) previous studies on the
redeye mullet are only limited to genetics (Nirchio et al., 2007; Neves et al., 2020),
parasitism (Cardim et al, 2018), and length-weight relationships (da Silva et al., 2017).
Accordingly, this is the first study to report age-length relationships and growth parameters

105

according to the von Bertalanffy equation for this species. Our results demonstrate that
the redeye mullet is fast-growing relative to the other mullet species in this study, which is
sustained even until after maturation. The VBGF model also provided a satisfactory fit,
with the curve clearly reaching an asymptote (Figure 6).
Although the parameters in this study are considerably similar to estimations in
previous studies, there is still a notable amount of variation (Table 7). This may be
because mullets exhibit complex, estuarine-dependent life cycles that are largely
constrained by local factors. Therefore, it is reasonable to expect that their growth patterns
show a substantial amount of geographical variation in response to local environmental
variability (Hegarty et al., 2022).

Table 3. von Bertalanffy growth parameters for each studied species gathered from the
literature
Study

Location

Species

L∞

Present study

Tropical
Southwestern
Atlantic
Cuba

Lebranche
mullet

70.37

0.21

Lebranche
mullet

88.8

0.11

25 - 37

Temperate
Southwestern
Atlantic
Temperate
Southwestern
Atlantic
Subtropical
Southwstern
Atlantic
Tropical
Southwestern
Atlantic
Tropical
Southwestern
Atlantic
Southwestern

Lebranche
mullet

56.8

0.30

13 – 54

Lebranche
mullet

66.2

0.168

24 – 65

Lebranche
mullet

50.4

28–81

White
mullet

39.45

0.25

4.9 – 45

White
mullet

34.4

0.36

1.3-39.5*

White

40.3

0.161

18-41

AlvarezLajonchere
(1981)
Castro (2009)

Garbin et al.
(2014)
Giombelli-daSilva et al
(2021)
Present study

Santana et al.
(2009)
Ibáñez-Aguirre

Size
Maximum
range
observed
(cm)
age
7 -75
8

1.10

106

& GallardoCabello,
(1996)
GallardoCabelo et al
(2005)
Giombelli-da
Silva & Vazdos-Santos
(2019)

Gulf of Mexico

mullet

Subtropical
Pacific, Mexico

White
mullet

36.4

0.21

7-32

Tropical
Southeastern
Atlantic

White
mullet

47.3

0.34

0.2-42.2

4.3. Implications for fisheries management
Mugilids are important fisheries resources along the Southwestern Atlantic, being
usually exploited by large artisanal and semi-artisanal fleets for local commercialization
(González-Castro et al., 2009; Garbin et al., 2014). However, coordinated efforts for
assessing and managing such fisheries are considerably scarce, being only available for
the Southern and Southeastern regions of Brazil (Miranda et al., 2006; MPA and MMA,
2015). Still, formal reports on mullet fisheries remain largely inconclusive regarding their
exploitation status, as well as on the most appropriate management strategy that should
take place. In great part, this is due to the lack of appropriate data concerning population
structure and dynamics, which prevents the use of established models to inform suitable,
evidence-based management targets (ICMBIO, 2007; Garbin et al., 2014). However, such
information must be considered of urgent priority to acquire for all exploited stocks, as
mullets in the tropical Southwestern Atlantic have showed signs of overexploitation
(Mendonça and Bonfante, 2011; Aguirre-Pabon et al., 2022), and their estuarinedependent life cycles makes them considerably exposed to anthropogenic-related
changes in environmental health (Whitfield and Cowley, 2010).
Despite being able to inform patterns of relative vulnerability to exploitation,
information on age and growth is only the first step for conducting evidence-based
fisheries management (Goethel et al., 2022). Next steps on assessing mullet stocks in the
tropical Southwestern Atlantic must include acquisitions of catch and effort time-series, as
well as estimates of mortality using the parameters estimated in this study as input.
Importantly, any management advice and its implementation should follow bottom-up,

107

participatory guidelines to ensure compliance and that local needs of communities are
met (Mendonça and Bonfante, 2011; Batista et al., 2014). We also demonstrate in this
study that examining allometric variation in fish otoliths can give important insights into
crucial life cycle events, such as age at migration to the sea and sexual maturation for the
studied species. Consequently, such methods can be utilized as potential indicators for
life stages and size classes that are important for population persistence and stock
maintenance and should be protected.

Conclusion
This study provided important insights about crucial life-history traits and their

relationships with allometric growth patterns and life cycle of the widespread, sympatric,
and congeneric mullets M. liza, M. curema and M. rubrioculus. More specifically, through
crossing information on otolith allometric variation, age and growth, and reproduction, we
added evidence that otolith allometric growth patterns traits may be important predictors
of major life cycle events, as well as providing insights into ecological consequences of
coexistence. Importantly, this study also provided important parameters for future
assessment of stock status and ecological modelling, which may be needed in face of
potential threats of overexploitation for such crucial fisheries.

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 – (#441657/20168), FAPEAL - Research Support Foundation of the State of Alagoas (#60030.1564/2016)
and by Coordination for the Improvement of Higher Education Personnel CAPES-Brazil
CAPES (#23038.000452/2017-16). We are thankful to CNPq for the research grant to
N.N.F., (#306624/2014-1), all fishermen who helped in the field work, and to all members
of the Fish and Fisheries Ecology Laboratory and the Conservation and Management of

108

Natural Resources Laboratory. Thanks to Francisco Santana for insights into age reading
and Naércio Menezes for species identification.

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5. INDIVIDUAL AND INTERSPECIFIC PLASTICITY IN THE LIFE HISTORY OF THREE
SYMPATRIC MUGIL SPECIES IN TROPICAL ENVIRONMENTS: IMPLICATIONS FOR
MANAGEMENT AND CONSERVATION.
Jordana Rangely*1,2, Matheus S. F. de Barros3,4, Cicero Diogo Oliveira1, Jessika M.
M. Neves1, Fabrice Duponchelle5, Nathan Miller7, Nidia Noemi Fabré1
1Laboratório

de Ecologia, Peixes e Pesca (LaEPP) da Universidade Federal de

AL, USA
4Shelby Center for Ecosystem-Based Fisheries Management, Dauphin Island Sea

Lab, Dauphin Island, AL 36528
5Institut

de Recherche pour le Développement (IRD), Unité Mixte de Recherche

Biologie des Organismes et Ecosystèmes Aquatiques (UMR BOREA - MNHN, CNRS7208, SU, UCN, UA, IRD_207), Avenue Agropolis, 911, 34394 Montpellier, France.
7 Quadrupole ICP-MS Laboratory. The University of Texas at Austin.

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Abstract
Understanding the causes and consequences of plasticity is crucial for studies of animal
behavior and physiology, especially in exploited populations affected by size-selective
fishing. Estuaries, with their fluctuating abiotic conditions, challenge fish to exhibit flexible
behavioral responses. This study focuses on the Mugilidae family, exploring individual and
intraspecific plasticity in estuarine dependence among Mugil curema, Mugil liza, and Mugil
rubrioculus. We hypothesize that greater estuarine dependence corresponds to reduced
individual variability in habitat use strategies. Using otolith microchemistry to assess fish
migration patterns and connectivity among coastal, marine, and estuarine environments,
we sampled across four tropical estuaries along 170 kilometers of the Atlantic coast. Our
analyses of Sr and Ba ratios revealed significant differences in habitat use among species.
Mugil liza demonstrated a strong preference for estuarine habitats, while M. curema
exhibited higher plasticity across habitats, occupying both marine and freshwater
environments. M. rubrioculus preferred saltier waters but showed variability in habitat use.
Our findings indicate that individual plasticity correlates with lower estuarine dependence,
reflecting evolutionary habitat selection processes. This mechanism may be contributing
to the coexistence of the three species in sympatry. These results underscore the
importance of recognizing individual and species-specific habitat use in fisheries
management and conservation, particularly in the context of partial migration and the
impacts of global warming.
Keywords: sympatry, estuarine-dependent, life cycle, partial migration, microchemistry.

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Introduction

Plasticity in terms of ecology is the ability of an individual to adjust their behavior in
response to changes in the environment in which they are inserted (Dingemanse et al.,
2010). Variation in individual plasticity can have different causes, such as overfishing and
sexual maturity size, and when it is persistent over time it can have important evolutionary
implications for the persistence of populations in environments that are undergoing
change (Nussey et al., 2007; Stamps, 2016). Understanding the causes and
consequences of plasticity is fundamental in studies of animal behavior and physiology
and it is urgent for exploited populations, where size-selective fishing can induce changes
in life history traits (Wilson, et al. al 2019). This need is due to the fact that an organism's
ability to respond adaptively to environmental changes is a strategy to mitigate the effects
of variations in the environment, maximizing its fitness (Fawcett & Frankenhuis, 2015;
Polverino et al., 2019, Urszan et al., 2018). Another way to maximize the fitness of
individuals, increasing foraging opportunities, is migration. This behavior establishes
connectivity between habitats that are used throughout the life cycle and can occur at
different spatial scales (Bauer & Hoye, 2014).
The concept of migratory species has evolved from the traditional view of obligatory
long-distance movements to a more flexible one that includes a gradient of behaviors
ranging from complete residence to full migration, depending on various habitats and
spatial scales (McDowall, 2001, Chapman et al., 2012). This intraspecific variation, known
as partial migration, is widespread across the animal kingdom, particularly in fish, where
individuals adapt their migratory behavior based on ecological factors and phenotypic
differences (Jonsson & Jonsson 1993, Newton 2008; Chapman et al. 2011). Partial
migration has significant ecological and evolutionary implications. Ecologically, it
contributes to variations in organism abundance, nutrient flows, and ecosystem dynamics,
while also influencing the stability of ecosystems (Swanson et al., 2010, Swanson & Kidd,
2010). Evolutionarily, partial migration creates different adaptive landscapes for migrants
and residents, leading to varying selection pressures (Chapman et al. 2012). In fish,
tropical coastal habitats are ideal for promoting this type of migration, as they offer a

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diverse range of resources and favorable conditions at different periods of the life cycle
(da Silva et al. 2018, 2021).
For estuarine-dependent fish behavioral plasticity plays a crucial role in the survival
and ecological success of these organisms in highly dynamic environments (Mery &
Burns, 2010; Ray, 2005). Mainly for juveniles, this behavioral plasticity is essential, as by
moving between different coastal environments and micro-habitats within estuaries,
juveniles are able to exploit temporarily abundant food resources, avoiding unfavorable
areas due to seasonal events or sudden changes in water conditions. tides. This
adaptability not only increases their chances of survival, optimizing the use of temporary
habitats, but also directly influences their growth and development, impacting the rate of
recruitment into the adult population (Bowen, & Allanson, 1982; Blewett et al. 2022 ).
(Bowen, & Allanson, 1982; Blewett et al. 2022). Thus, the behavioral adaptation of fish in
estuarine environments reflects the complex interaction between ecological and
evolutionary factors that shape their life ecology (Mery & Burns, 2010).
In that regard, the Mugilidae are a good example to verify individual and
intraspecific plasticity as they are very morphologically similar species, which co-occur in
estuarine and tropical coastal marine environments (Rangely et al. 2023, Rangely et al.
2024,). However, despite being obligatory estuarine dependent (Able 2005), since they
spend at least one phase of their life cycle in this environment, they occupy the estuary
differently, with abiotic variables such as salinity and dissolved oxygen playing an
important role in this habitat segregation (Rangely et al. 2024). Recent research has
demonstrated high intraspecific and interspecific variability in migration patterns between
distinct Mugil species (Chang et al., 2004; Chang & Iizuka, 2012; Ibáñez-Aguirre et al.,
2012; Avigliano et al., 2015, Fowler et al., 2015; Fowler et al., 2016). This variation in
estuarine habitat use indicates a more complex migratory behavior than initially predicted
for mullets (Fowler et al., 2016; Mai et al., 2018).
In the first year of life, a change in growth variation occurs in Mugil species and the
reason for this is still unknown (Rangely et al. 2023). Like this, we want to understand the
dynamics of habitat occupancy between different species during the first year of life, a
period in which individuals are more restricted to the estuarine habitat. In this sense, we

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raise the following question: is there individual variability in estuarine dependence for the
species M. curema, M. liza and M. rubrioculus related to the first phase of the life cycle?
Our hypothesis is that: greater estuarine dependence in Mugil species (interspecific
variation) implies less individual variability (intraspecific variation) in the strategies for
using tropical estuarine and coastal habitats. To test this hypothesis we used otolith
microchemistry, a powerful tool that allows high resolution to define migration and habitat
occupancy and consequently individual plasticity (Walther, 2019, Mai et al. 2018, Santana
2018, de Almeida et al. 2024).

Materials and methods
2.1 Study area and sample collection
Sampling activities were carried out in four tropical estuaries of the Atlantic, totaling

170 kilometers, three of which are within the Costa dos Corais Marine Protection Area,
namely: Várzea do Una (08°51'39.8"S 035°07'49.6"W), estuary of the Manguaba river (
09°09'29.39"S 035°17'35.45"W), estuary of the Santo Antônio river (09º24'50”S and
035º30'24”W) and Estuarine

Complex Lagunar Mundaú-Manguaba

- CELMM

(09°42'52.0" S 035°48'13.1"W) Brazil (Figure 1). These areas exhibit a semi-humid
tropical climate, with two well-marked periods, the rainy and the dry. Rainy periods from
March to August (rainfall 242.9 - 94.2 mm) and dry periods between September and
February (100.7 - 63.9 mm) (Calado & Souza, 2003). Rainfall (in mm) was recorded
monthly based on data from the Brazilian National Weather Institute. The average water
temperature of 28.3°C. Várzea do Una is characterized by an estuary with an entrance
approximately 300 meters wide. While the Mangua

ba River estuary is approximately

500 meters at the entrance. The Santo Antônio River estuary has an estuary entrance
that is 300 meters wide. These estuaries have mangrove vegetation on their banks
dominated by Rhizophora mangle, Avicennia schaueriana and Laguncularia racemosa. In
relation to CELMM, sampling was carried out in Lagoa Mundaú, which has a permanent
connection with the sea, and an area of 36 km². (Calado & Souza, 2003, Rangely, 2011).
Between 2017 and 2020, the fish were captured during periodic collections
conducted by researchers from the Fish and Fisheries Ecology Laboratory at the Federal

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University of Alagoas. Using two canoes, the individuals were captured with gillnets
forming a semi-siege. The fishermen approach, join the ends of their nets, and then launch
the nets into the sea. They hit the water with their oars to direct the school of mullet into
the net. Soon after, they retrieve the nets.

2.2

Otolith macrostructure
The sagittae otoliths of the three studied species, M. curema (66), M. liza (21) and M.

rubrioculus (55), were extracted, cleaned with NAOH (2%), rinsed in distilled water to
remove any remaining contaminants, and stored in bottles. The otoliths, on the right side,
of each individual collected were embedded in epox resin, which became solid within 48
hours. The blocks were then cut at the height of the otolith nucleus, each cut with a
thickness of 1 mm, carried out on a Metalographic saw (ISOMET 1000). The sections
were fixed on microscope slides (10 sections per slide). Each section was photographed
and then cleaned in deionized water, in which it was submerged for 10 minutes and
simultaneously an anti-static brush was rubbed.

2.3

Microchemistry of otoliths

Elemental concentrations of Mugil otolith transects were quantified using an Elemental
Scientific NWR193 excimer laser system coupled to an Agilent 7500ce inductively coupled
mass spectrometer at the University of Texas at Austin. The laser system is equipped with
a large format two-volume laser cell with fast washout (<1s), that accommodated all otolith
samples and standards in two separate loadings. Laser ablation parameters were
optimized for sensitivity and signal stability from test scan ablations on representative
unknowns (Table 1). Prior to analysis, otoliths and standards were pre-ablated (4.5 J cm2 fluence, 20Hz, 75µm spot, 75µm/s scan rate) to remove potential surface contamination

(note that some otoliths were coated with epoxy or were unexposed in epoxy below the
plane of the surface). All otolith transects ran from cores to edges. Otolith transects were
bracketed hourly by standard measurements (MACS-3 and NIST 612, measured in
triplicate for 60-s). Oxide production, as monitored during daily tuning on NIST 612,

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averaged 0.38±0.03%. Laser energy densities over the analytical sessions averaged
3.23± 0.03 J cm-2. The quadrupole time-resolved method measured 13 masses using
integration times of 10 ms (43-44Ca, 88Sr), 20 ms (24Mg, 85Rb), and 50 ms (7Li, 63Cu, 66Zn,
137-138Ba).

The sampling period of 0.4552 s corresponds to 94.5 % quadrupole

measurement time, and 11 duty cycles per 25µm spot. Time-resolved intensities were
converted to concentration (ppm) equivalents using Iolite software (Univ. Melbourne,
Hellstrom et al., 2008), with 43Ca as the internal standard and a Ca index value of 38.3
weight %. Baselines were determined from 30-s gas blank intervals measured while the
laser was off and all masses were scanned by the quadrupole. USGS MACS-3 was used
as the primary reference standard and accuracy and precision were proxied from
replicates of NIST 612 analyzed as an unknown. Iron (57Fe) analyses in high-Ca materials
are susceptible to Ca- and plasma-related interferences (40Ca17O+, 40Ca16OH+, 40Ar17O+,
40Ar16OH+, 38Ar18OH+), as indicated by high over-recoveries on NIST 612.

Excluding Fe,

NIST 612 analyte recoveries (N=48) were typically within 6% of GeoREM preferred values
(http://georem.mpch-mainz.gwdg.de).

Table 1. LA-ICP-MS Operating Conditions
Laser: ESL NWR193UC

ICP-MS: Agilent 7500ce

Wavelength: 193nm

RF power: 1600W

Pulse width: <4 ns

Cones: Nickel

Ablation cell: Large format 2-volume

Sampling depth: 6mm

He flow: 850 ml/min

Quadrupole parameters

Ar flow: 900 mL/min

Points per mass: 1

Fluence: 3.23±0.03 J/cm2

Integration times for masses:

Repetition Rate: 20 Hz

10ms – 43, 44, 88

Spot size: 25 µm

20ms – 24, 85

Scan rate: 5µm/s

30ms – 55, 57
50ms – 7, 25, 63, 66, 137, 138
Sampling period: 0.45

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Therefore, the habitat use and specific movement patterns of each individual of the
three Mugil species were investigated by ablation along the growth axis of the limestone
structure starting from the transect of the otolith nucleus, passing through annual growth
increments towards to the edge of the otolith (figure 2). Currently there are some studies
that validate relationships between ambient salinity and concentrations of elements in
otoliths for Mugil fish species. So, each individual was classified based on movements
between different salinity environments after the early larval/juvenile stage and before
capture (the edge of the otolith), following Santana and colleagues (2018), work carried
out close to the study area of this research:
Lower limit of the estuarine zone Sr:Ca = 5,0x10-3
Upper limit of the estuarine zone Sr:Ca = 7,4x10-3

2.4

Fish ageing
Growth rings were first evaluated and read in the entire otolith, following Rangely

et al. (2023). After that, the otoliths were sectioned and the growth rings were visualized
along the laser ablation raster with the aid of an under transmitted light magnifying glass,
coupled to a computer with the imaJ program. To this end, each cut was polished with
1.200 and 2.400 sandpaper and aluminum pruning. They were subsequently stained by
leaving them in ethylenediamine tetraacetic acid, (EDTA) 5%, for five minutes, washed in
water and left in toluedine blue 1%, for seven minutes, to facilitate the visualization of the
growth rings. Aging was done along the laser ablation transects, then the age was linked
to otolith chemistry data to visualize variation of elemental concentrations against age.

2.5

Data analysis
To eliminate noise for LA-ICPMS data, Sr:Ca and Ba:Ca ratios were smoothed

using a 9-point moving average. Profiles of these ratios were plotted from the core to the
edge of the otolith together with thresholds of environments (estuary and marine waters)
to interpret migratory strategies. Additionally, the regime shift technique (Rodionov, 2004)

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was used to distinguish zones along a transect profile that are chemically different
between adjacent zones. A new regime shift or otolith zone was created if the mean values
of the two adjacent zones were significantly different using a two-tailed Student t-test (p <
0.01). These zones can be referred to environments or habitats because elemental
concentrations (e.g. Sr and Ba) between environments are significantly different (Vu et
al., 2021a). Kruskal Wallis tests were used to compare means of two independent groups
because Sr:Ca data were not normally distributed.
To understand the intraspecific plasticity in the use of coastal esutarine
environments in the first phase of growth (described by Rangely and collaborators, 2024),
a Generalized Additive Models (GAM) was carried out using the months of the year and
the amount of strontium throughout the first year of growth as variables. life, using R. We
use the residual analysis of the adjusted model and was used as a proxy for individual
plasticity.

Results
Mean strontium and barium concentrations varied significantly among the three

species (figure 1). Strontium concentrations were lowest for M. liza and highest for M.
rubrioculus, with this species presenting higher amplitude values. Mugil curema presented
intermediate values and the lowest amplitude.
Analysis of residuals from the adjusted model from GAM analyzes provides
insights into data variability, being used as a proxy for Mugil individual plasticity over time.
Individuals of M. curema were those that showed greater plasticity of use within
environments. And the individuals of M. liza were those that showed less plasticity of use
in the first stage of the life cycle.

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Figure 1. Means and standard deviations (SD) of Ba/Ca and Sr:Ca (mmol.mol-1); in
otoliths of Mugil liza, M. curema and M. rubrioculus caught in estuaries of northeastern
Brazil. See Appendix for Sr:Ca ratios at the core vs whole transect profile.

Fig 2. interspecific plasticity in relation to the use of coastal environments, in the first phase
of the life cycle (Rangely et al. 2023) GAM residues from the strontium ratio during the
first year of life.

The life profiles among otoliths derived from Sr:Ca proportions showed differences
in habitat use within M. liza, M. curema and M. rubrioculus individually, demonstrating
individual variability regardless of species (Appendix 1). Lifetime transects of Sr:Ca
indicate at least six distinct habitat use patterns, In this way, it was possible to group these
profiles into six different categories of habitat use (figure 3). Consecutive migrations:

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individuals who carry out repeated migrations between different environments throughout
their life cycle. Estuarine resident: individuals who spend all or most of their lives in
estuarine environments. They do not make significant migrations to the sea or freshwater
rivers. Estuary-sea: individuals that begin their life cycle in the estuarine region but migrate
to the sea. Freshwater-sea: These are fish that are born or are in freshwater in their first
days of life, after an initial period in these environments, they migrate to the sea. Sea
resident: individuals who spend their entire lives exclusively in the marine environment,
without making significant migrations to continental or estuarine waters. Sea-estuary: fish
that are born in the marine environment but migrate to the estuary before their first year
of life.
Mugil liza has only three patterns of habitat use, with a preference for estuarine
habitat, making occasional incursions into the marine environment, as in “consecutive
migrations” and “estuary-sea” pattern. It is possible to observe greater variability for the
beginning of life (large amplitude of the confidence interval) in M. liza, mainly for the
estuary-sea category.
Mugil curema has greater plasticity between habitats, with individuals occupying
both marine, freshwater and estuarine environments, being represented in the six
categories of habitat use. In the “freshwater-sea” category it is possible to observe
individuals that were in a freshwater environment at the beginning of their lives, while in
the “sea residents” category the individuals were in marine waters. Within each category
of habitat use, individual variability (amplitude of the confidence interval) was smaller for
this species compared to the other two.
Mugil rubrioculus was represented in five categories, with a preference for saltier
waters. During the beginning of its life, it is almost always in marine environments. As the
individual has more time to live, their choice is always for marine environments, with
individuals up to four years old being present in this environment.

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Figure 3. Variations in Sr:Ca ratios from core to edge of otoliths (birth-to-capture) of M.
curema, M. rubrioculus and M. liza, with colour representing corresponding age along the
ablation path. Red dotted lines are lower (5.0 × 10−3 ) and upper (7.4 × 10−3 ) bounds
of the estuarine zone. See Appendix A for individual plots of Sr:Ca ratios Data from LAICPMS.

The three species had the highest number of individuals in the “consecutive
migrations” category, with around 50% of individuals in this category (figure 3). M. liza is
the species with the largest number of individuals in the “estuarine resident” and also
“estuary-sea” categories. M. curema has the most divided individuals between the
categories, with the “sea-estuary” standing out, after the “consecutive migrations”. M.
rubrioculus is the species that presents the most individuals in the “sea resident” category.

129

Figure 4. Relative frequency of individuals of each species (M. liza, M. curema and M.
rubrioculus) in each of the six habitat use categories.

Discussion
Our results indicate that there is intraspecific and interspecific variability in habitat

occupation strategies throughout the first phase of the mullet life cycle, which may be a
reflection of evolutionary processes of habitat selection. Greater individual plasticity –
greater mobility between estuarine and coastal habitats – related with lower estuarine
dependence. In addition to the spatial differentiation between Mugil species, there is a
temporal differentiation in intraspecific plasticity, the younger the individuals, the greater
the movement between habitats (p < 0.5).
Mugil curema is the species with the greatest diversity in habitat use, being present
in freshwater environments, estuaries and the ocean, in addition to high individual
plasticity, as the same individual can frequently migrate between these habitats. Mugil
rubrioculus also occupies the 3 environments, but this species has a high preference for
saltier waters and individuals migrate less between these environments. M. liza, on the
other hand, prefers to use the estuary, and has low individual plasticity between habitats,
remaining more restricted to the estuarine environment. In this sense, a specific inter and
intra gradient of estuarine-dependence can be described, between the 3 species that co-

130

occur in the tropical estuaries of the region. Which may be important for the fitness and
growth of individuals.
M. liza is the species with the lowest plasticity of use between estuarine and coastal
marine habitats, confirming our hypothesis. However, when observing the large amplitude
in the confidence interval close to the first year of life (figure 3), where the change in
growth speed occurs (Rangely et al. 2023), it can be seen that individuals are migrating
within the same environment demonstrating the adaptation of the species to occupy
microhabitats. Mugil liza, spends more time in its breeding area, reaching greater total
length (Rangely, 2023). At the other extreme, M. rubrioculus is the smallest estuarinedependent species and also the one with the smallest total length (Rangely et al., 2023).
M. curema is capable of occupying marine, estuarine and even freshwater environments
in the first phase of its life cycle.
Avigliano et al. (2021), the present work demonstrated that M. curema has high
plasticity in the use of habitats, which may be related to the species' greater genetic
diversity and its evolutionary time. Mugil liza, on the other hand, has low plasticity and a
preference for the estuarine environment. This species is one of the lineages of the M.
cephalus complex and has diversified more recently (Neves et al., 2020), perhaps for this
reason it presents low habitat use plasticity. M. rubrioculus shows some plasticity but
prefers the marine environment. The phylogenetic status of this species is a little more
complicated, as although some cryptic lineages have been described (Durand & Borsa,
2015; Neves et al. 2020), the monophyly of the species cannot be rejected (Neves et al.,
2020). However, their preference for more saline environments may explain the low
genetic diversity, since Poulin & Leon (2017) argue that freshwater environments
generate more diversity than marine or terrestrial environments since the fragmentation
of habitats promotes greater genetic differentiation.
The capacity for individual plasticity for habitat use and migration patterns appears
to have a genetic and phylogenetic character. It has been demonstrated that Mugil
cephalus presents different migratory patterns according to the microchemistry of the
otoliths (Fortunato et al 2017) and it is already known that the species is composed of
several cryptic lineages (Durand & Borsa, 2015; Neves et al 2020). Avigliano et al (2021)

131

also analyzed the microchemistry of otoliths from individuals from different M. curema
localities and found different patterns of habitat use and migration. Furthermore, it is also
known that M. curema is a species complex composed of several cryptic lineages (Durand
& Borsa, 2015; Neves et al 2020).
Hanahara et al (2023) demonstrated that within the genus Eviota (Gobidae), several
cryptic lineages exhibit spatial segregation and the authors suggest that the lineages
speciated by spatial segregation on a fine scale. Therefore, there appears to be a
correlation between genetic diversity and plasticity in habitat use.
This plasticity in habitat use and estuarine dependence has already been
demonstrated through otolith microchemistry (Albuquerque, et al. 2010, 2012, Condini et
al., 2016, Mai et al. 2019). Chemical heterogeneity within estuaries, due to riverine and
anthropogenic discharges, creates spatial variability between adjacent estuarine and
coastal environments. This heterogeneity affects, spatially and temporally, the biological,
physical and chemical processes of fish, which can be chemically identified in otoliths
(Elsdon & Gillanders, 2005; Elsdon et al., 2008; Walther & Thorrold, 2009). Several
researchers have already demonstrated connectivity between the coastal marine region
and the estuary, indicating a direct relationship between the amount of Sr:Ca in otoliths
and salinity (Santana et al, 2018, Ibáñez et al. 2012, Callicó Fortunato et al. 2017 , Secor
et al. 2001, Zimmerman 2005, Labonne et al. 2009). And it is precisely this heterogeneity
of habitats that allows the coexistence of Mugil species, favoring decoupled in relation to
the pattern of habitat use, with M. curema being influenced by factors such as temperature
and dissolved oxygen, chlorophyll and turbidity, while M. rubrioculus is driven by variations
in salinity (Rangely et al. 2024) and M. liza is mainly influenced by rainfall (Sousa et al.
2015).
It is possible that intraspecific competition, interspecific competition (in the case of
similar species such as Mugil) and predation act in synergy to shape partial migration
patterns (Ward et al., 2004), thus allowing coexistence. Therefore, partial migration is the
temporary reduction of competition with non-migratory species, that is, it can affect the
structure of the community, reducing competition and, therefore, allowing coexistence
(Johnson, 1980).

132

4.1 Management and conservation of species
Our research made it possible to classify these three species that co-occur in tropical
estuaries, in relation to the time of use of the estuaries, throughout the first phase of the
life cycle. And so, it was possible to indicate the priority species for management and
conservation for the estuaries studied as M. liza, as it is the species that spends almost
the entire first phase of its life cycle in this environment. Considering that the longer the
stay in this habitat, the more vulnerable the species becomes. This way, we have a
measure of vulnerability to habitat loss. This is particularly relevant if we consider the
speed of degradation of tropical coastal environments, for the construction of real estate
projects and tourism (Miranda et al., 2002). Therefore, the species with the least plasticity
in habitat use, which migrates least between environments, will have the greatest damage
in relation to the preservation of stocks. Evolutionarily, greater migratory plasticity
between habitats can generate greater adaptability of the species and consequently
greater resilience (Tamario et al. 2019). This is particularly critical for the estuaries
studied, as in 2019 there was one of the largest oil spills in the country's history, one of
the most significant global events in terms of contamination and environmental impact in
recent years, with concentrations of mercury, cadmium, lead and copper above what is
foreseen in Brazilian legislation (Soares et al. 2021).
An important question to consider is how human activities have affected the
dynamics of partial migration and the promotion of the evolution of plasticity (Crispo et al.,
2010). This can be observed both in relation to fishing and in relation to climate change.
For example, the diversity of phenotypes in migratory behaviors that exists within the
same population and among the three Mugil species studied can also lead to differential
survival of individuals due to resilience to fishing pressure. When partial migration occurs,
the stock as a whole, to a certain extent, becomes less vulnerable to fishing activity, for
example, having greater chances of survival, as they have multiple contingents of fish that
use different habitats within the same population (Folwer et al. 2016). And even the
reduction in migratory numbers can have negative consequences for resident fish of the
same species, as was the case with S. confluentus, where remaining populations of this

133

species persisted as small residents isolated in streams, increasing the risk of extinction.
(Nelson et al., 2002, Ryman et al., 1995).
Therefore, understanding partial migration becomes relevant when making
decisions related to stock management (Chapman, 2012). Since, population sustainability
and resistance to disturbance and potentially the recovery capacity of the stock can be
negatively affected by widespread fisheries management, not considering partial
migration and different categories of habitat use (Ruzzante et al. 2006). In the present
work, although the individuals were grouped into six categories of habitat use, all species
present the largest number of individuals in “consecutive migrations”, demonstrating that
partial migration is always a strategy of the Mugilidae.
This understanding is also critical for predicting the effects of climate change and
informing effective conservation strategies in these scenarios (Chessman, 2013; Comte,
Murienne, & Grenouillet, 2014; Sunday, Bates, & Dulvy, 2012). Since global warming can
lead to changes in individual growth rate, which can be important in individual migration
decisions (Skov et al. 2010). Furthermore, temperature influences habitat preference for
species (Matis et al. 2018), and may be an immediate driver that drives partial migration,
which is phenotypically plastic (Skov et al. 2010). As ocean temperatures continue to rise
we expect increasing pressure on species that depend on a particular habitat to survive
while those that utilize a variety of habitats may be considered less vulnerable (Munday,
2004; Pratchett, 2005).

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), FAPEAL - Research Support Foundation of the State of Alagoas
(#60030.1564/2016) and by Coordination for the Improvement of Higher Education
Personnel CAPES-Brazil CAPES (#23038.000452/2017-16). We are thankful to CNPq for
the research grant to N.N.F., (#306624/2014-1), all fishermen who helped in the field work,

134

and to all members of the Fish and Fisheries Ecology Laboratory and the Conservation
and Management of Natural Resources Laboratory. Thanks to Francisco Santana and
Marcia Ferreira de Sousa for insights into age reading and Naércio Menezes for species
identification.

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143

Appendix 1

Figure 1 – Microchemical profiles of otoliths of 52 Mugil curema from the Northeast coast
of Brazil. Red dotted lines are lower (5.0 × 10−3) and upper (7.4 × 10−3) bounds of the
estuarine zone. Data from LA-ICPMS.

144

Figure 2 – Microchemical profiles of otoliths of 49 Mugil rubrioculus from the Northeast
coast of Brazil. Red dotted lines are lower (5.0 × 10−3) and upper (7.4 × 10−3) bounds of
the estuarine zone. Data from LA-ICPMS.

145

Figure 3. Microchemical profiles of otoliths of 12 Mugil liza from the Northeast coast of
Brazil. Red dotted lines are lower (5.0 × 10−3) and upper (7.4 × 10−3) bounds of the
estuarine zone. Data from LA-ICPMS.

146

JOINING

DATA-LIMITED

STOCK

ASSESSMENT

AND

TRADITIONAL

ECOLOGICAL KNOWLEDGE TO INFORM TROPICAL MULLET MANAGEMENT
Jordana Rangely1,2, Matheus de Barros3, José Gilmar Cavalcante de Oliveira Júnior1,
Cicero Diogo de Oliveira1, Jessika M. M. Neves1, Vandick da Silva Batista1, Nidia Noemi
Fabré1
1Laboratório de Ecologia, Peixes e Pesca (LaEPP) da Universidade Federal de Alagoas

(UFAL), Instituto de Ciências Biológicas e da Saúde
2Instituto Federal de Educação, Ciência e Tecnologia de Alagoas (IFAL)
3School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA.

147

Abstract
Small-scale fisheries (SSF) constitute more than half of global fisheries. SSF fishers can
offer vital insights into the life history characteristics of target species. Upholding the
principles of good governance, the combination of conventional scientific knowledge
(CSK) with local ecological knowledge (LEK) is pivotal to ensure the success of SSF
management. In this study, we used CSK and LEK to holistically assess the stocks of
three commercially important mullet species in three estuaries in the Tropical
Southwestern Atlantic, examining how both information sources can contribute to
conservation and management efforts. For CSK, we employed a Bayesian size-based
model to conduct a stock assessment grounded in prior information on life history
parameters. For LEK, we conducted interviews with fishermen, aiming to understand how
they perceive stock status, and which factors affect these resources. Both knowledge
streams indicated significant fishing pressure, suggesting that two of the stocks are
overexploited while one is operating at its maximum sustainable yield. We demonstrate
that LEK and CSK largely agree on mullet stock status but not on the causes of declines,
highlighting the importance of LEK to provide auxiliary information to fisheries
management. Horizontal collaboration is essential in artisanal fisheries, allowing fishers,
managers, and scientists an active voice in decision-making. We also identified strengths,
weaknesses, opportunities, and potential threats to the mullet stocks in the region,
allowing enhanced governance through collaboration among stakeholders and the
scientific community.
Keywords: Artisanal fisheries, Mugil, Co-management, Traditional Ecological Knowledge

148

Introduction
Small-scale fisheries (SSF) play a significant role in global fish landings,

contributing approximately 40% of the world's total marine fisheries catch and employing
a substantial amount of people directly involved in fisheries. According to FAO (2022) and
Kelleher et al. (2012), almost half a billion people worldwide depend at least partially on
SSF. However, due to their dispersed nature and limited funding allocated to agencies
responsible for their management, stocks targeted by SSF are often poorly managed, and
their statuses are frequently unknown (Castello et al. 2009). Consequently, many SSF are
believed to be overexploited and unproductive (Kurien and Willmann, 2009). These issues
highlight the critical need to properly manage SSF to ensure local food security and
conservation. Current approaches to fisheries management incentivize understanding
human interactions with the environment and promoting fishers' participation in data
collection and decision-making processes (Castello et al. 2009).
As opposed to the traditional exclusive reliance on Conventional Scientific
Knowledge (CSK), incorporating Local Ecological Knowledge (LEK) into the management
process is an alternative to transition to a bottom-up management process that aids in
resolving potential disputes between local communities and management needs (Jones
et al., 2010). With their extensive empirical experience, fishers can provide valuable
information on the life history of target species, including size at first maturity, maximum
sizes, habitat use, reproductive seasons, and optimum sizes for capture (Silvano and
Valbo-Jørgensen, 2008, Pereira et al., 2021). Obtaining this data solely through CSK
would require greater sampling efforts and financial resources. Therefore, the inclusion of
LEK not only fosters trust in management measures by incorporating traditional
communities on SSF management but also offers useful and costless information than
assessments by CSK, aiding in identifying historical baselines and establishing restoration
and sustainability for target species (Thornton and Scheer 2012). The integration of CSK
and LEK has proven effective in managing SSF, promoting higher compliance with
management rules, facilitating data collection, and helping understand the social

149

dynamics involved in the system (Pita et al., 2009; Mikalsen and Jentoft, 2008, Lorenzen
et al., 2010).
In the Tropical Southwestern Atlantic, many SSF target estuarine-dependent fishes
of the Mugilidae family, particularly mullets of the genus Mugil. Almost entirely small-scale,
mullet fisheries account for about 20% of all commercial fishing catches in Brazil and
support numerous traditional communities (Garbin et al. 2014; MPA 2011). Despite their
importance, mullets are considered data-deficient by the IUCN. Most mullet fisheries in
Brazil remain unassessed and are consequently unregulated due to the chronic lack of
fisheries statistics and long-term monitoring programs in the country (Santos et al. 2023).
In fact, some stocks are reportedly overfished due to unregulated fishing effort (Mendonça
and Bonfante, 2011, Lan et al., 2017). Current management rules, when in place, are often
ineffective and fail to meet conservation or fishers' needs (Mendonça and Bonfante, 2011).
Without intervention, mullet fishing faces a threat in the near future.
Our study aimed to showcase the integration of Conventional Scientific Knowledge
(CSK) and Local Ecological Knowledge (LEK) as a means to foster promote bottom-up
management on tropical multispecies mullet fisheries in a tropical Southwestern estuary
system in Northeast Brazil. Specifically, we evaluated the stock status of three mullet
species (white mullet Mugil curema, lebranche mullet Mugil liza, and redeye mullet Mugil
rubrioculus) utilizing length-based methods adapted for data-limited stocks. Additionally,
we employed LEK as a complementary method to gather important life-history and fishery
information, as well as to identify the strengths, weaknesses, opportunities, and threats
associated with the studied fisheries.

150

2. Materials and methods

2.1

Sample collection

Sampling was conducted in three estuaries and adjacent marine areas in the
Tropical Southwestern Atlantic: the estuary of the Santo Antônio River (9º24’50” S and
35º30’24” W), the Mundaú Lagoon (9°38’15” S and 35°46’20” W), and the Manguaba
Lagoon in Alagoas, Brazil (Figure 1). These regions experience rainy periods from April
to August (with an average rainfall rate of 165.6 mm) and dry periods between September
to March (with an average rainfall rate of 85.8 mm), characterized by a semi-arid tropical
climate (Nery et al., 1998; Paredes-Trejo et al., 2018).
Monthly length samples (Total Length, cm) were collected over one-year periods
for each species: Mugil curema and Mugil rubrioculus in 2022–2023, and Mugil liza in
2011–2012. We used past length frequency data for M. liza because not enough
individuals were caught in 2022-2023. We therefore caveat that M. liza stock status
reflects the years 2011-2012. Connections of LBB outputs with the fisher’s perceptions
should therefore be made with caution for M. liza. Gillnets made of monofilament nylon
with mesh sizes of 30 and 40 mm (for M. rubriculus and M. curema) and 50 and 60 mm
(for M. liza) were used. These nets were deployed from two canoes, each manned by two
crew members. As the canoes approached each other to close the ends of their nets, the
fishermen launched them into the sea. To direct the school of mullet into the net, fishers
used their oars to strike the water. Following this, the nets were inspected for captured
fish. Interviews with fishers were conducted from December 2022 to March 2023 at the
landing ports for traditional mullet fishing in the Santo Antônio River, Mundaú Lagoon, and
Manguaba Lagoon (Figure 1). Length frequency distributions from these different
estuarine systems were pooled to reflect the assumption that there is a single stock for
the three species

151

.
Figure 1. Sampling locations of mullet in the Tropical Southwestern Atlantic: Santo
Antonio River (upper point) and Mundaú Lagoon (middle point) and Manguaba Lagoon
(lower point), Alagoas state, Brazil.

2.2 Conventional Scientific Knowledge (CSK)
In the field, we measured fish Total Lengths (TL) to the nearest centimenter after
the individuals were identified to the species level using a dichotomous key (Menezes et
al., 2015). A random subsample was then transported to the laboratory, where individual
female gonad development stages were determined through visual examination using a
stereoscopic microscope. The stages were classified as immature (stage I), developing
(stage II), mature (stage III), post-spawning (stage IV), and spent or resting (stage V)
following Vazzoler (1996). To estimate the size at first maturation (L50), the proportion of
young and adult female individuals (gonadal development stages I, II, and III) was

152

calculated based on Vazzoler's (1996) gonadal development stages. All females were
included in the analysis, with stages I and II considered immature and stages III, IV, and
V considered mature. Subsequently, a logistic curve (King, 2007), was fitted to determine
the L50, denoting the length at which 50% of the fish can reproduce.

2.2.1 The length-based Bayesian biomass (LBB) assessment model
The LBB method is grounded in a conceptual model that correlates life-history traits
with length-dependent gear selectivity, illustrating how they interact to generate a specific
length-frequency distribution (Froese et al., 2018; Wang et al., 2020). Trends in size over
time denote elapsed time and are thus utilized to deduce population dynamics, enabling
the model to project relative catch, mortality rates, and reference points for management.
The model relies on life-history ratios rather than absolute values to reduce parameter
demands. Initially, total mortality/growth rates (Z/K) are estimated by estimating the
curvature of the predicted catch for fully selected fish in the numbers-at-age curve,
formulated as follows:

𝐿∞ − 𝐿
𝑁𝐿 = 𝑁𝐿𝑠𝑡𝑎𝑟𝑡 (
)
𝐿∞ − 𝐿𝑠𝑡𝑎𝑟𝑡
In this equation, NL represents the number of fish surviving at length L, NLstart
denotes the number of fish at the starting length (Lstart), where full selection occurs. The
following set of equations is utilized to estimate L∞, selectivity parameters, M/K, F/K, and
proportions-at-length (PLi) as follows:

𝐿∞ − 𝐿𝑖 (𝑀+ 𝐹 𝑆𝐿 )
𝑁𝐿𝑖 = 𝑁𝐿𝑖−1 (
)𝐾 𝐾 𝑖
𝐿∞ − 𝐿𝑖−1
𝐶𝐿𝑖 = 𝑁𝐿𝑖 𝑆𝐿𝑖
𝑆𝐿 =

1
1 + 𝑒 −𝛼(𝐿−𝐿𝑐)

153

𝑃

𝐿𝑖 =

𝑁 𝐿𝑖
∑𝑁𝐿𝑖

𝑁𝐿𝑖 𝑀𝑢𝑙𝑡𝑖𝑛𝑜𝑚𝑖𝑎𝑙(𝑃𝐿𝑖 , 𝑛)
𝑃𝐿𝑖 𝐷𝑖𝑟𝑖𝑐ℎ𝑙𝑒𝑡(𝜋)
𝜋𝑢𝑛𝑖𝑓𝑜𝑟𝑚(0.5)
In these equations, NLi represents the number of individuals in length class Li, and
NLi-1 denotes the number of individuals in the previous length class. CLi signifies the
expected catch when selectivity (SLi) is taken into account. Selectivity parameters
encompass α, the slope of the logistic selectivity curve, and Lc, the length at which 50%
of individuals are retained by the gear. Proportions-at-length (PLi) are presumed to adhere
to a Dirichlet-Multinomial distribution, where NLi conforms to a multinomial distribution
delineating the predicted catch at each size class L with proportions PLi. The Dirichlet rate
parameter π follows a uniform distribution as an uninformative prior.
Reference points for management are estimated from the preceding parameters
as follows:

𝐿𝑜𝑝𝑡 = 𝐿∞ (

3
𝑀
3+
𝐾

)

𝐹
𝐿∞ (2 + 3 )
𝑀
𝐿𝑐𝑜𝑝𝑡 =
𝐹
𝑀
(1 + )(3 + )
𝐾
𝐾
𝐿
𝐿
𝐿
𝐹
3(1 − 𝑐 )
3(1 − 𝑐 )2
(1 − 𝑐 )3
𝑀
𝑌′
𝐿
𝐿∞
𝐿∞
𝐿∞
𝑐
= 𝑀 (1 − ) 𝐾 (1 −
+
−
)
𝐹
1
2
3
𝑅
𝐿
∞
1+
1+ 𝑀 𝐹
1+ 𝑀 𝐹
1+ 𝑀 𝐹
𝑀
( + )
( + )
( + )
𝐾 𝐾
𝐾 𝐾
𝐾 𝐾

154

𝑌′
𝐶𝑃𝑈𝐸 ′ = 𝑅
𝐹
𝑀
𝐿𝑐
𝐿
𝐿
3(1 − ) 3(1 − 𝑐 )2 (1 − 𝑐 )3
𝐿𝑐 𝑀
𝐿∞
𝐿∞
𝐿∞
𝐵′0 = (1 − ) 𝐾 (1 −
+
−
)
1
2
3
𝐿∞
1+ 𝑀
1+ 𝑀
1+ 𝑀
( )
( )
( )
𝐾
𝐾
𝐾
𝐵
= 𝐶𝑃𝑈 𝐸 ′ ⁄𝐵′0
𝐵0
In these equations, Y’/R represents the yield per recruit, CPUE’ denotes an index
of relative catch per unit of effort, calculated by dividing Y’/R by F/M, and B/B0 denotes
the exploitable fraction of the total virgin biomass (B0). The relative biomass to achieve
maximum sustainable yield (BMSY/B0) is estimated by setting F/M to 1 and Lc = Lc_opt
(Froese et al., 2018). We also employed three indicators to evaluate the structuring of the
captured stock and identify population status (Medeiros-Leal et al., 2023).
Stocks were classified into different exploitation statuses based on B/BMSY values
(a proxy for current biomass relative to the biomass at maximum sustainable yield) as
follows: overexploited status was assigned when B/BMSY < 0.8, fully exploited status
when 0.8 ≤ B/BMSY ≤ 1.2, and non-fully exploited status when B/BMSY > 1.2 (Amorim et
al., 2019; Froese et al., 2015).
Between-chain convergence was assessed by visually examining MCMC
traceplots for each parameter and the potential scale reduction factor (Kruschke, 2021).
Model results were considered acceptable if simulated parameter values were consistent
across chains and exhibited a potential scale reduction factor close to unity.

155

2.3 Local Ecological Knowledge (LEK)
2.3.1 Data collection
Fisheries in the coast of Alagoas state, Brazil, are entirely artisanal and yield a few
hundred tonnes of catch every year . Mullets are amongst the most important exploited
species, contributing up to 20% of the total yearly yield (Torres et al. 2007). Other fished
species include various Sciaenids, penaeid shrimp, Carangids, Lutjanids, and spiny
lobster (Torres et al. 2007, Rangely et al. 2010, de Barros et al. 2021, 2022). Mullets are
mostly targeted with the use of cast nets and gillnets (Torres et al. 2007). Each
municipality often houses hundreds of fishers, with thousands alongside the state’s coast.
Interviews were conducted with 34 artisanal fishers from December to March 2023. These
fishers were all commercial fishers specializing in mullet fisheries along the coast of
Alagoas State. Among them, 12 were from the municipality of Barra de Santo Antônio
(North coast), 20 were from Pontal da Barra in Maceió City (Central Coast), and 2 were
from the municipality of Marechal Deodoro (Central Coast). The initial interviewees were
local leaders who then recommended other fishers for the survey, following the snowball
method (Gabor, 2007). A questionnaire consisting of semi-structured interviews with
open-ended, single-choice, and multiple-choice questions was utilized to gather
information on their Local Ecological Knowledge (LEK) regarding mullet species and their
fishing practices (see Appendix).

2.3.2 Data analysis
First, normality and homoscedasticity tests were conducted on fishing production
data reported by the fishermen. To assess if there is a significant perception of a decrease
in mullet stock, we conducted a paired t-test, comparing the weight values (in kg) reported
by each fisher for captures per fishing trip in the past and captures per fishing trip
nowadays (Appendix, question 10).

156

During interviews the LEK of fishers were assessed by questions (See, question 2
in questionnaire) related to aspects of life history traits used for stock assessments, such
as L50 and Lopt (Table 1). During interviews the LEK of fishers were assessed by
questions (See, question 2 in questionnaire) related to aspects of life history traits used
for stock assessments, such as L50 and Lopt (Table 1).
Table 1. Life history traits of stock assessments and respective questions used to assess
LEK.
Life history
trait

Meaning
The length at which the product of
the number of survivors and their
average weight is at its maximum
The length at which 50% of the
cohort of a fish species reached the
sexual maturity.

Lopt

L50

Question used to assess life
history trait by LEK
Which is
capture?

the

best

size

Which was the smaller size of
ovate female you captured?

Additionally, we performed binary tests to evaluate differences in:
I.

perceptions of mullet taste by development stage (questions 3 and 4);

II.

the practice of selling ovate lebranche mullet at a higher price (question 5).

To evaluate their perception of accountability and attitude toward stock recovery, we
categorized their responses regarding the cause behind the alteration (question 11: “Why
do you think they are decreasing?”) and the actions needed for stock recovery (question
12: “In your opinion, what must be done in order to recover the mullet stock?”). The
perception of accountability of the fisheries sector regarding mullet stock was classified
into the following options:
I.

Feels that fishers are partially responsible for the mullet stock decreasing;

II.

Does NOT feel that fishers are partially responsible for the mullet stock decreasing.

157

Their attitudes regarding the shared responsibility of fisheries sector to mullet stock
recovery was classified in the following options:
I.

Recognizes that fisheries sector must share the burden of actions to recover the
stock;

II.

Does NOT recognize that fisheries sector must share the burden of actions to
recover the stock.

To identify points of divergence and convergence between LEK and CSK, information
from various sources was compared. Divergences were examined to explore gaps that
require further investigation, while convergences were analysed to assess both positive
and negative findings, whether they were internal or external to fishery activities.2.5
Similarity between LEK and CSK.
The distributions of fishers' responses regarding Lopt and L50 values for the three
species was estimated using the kernel density function of the "ggplot2" R package
(Wickham, 2011). To test for overlaps between CSK and LEK, we employed one-sample
Wilcoxon signed-rank tests to compare fishers perceptions of Lopt and L50 with CSK
model results. Fisher’s responses regarding Lopt and L50 were considered samples to be
tested against the median CSK outputs. This non-parametric test was chosen after
verifying that the data does not meet parametric assumptions of normality with a ShapiroWilk test (p < 0.05). We used a significance level of 0.05.
To summarize good and bad practices among mullet fishers, we developed a SWOT
matrix (Humphrey, 1960) from the fisher’s interviews, which comprises positive and
negative observations pertaining to mullet fisheries, categorized as internal and external
factors:
•

Strengths (Positive + Internal): Factors within the fishery that are advantageous or
beneficial.

158

•

Weaknesses (Negative + Internal): Factors within the fishery that are
disadvantageous or problematic.

•

Opportunities (Positive + External): External factors outside the fishery that present
opportunities for improvement or growth.

•

Threats (Negative + External): External factors outside the fishery that pose risks
or challenges to the fishery.

3. Results
3.1 Conventional Scientific Knowledge (CSK)
A total of 1,166 specimens were analyzed, comprising 430 individuals of M.
rubrioculus, 376 of M. curema, and 360 of M. liza. Mugil rubrioculus exhibited the lowest
mean size (30.31 ± 2.62 cm) and maximum total length (44 cm), followed by M. curema
(31.97 ± 4.17 cm and 46 cm) and M. liza (48.61 ± 9.87 cm and 78 cm) (Fig. 2).

159

Figure 2. Length frequency data of populations of three mullet species: Mugil rubrioculus,
M. curema and M. liza.
Lc/Lc_opt ratios were above unity (1) for all stocks, indicating that length
distributions are not truncated and thus providing no evidence of inadequate catch of
small, undersized individuals. However, other indicators suggest potential overfishing
situations (Figure 3). For instance, despite the infrequent capture of small individuals,
L95/L∞ ratios indicate very low abundances of larger and older individuals. Additionally,
mortality/growth (Z/K) ratios were considerably high for all species (see Figure 3).
Similarly, the estimated current biomass values relative to the virgin stock biomass (B/B0)
were low, and posterior distributions for B/BMSY allowed us to classify M. rubrioculus and
M. liza as overexploited, and M. curema as fully exploited. Total mortality rates (Z) were
0.45, 0.39, and 0.37 year-1 for M. rubrioculus, M. curema, and M. liza, respectively (see
Table 2).

Figure 3. The top curves depict the LBB model’s fit to the length data, and the bottom
curves depict the LBB method’s prediction, where Lc denotes the length of 50% of the
individuals caught, L∞ is the asymptotic length, and Lopt is the length when the maximum
sustainable yield is achieved.

160

Table 2. Outputs of the Length-Based Bayesian Biomass (LBB) for Mugil rubrioculus, M.
curema and M. liza. Quantities are displayed as medians and 95% credible intervals of
Bayesian posterior distributions. Z stands for total mortality rates (year-1), Lc stands for the
length at first capture, Lc_opt stands for the optimal length at first capture, K and L∞ are von
Bertalanffy growth parameters, B stands for current biomass, B0 stands for the virgin or
unexploited biomass, BMSY stands for the biomass at the maximum sustainable yield, and
simple capture structuring indicators.
Species

M. rubrioculus

M. curema

M. liza

L50 (cm)

27.7 (25.9 – 29.9)

29.3 (28.6 – 30.0)

51.0 (50.4 – 54.0)

Z (year-1)
Lc (cm)
Lc/Lc_opt

0.45 (0.38 - 0.55)
28
1.2

0.39 (0.175 - 0.617)
27
1.3

0.37 (0.201 - 0.632)
40
1.1

Z/K

3.11 (2.81 – 3.37)

2.78 (2.53 – 3.05)

5.35 (4.87 – 5.34)

L∞ (cm)

38.5 (37.81 – 39.26)

41.1 (39.64 – 42.89)

74.3 (71.01 – 78.23)

B/B0

0.35 (0.24 – 0.47)

0.43 (0.28 – 0.65)

0.21 (0.17 – 0.27)

B/BMSY

0.78 (0.58 – 1.04)

1.13 (0.76 – 1.4)

0.59 (0.47 – 0.74)

Lc/Lmat (>1)

1.01

0.92

0.78

Lmax/Linf (>0.8)

1.14

1.12

1.05

Lmean/Lopt (>0.9)

1.29

1.53

1.28

Stock Status

Overexploited

Fully exploited

Overexploited

3.2 Local Ecological Knowledge (LEK)
On average, fishers have 35.44 (±18.19) years of experience. All the interviewed
fishers reported a drastic perceived decrease in the mullet stocks, regardless of age. The

161

current reported captures are 15.22% (±8.5) less than in past years, reflecting their
perception of a decline in the mullet stocks.
Of the 34 fishers interviewed, 70.5% stated that they prefer to consume mullet
based on its stage of development (p < 0.05), while the remaining fishers asserted that
the taste of mullets is not influenced by the stage of development. Among those fishers
who expressed a preference for taste based on the stage of development, 70.8% favoured
adult mullets (p > 0.05), while the remainder preferred juveniles.
When asked if they sell the ovate lebranche mullet (female Mugil liza with full
gonads), only 23.53% of the fishers reported this practice (binomial test – p < 0.01). These
fishers mentioned identifying the ovate lebranche mullet by the volume and shape of the
belly and selling the entire fish to clients. All fishers reported that they do not sell the
gonads separately, and the majority prefers to sell the fish body while keeping the gonads
for consumption at home, either fried or stewed as a culinary delicacy.
All fishers reported declining stocks for the three species studied over the years.
When analyzing the fishers' responses regarding the perception of the reasons for the
depletion in mullet stocks and what should be done to reverse this depletion, 41% of
fishers did not cite fishing as a causal factor for the depletion, nor did they point to
regulation of fishing as an action for improvement. Only six (~ 17%) fishers cited fishing
as a causal factor and regulation of fishing among the actions needed to recover the stock.
Nine fishers (~ 26%) cited fishing as responsible for the depletion but did not cite
regulation of fishing as an action to promote stock recovery, while three (~ 9%) did not
attribute fishing as responsible but cited regulation of fishing as an action to recover mullet
stock. The remaining 7% chose not to respond. The Chi-squared test indicates that fishers
who feel that increased fishing pressure is responsible for the perceived stock decline are
more likely to suggest regulatory measures to promote recovery (p < 0.05).
According to the fishers, M. liza is called "curimã" and the average value declared
for L50 is 59.32 cm with ±11.27 cm of Standard Deviation (S.D.). M. rubrioculus is known
as "negrão" or "tainha olho de fogo" and has an L50 of 29.68 cm (±5.31 cm S.D.). Mugil

162

curema is called "tainha" and reaches its L50 at 28.95 cm (±4.58 cm S.D.). The species
found most frequently in the marine environment was M. curema, and in the estuarine
environment, it was M. liza. The average Lopt for M. liza declared by fishers was 73,03
cm (±9.1 cm S.D.), while for M. rubrioculus was 37.83 (±4.97 cm S.D.) and for M. curema
was 40.06 cm (±5.55 cm S.D.).
3.3 Overlap between CSK and LEK
We found that the Lopt sizes indicated by fishers significantly differ (p-value > 0.05)
from the Lopt of the LBB model, with the model's Lopt consistently smaller than those
indicated by the fishers. Regarding maturation size (L50), there was no difference between
LEK and CSK for M. curema (p-value = 0.52), M. rubrioculos (p-value = 0.35), and M. liza
(p-value = 0.11) (see Figure 4).

Figure 4. Density distribution of fishers’ responses on Lopt (A) and L50 (B) values for the
three Mugil species. The red bars indicate the values estimated CSK (the LBB model) of

163

Lopt (A) and L50 (B). The distribution of responses given by fishermen for M. rubrioculus,
M. curema, and M. liza is represented by the colours blue, gray and green respectively.

4. Discussion
Our study applied the LBB method for the first time to mugilid stocks in conjunction
with LEK data in the Tropical Southwestern Atlantic. Overall, results suggest that Mugil
liza and M. rubrioculus stocks are overexploited. Notably, the Mugil liza stock appears to
be in the most critical situation, with current biomass close to only 20% of virgin biomass
(Table 2). This may be closely related to the species' slower growth and late maturity
relative to the other species, which is generally associated with lower resilience to
exploitation (Rangely et al., 2023; Tanner et al., 2019). This species also reaches the
largest size and is therefore highly sought after by fishers due to its high sales value.
Nevertheless, our results demonstrate that the three mullet stocks analysed here are
impacted by high fishing pressure and therefore need more comprehensive management
plans in place to ensure long-term sustainability in resource use and yield maximization.
Although artisanal fishing has been considered less impactful on the environment due to
a substantial subsistence component compared to industrial fishing (FAO, 2005; Teh and
Sumaila, 2018), this practice can also affect biomass levels and cause suboptimal yields
(Goetze et al., 2011; Hawkins; Roberts, 2004).
Data with appropriate spatial-temporal resolution such as several years of spatiallyexplicit monitoring are pivotal to obtain detailed information about population dynamics,
as well as biological responses to fishing pressure and environmental changes, a growing
scientific concern nowadays (Tanner et al., 2019). However, these long-term datasets are
scarce for artisanal fisheries due to their patchy, unregulated nature and poor resource
allocation to monitoring efforts. This creates a considerable mismatch between
management needs and resource availability, since only ~ 20% of the global catch comes

164

from regularly assessed industrial stocks (Worm et al., 2006; Costello et al., 2012). In this
context, LEK has great relevance to help manage artisanal, small-scale fisheries, as it
provides additional information that helps guiding potential strategies to ensure long-term
resource use. In this study, we underscore the usefulness of LEK data in monitoring efforts
aiming to understand the status of exploited, economically and socially important fish
stocks by demonstrating its close agreement with statistical assessment models.
We specifically found that the fisher’s perception of stock declines for the three
mullet species over the years agree with LBB model results indicating very low relative
biomass levels, especially for M. liza (Figure 3, Table 1). Our results are strikingly similar
to research conducted in the Southwestern Atlantic reporting close agreement between
fisher’s perception and long-term ecological data on the decline in catches and abundance
of important fishery species (Bender et al. 2014). Despite close agreements on stock
declines between CSK and LEK, these two sources diverge on the causes of these
declines. While LBB model results point to overfishing as the potential cause, most fishers
actually point out to environmental degradation. We argue that these results show the
potential of LEK not only to inform the management of data-limited fisheries by providing
past data on resource trends through structured interviews, but also to provide more
comprehensive and holistic views on management problems. We also demonstrated that
LEK data closely agrees with CSK on the L50 parameter, but not for Lopt. This is because
life-history traits such as growth/size and reproduction are more meaningful and tangible
to fishers when compared to Lopt (Herbst and Hanazaki, 2014; Nunes et al., 2019). In
fact, the “optimal” size for fishers would simply denote bigger fish that sell for higher prices,
while Lopt for LBB denotes the mean length of capture at which yield is maximized. This
demonstrates that information on life-history traits and stock status derived from LEK will
not always reflect the true underlying population dynamics, and highlights that extensive
validation might be needed before using LEK data on its own.
It is paramount to account for potential biases in LEK data such as the Shifting
Baseline Syndrome (SBS), where younger fishers are more likely to underestimate
potential population declines (e.g. Bender et al., 2014). This phenomenon can happen

165

because, with the ongoing and widespread environmental degradation that started a long
time ago, fisher’s acceptable conditions for what resembles a healthy fishery tends to
decrease over time (Soga and Gaston, 2018). To tackle this issue, we recommend the
inclusion of diverse age groups when conducting interviews to ensure enough contrast in
the data, as well as the inclusion of age as a covariate should an effect of this variable be
uncovered.
4.1 Good (and Bad) Management Practices
A strong indication that the mullet stocks analysed here are not being appropriately
managed is the widespread perception of decline over the past decades, possibly due to
historic negative fisher behaviours or external factors such as pollution and habitat
degradation (Silva et al., 2010; Silva et al., 2009). An example of good management
practices already adopted by local fishers is the preference for consuming adult mullets,
which allows at least one or more reproductive cycles to take place before capture (Soares
et al., 2020). Moreover, reports of more frequent sizes of mullets ranging around the
optimal weight or above the L50 are also beneficial for stock management for the same
reason (Soares et al., 2020).
However, the practice of consuming M. liza (lebranche mullet) roe is potentially
negative for stock management since it involves capturing the fish during their
reproductive period, specifically before spawning. Historically, during the ascension
Thursday, a tradition known as "Dia-da-hora" in Alagoas State, locals consumed
lebranche roe without necessarily utilizing the entire fish for consumption (Cascudo,
1984). This led to large quantities of captured lebranche being discarded, which ultimately
contributes increased fishing pressure due to the high demand. Nowadays, the practice
of consuming lebranche roe has significantly decreased due to the stock decline, and also
possibly due to environmental education initiatives (Marques et al., 2005; Santos and
Sampaio, 2013; Siemer and Knuth, 2001; Patterson et al., 2009). While the practice of
consuming gonads still exists, fishers now also utilize the whole fish for consumption or

166

selling as opposed to consuming gonads only, which is a positive factor for stock
restoration.
The low sense of responsibility among fishers for stock management presents a
challenging scenario for management (Table 2). A significant challenge in the recovery of
mullet stock in the Mundaú Lagoon and Santo Antônio River is the historical lack of
accountability among fishers and their low sense of guilt or responsibility due to
unsustainable fishing practices. The magnitude of impacts from pollution and mining in
both estuaries may lead fishers to perceive fishing pressure as less impactful, resulting in
a reluctance to implement fisheries regulations (Silva and Sousa, 2009; Almeida et al.,
2009; Drymon and Scyphers, 2017; Cardona et al., 2013). Historically, global fisheries
have been managed through centralized models with limited social participation, leading
to a lack of recognition of stakeholders' roles in decision-making (Cochrane, 2000). Efforts
to change fisher’s perceptions regarding causes of stock declines will improve collective
behaviour in the future (Gelcich et al., 2005; Thompson, 2008), and initiatives engaging
fishers in decision-making have shown promising outcomes by increasing their sense of
participation and promoting accountability in stock management (Pita et al., 2009;
Mikalsen and Jentoft, 2008; Lorenzen et al., 2010).
Among positive factors that might contribute to stock recovery in the future, the
increased interest of environmental agencies in integrating fishers in the management
process is an important factor (Table 2). Local environmental agencies and academic
entities are increasingly approaching traditional fisher communities to offer them
opportunities to engage in discussions regarding potential management strategies. In
addition to building more trust between governmental agencies and traditional
communities, these initiatives also help foster a sense of inclusion amongst these
communities, which might contribute to increased compliance with eventual management
procedures put in place (Castillo et al. 2024).

Table 2. SWOT matrix composed of Positive vs negative points and internal vs. external
factors associated with overexploitation according to fishers.

167

●

INTERNAL
●
●

●

EXTERNAL
●

POSITIVE
Strengths:
Consumption of fishes with
size/weight ranging within the
Optimum Yield per recruit;
Higher
preference
for
consumption of adult mullet
individuals;
Low rate of selling of ovate
lebranche mullet;
High sense of perception of
mullet stock decreasing.

Opportunities:
Increasing
interest
of
environmental
agencies
to
integrate
fishers
in
comanagement initiatives;
Academia is interested in
collaborating with the fisheries
sector using LEK.

●

NEGATIVE
Weaknesses:
Strong
practices
of
consumption of mullet roe
among fisher;
Low sense of association
between stock decreasing
and fishing pressure;
Low sense of accountability in
management actions needed
for mullet stock recovery;
Use of gillnets with mesh size
below 35mm between knots
among some fisher.
Threats:
High levels of estuarine
pollution caused by the sugarcane industry;
Estuarine silting up caused by
pollution
and
mining
activities.

Integrating ecological systems with environmental managers, the scientific
community, and users of the system, such as fishers, who have different perspectives on
the same problem, is a significant challenge. Socio-environmental conflicts and tensions
among these actors underscore the need for co-management to achieve genuine socioecological connectivity and effective management of this crucial fishing resource. Comanagement, as defined by Berkes et al. (1998), involves sharing responsibility and
power between resource users and the government. Therefore, management plans must
integrate both Local Ecological Knowledge (LEK) and Conventional Scientific Knowledge
(CSK) through robust and reliable co-management strategies (Carlsson and Berkes,
2005). Horizontal collaboration is essential, allowing fishers, managers, and scientists to
have an active voice in the decision-making process while acknowledging the experiences
of actors and stakeholders from traditional communities. The construction of the SWOT
matrix (Table 2) serves as an initial step in identifying Strengths, Weaknesses,
Opportunities, and Threats. In the case of the mullet stocks, co-management is urgently
needed due to the overexploitation of these stocks.

168

5. Conclusion
Our findings reveal that two of the studied stocks, M. liza and M. rubrioculus, are
overexploited, while one is at its maximum sustainable yield and therefore fully exploited
(M. curema). The overlap between Conventional Scientific Knowledge (CSK) and Local
Ecological Knowledge (LEK) on stock declines underscores the potential of LEK as an
accessory tool to inform the management of data-limited fisheries, while differences in
perceived causes of declines reflect the need to adopt increasingly holistic approaches to
solve broader environmental problems that might contribute to stock declines. This
highlights the importance of participatory management (horizontality) among various
stakeholders, including government managers, fishers, and the scientific community, to
address challenges, promote responsible resource management, and ensure the wellbeing of ecosystems and fishing communities. The SWOT matrix derived from LEK
interviews serves as an initial step in this process, offering insights into the perceptions,
attitudes, and behaviours of mullet fishers. Stock assessment outputs emphasize the
need for ecological conservation of the species in the face of overexploitation and other
anthropogenic effects.

Declaration of interest
We have no conflicts of interest to disclose.

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 and #442237/2020-0), FAPEAL - Research Support Foundation of the
State of Alagoas (#60030.1564/ 2016) and by Coordination for the Improvement of Higher
Education Personnel CAPES-Brazil CAPES (#23038.000452/2017-16). We are thankful
to CNPq for the research grant to N.N.F., (#306624/2014-1), all fishermen who helped in

169

the field work, and to all members of the Fish and Fisheries Ecology Laboratory and the
Conservation and Management of Natural Resources Laboratory.

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178

7. Discussão geral

Os resultados aqui apresentados demonstram a alta complexidade nos
mecanismos

coexistência

espécies

congenéricas

morfologicamente

semelhantes, que podem ser evidenciados por uso de habitat, crescimento e plasticidade
individual e interespecífica. Sedo esses mecanismos importantes para compreensão da
dinâmica e das interações dentro e entre as populações e que influenciam até mesmo
para a avaliação dos estoques pesqueiros.
No primeiro capítulo a diferenciação em relação ao padrão de uso de habitat nos
permite compreender os mecanismos de coexistência de duas espécies de Mugil. Sendo
que M. curema é influenciado por fatores como temperatura e oxigênio dissolvido,
clorofila e turbidez, enquanto que M. rubrioculus é influenciado por variações na
salinidade. Considerando que o M. rubrioculus e M. curema são filogeneticamente mais
próximos (Neves et al., 2020), já prevíamos que exibiriam graus mais elevados de
sobreposição de nicho e, portanto, precisam realizar ciclos de vida temporariamente
desacoplados. Especificamente, M. rubrioculus, ocupa a parte externa do estuário e o
mar, já M. curema é capaz de ocupar os três ambientes na primeira fase do seu ciclo de
vida.
Portanto, um dos mecanismos que poderia ter levado a tais histórias de vida
dissociadas em tainhas tropicais é o deslocamento de caráter, reconhecido como um
processo comum quando se descobre que espécies simpátricas diferem no uso de
recursos (Goldberg & Lande, 2006). Que pode ser explicado como diferenças induzidas
pela competição nas características da história de vida através da plasticidade fenotípica,
causando a ocorrência de seleção diferencial (Slatkin, 1980). Além das interações
complexas entre variáveis bióticas e abióticas podem explicar variações no uso do habitat
dos peixes ao longo do tempo e do espaço (da Silva et al., 2021, 2022).
No segundo capítulo nós demostramos que o crescimento polifásico alométrico
em otólitos de peixes pode ser um indicador adequado de eventos cruciais do ciclo de
vida, como maturação sexual e mudanças ontogenética de habitat. Já que a espécie de
crescimento mais rápido (M. rubrioculus) atingiu os menores tamanhos assintóticos e

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exibiu mudanças mais precoces na alometria e maturação, e a espécie de crescimento
mais lento (M. liza) mostrou tamanhos maiores e mudanças posteriores nos padrões
alométricos e maturidade. Sendo M. curema a espécie intermediária, tanto em
comprimento, quanto em velocidade de crescimento. Então, as diferentes idades na
maturidade e mudanças na alometria mostram que espécies simpátricas de Mugil podem
ter uma assincronia de tempo e espaço nos ciclos de vida para permitir a coexistência.
Essa assincronia é provavelmente uma resposta evolutiva que aumenta a aptidão de
espécies coocorrentes ecologicamente semelhantes expostas aproximadamente às
mesmas condições ambientais (Chang e Iizuka, 2012; Scott & Johnson, 2010).
Partindo do pressuposto de que a estuarino dependência gera um ponto de
inflexão no ciclo de vida, mudando a velocidade de crescimento, ou seja, quanto mais
tempo eles passam no estuário, maior é o pré ponto de inflexão, que é a etapa do ciclo
de vida de maior investimento em crescimento (Sousa et al. 2015) e isso poderá se
traduzir em maiores tamanhos. Então, no terceiro capítulo da tese, foi utilizado a
temporalização da microquímica expressa pelas diferentes quantidades do elemento
traço estrôncio ao longo do raster do núcleo a borda do otólito, percebemos que, das três
espécies, a que passa mais tempo da sua primeira fase do ciclo de vida no estuário é M.
liza. Que é justamente a espécie com menor velocidade de crescimento, que possui maior
longevidade, com menor plasticidade individual em relação ao uso de habitats. No outro
extremo encontramos M. rubrioculus, que possui uma menor estuarino dependência,
estando adaptado a salinidades mais altas, maior velocidade de crescimento, chega a
um tamanho máximo menor entre as espécies estudadas e possui grande plasticidade
no uso de habitat. Já os indivíduos de M. curema apresentaram a maior plasticidade
individual no uso dos habitats, apresentando maior migração parcial.
A migração parcial gera uma redução temporária da concorrência com espécies
não migratórias, ou seja, afeta a estrutura da comunidade, reduzindo a concorrência e,
portanto, permitindo a coexistência (Johnson, 1980; Peller et al., 2023). Evolutivamente,
a maior plasticidade migratória entre habitats pode gerar uma maior adaptabilidade da
espécie e consequentemente maior resiliência (Tamario et al., 2019). Quando ocorre a
migração parcial o estoque como um todo, até certo ponto, fica menos vulnerável a

180

atividade pesqueira, por exemplo, tendo maiores chances de sobrevivência, já que eles
têm múltiplos contingentes de peixes que usam diferentes habitats dentro da mesma
população (Fowler et al., 2016). Dessa forma, essa menor plasticidade no uso de habitats,
assim como menor taxa de crescimento pode estar afetando diretamente a resiliência em
relação a pesca para a população de M. liza.
Então, no quarto capítulo dessa tese, constatamos que o estoque de M. liza é o
mais afetada por essa atividade na região estudada, apresentando o maior declínio,
tendo hoje apenas 20% do estoque original. Nesse sentido, é possível indicar essa
espécie como prioritária para o manejo e conservação de Mugilidae nos estuários
estudados, considerando que quanto maior a permanência no habitat a espécie se torna
mais vulnerável a perda desse habitat e a pressão por pesca. Dessa forma, temos uma
medida da vulnerabilidade à perda de habitat, às mudanças climáticas e à pesca. Isso é
particularmente relevante ao considerarmos a acelerada degradação dos ambientes
costeiros tropicais, impulsionada pela especulação imobiliária e pela expansão de
empreendimentos voltados ao turismo, frequentemente acompanhados de ocupação
desordenada e destruição de áreas essenciais, como manguezais e estuários (Miranda
et al., 2002). Adicionalmente, a descarga de esgoto doméstico e industrial não tratado,
bem como o despejo de resíduos da tiborna de cana-de-açúcar diretamente nos rios,
agravam a poluição e comprometem ainda mais esses ecossistemas frágeis. Esses
fatores são agravados pelo aumento da pressão da pesca decorrente do crescimento
populacional na região (Blaber & Barletta, 2016) e pelos registros de sobrepesca
(Mendonça & Bonfante, 2011). Diante desse cenário, a necessidade de preservar os
estuários torna-se crucial, uma vez que eles desempenham um papel indispensável como
áreas de berçário para diversas espécies marinhas e como reguladores naturais da
qualidade da água. A conservação desses habitats é vital para garantir não apenas a
sustentabilidade dos recursos pesqueiros, mas também a manutenção da biodiversidade
e o equilíbrio ecológico.
Nesse sentido, para fazer a gestão adequada desse recurso também é relevante
considerar o conhecimento Conhecimento Ecológico Local (LEK), já que ressaltamos a
compreensão dos pescadores sobre os traços da história de vida. Como já visto por

181

Karnad (2022), o uso da gestão participativa pode aumentar a conservação dos
ambientes. E Sultana e Abeyasekera (2008) trouxe evidências estatísticas de que o apoio
à gestão de recursos foi mais eficaz quando iniciado através de um processo envolveram
a participação da comunidade e o estabelecimento de instituições locais de gestão das
pescas. Destacamos então a importância da gestão participativa (horizontalidade) com
os atores da pesca, incluindo gestores governamentais, pescadores e a comunidade
científica, para promover a gestão responsável dos recursos e garantir o bem-estar dos
ecossistemas e que as necessidades locais das comunidades sejam atendidas.
Constatamos que a coexistência entre espécies congenéricas de Mugil é facilitada
por uma complexidade de mecanismos, nos quais fatores como uso do habitat, padrões
de crescimento e plasticidade desempenham papéis fundamentais para a compreensão
das dinâmicas populacionais e das interações ecológicas. A segregação espacial
observada entre as espécies parece resultar de adaptações divergentes às condições
ambientais, refletidas nos padrões de crescimento alométrico dos otólitos, que se
mostram preditores significativos de eventos críticos do ciclo de vida.
Dada a plasticidade de uso do habitat, é razoável concluir que M. curema é mais
capaz de sobreviver e manter populações em uma variedade de salinidades. Essa
característica aumenta suas chances de sobrevivência ao otimizar o uso de habitats
temporariamente favoráveis o que a beneficia em relação a manutenção dos estoques
pesqueiros. Por outro lado, a menor plasticidade de M. liza em relação ao uso do habitat
a torna mais dependente de ambientes específicos e estáveis para completar seu ciclo
de vida. Essa dependência, aliada ao seu crescimento mais lento, aumenta a
vulnerabilidade da espécie à degradação dos habitats costeiros, como estuários e áreas
de manguezais, que são frequentemente impactados por atividades humanas, como
poluição e ocupação desordenada. Esses fatores, somados à intensa pressão de pesca,
resultaram na redução de seus estoques para apenas 20% do nível original. Concluímos
que a gestão adequada dos recursos pesqueiros de Mugilidae exige uma abordagem
abrangente, que leve em conta a variabilidade ambiental e as peculiaridades de cada
espécie, além de integrar o Conhecimento Ecológico Local (LEK) das comunidades
pesqueiras para promover uma gestão sustentável dos recursos.

182

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