Doctoral dissertation in Biology (Specialization in Marine Biology and Aquaculture)
presented to the University of Lisboa Dissertação apresentada à Universidade de Lisboa
para obtenção do grau de Doutor em Biologia (especialidade Biologia Marinha e Aquacultura)
Inês Pena dos Reis Alfaro Cardoso 2011
Recomeça…. Se puderes Sem angústia E sem pressa.
E os passos que deres, Nesse caminho duro Do futuro
Dá-os em liberdade. Enquanto não alcances Não descanses.
De nenhum fruto queiras só metade.
E, nunca saciado, Vai colhendo ilusões sucessivas no pomar. Sempre a sonhar e vendo O logro da aventura. És homem, não te esqueças! Só é tua a loucura Onde, com lucidez, te reconheças…
Miguel Torga
ABSTRACT AND KEY-WORDS 9
RESUMO E PALAVRAS-CHAVE 11
RESUMO ALARGADO 13
LIST OF PAPERS 17
PART 1-Aims and Scope of the thesis 19 CHAPTER 1 21
General introduction 23
Aims and importance of the thesis 26
Thesis outline 27
PART 2- Ecological Characterization of Small Estuaries Based on fish and Macroinvertebrate Communities: A Functional Approach. 33
CHAPTER 2 35
Fish assemblages of small estuaries of the Portuguese coast: a functional approach 37
CHAPTER 3 57
Distribution patterns of benthic macroinvertebrate assemblages in small estuaries of the Portuguese coast. 59
PART 3 - Ecological Quality Assessment on Small Estuaries of the Portuguese South and Southwest Coasts based on Fish and Macroinverterate Communities. 79 CHAPTER 4 81
Ecological quality assessment of small estuaries from the Portuguese coast based on fish assemblages indices. 83
CHAPTER 5 107
Ecological quality assessment of small estuaries from the Portuguese coast based on benthic macroinvertebrate assemblages indices. 109
PART 4-Vulnerability assessment 129
CHAPTER 6 131
Vulnerability assessment in small estuaries from the Portuguese coast 133
PART 5- General Discussion 149
CHAPTER 7 151
General discussion and final remarks 153
Abstract
Estuarine ecosystems are amongst the most valuable environments in the world because of their high productivity and their fundamental role concerning ecosystem services for coastal communities. These systems are historically under high levels of human induced impacts which drove to the acknowledgement that management measures must be taken. Within the European context, the Water Framework Directive established goals to preserve estuarine systems’ integrity and tools were developed by the scientific community to respond to those goals and produce some measurement of the systems’ ecological quality. For the establishment of ecological integrity, knowledge on systems ecological communities is fundamental. This work aimed to contribute to the actual knowledge on small estuarine systems of the Portuguese south and southwestern coasts highlighting their ecological relevance. Fish and benthic macroinvertebrate communities from five small estuarine systems were analysed since they are considered fundamental ecological indicators. Results showed that these small estuarine systems provide temporary habitats, shelter and feeding grounds to coastal fish communities. Seasonal patterns were important to the diversity values found for fish communities. For benthic communities, results indicated sediment components are important to explain differences between systems. With this knowledge support, tools to assess ecological quality were chosen and applied, for both fish and macroinvertebrate communities. Result interpretations were not straightforward to the assessment of ecological quality status in systems with high natural perturbations indices. Nevertheless, analyses of all metrics included was highly informative and enabled, to some extent, differentiating ecological conditions between systems. An assessment of systems vulnerability was made which allowed setting guidelines and recommendations for management and preservation of each system.
Key-words: benthic macroinvertebrate communities; ecological quality; fish assemblages; small estuaries; vulnerability assessment.
Resumo
Os sistemas estuarinos estão entre os ecossistemas mais valorizados não só devido à sua elevada produtividade mas também aos serviços fundamentais de ecossistema que proporcionam às populações costeiras. Estes ecossistemas têm sido historicamente sujeitos a elevados níveis de pressão antropogénica, o que levou à necessidade do estabelecimento de medidades de gestão. No contexto Europeu, com a Directiva Quadro da Água, foram delineados objectivos concretos para a preservação dos estuários e foram desenvolvidas ferramentas para uma avaliação do seu actual estado ecológico. As comunidades de peixes e de macroinvertebrados bentónicos são consideradas componentes fundamentais para a avaliação do estado ecológico dos sistemas estuarinos, sendo fundamental o conhecimento dos factores que determinam a diversidade, composição específica e distribuição destas comunidades. O presente trabalho contribui para o conhecimento da ecologia de cinco pequenos estuários das costas Sul e Sudoeste de Portugal, evidenciando a função ecológica destes sistemas. Os resultados mostraram que os sistemas escolhidos são importantes habitats temporários para as comunidades de peixes costeiras, servindo de abrigo e local de alimentação. Para estas comunidades, os padrões sasonais foram determinantes para os valores de diversidade. Para as comunidades de macroinvertebrados, os resultados suportaram a hipótese de que as características do sedimento explicam as diferenças entre as comunidades dos diferentes sistemas. Estes resultados contribuíram para a escolha das ferramentas a utilizar na avaliação da qualidade ambiental, e diversos índices ecológicos foram aplicados a cada comunidade. Apesar da dificuldade de interpretação das actuais ferramentas nestes sistemas de elevada variabilidade natural, os resultados evidenciaram que as métricas em que se baseiam os índices aplicados são bastantes informativas permitindo, até certa medida, diferenciar diferentes estados ecológicos ao longo dos sistemas. A avaliação de vulnerabilidade efectuada para cada sistema permitiu o estabelecimento de possíveis medidas e linhas de mitigação dos principais impactos antropogénicos.
Palavras-chave: comunidades de macroinvertebrados benónicos; comunidades de peixes; pequenos estuários; qualidade ecológica; vulnerabilidade.
Resumo Alargado
Os sistemas estuarinos estão entre os sistemas mais valiosos do planeta dada a sua elevada produtividade e diversos serviços de ecossistema que proporcionam às populações costeiras. Estes serviços são historicamente utilizados pelas populações humanas e o crescente desenvolvimento do sistema urbano em zonas adjacentes aos estuários tem-se traduzido, ao longo dos tempos, em elevados níveis de pressão antropogénica com impactos que põem em causa a integridade ecológica e funcional destes ecossistemas. Actualmente, a necessidade de tomar medidas mitigadoras desses impactos e promover a preservação dos estuários, promoveu o aparecimento de medidas legislativas, nomeadamente da Directiva Quadro da Água para o contexto Europeu, que visam o estabelecimento de objectivos comunitários para a preservação destes sistemas. Neste contexto, diversas ferramentas foram desenvolvidas para responder à necessidade de se avaliar o actual estado ecológico dos estuários e vários planos de monitorização foram desenhados. No entanto, quase todos os sistemas estuarinos de pequenas dimensões da costa Portuguesa foram excluídos dos planos de monitorização, tornando estes sistemas, sobre os quais o conhecimento cientifico é escasso, altamente vulneráveis a um desaparecimento funcional discreto. Sistemas estuarinos de pequenas dimensões têm particularidades que os tornam altamente dinâmicos em termos morfológicos: podem apresentar cordões dunares, que periodicamente encerram a abertura do estuário ao meio marinho, e o fluxo de água doce é torrencial dependendo em grande medida da sazonalidade relacionada com os níveis de precipitação. Aspectos relacionados com a evolução, no tempo e no espaço, dos gradientes ambientais diferem, por estas razões, de sistemas de maior dimensão, fazendo com que estes pequenos estuários se situem, provavelmente, num extremo máximo da variabilidade natural. Neste contexto, a presente tese pretende contribuir para o actual conhecimento sobre pequenos estuários, estabelecendo a sua função ecológica e a estrutura das suas comunidades biológicas, fazendo uma avaliação da actual integridade ecológica destes sistemas e, finalmente, quantificando a vulnerabilidade de cada sistema. Para isto, foram escolhidas as comunidades de peixes e de macroinvertebrados bentónicos como componentes biológicas fundamentais e foram estudados cinco pequenos estuários da costa Portuguesa: Mira, Odeceixe e Ajezur, situados na costa Sudoeste e inseridos no Parque Natural da Costa Vicentina e Sudoeste Alentejano; Bensafrim e Gilão, situados na costa Sul, estando este último em estreita ligação com o Parque natural da Ria Formosa.
A presente tese está dividida em cinco partes nas quais se distribuem sete capítulos, dos quais cinco correspondem a artigos científicos, produzidos para responder directamente aos
objectivos propostos e que estão publicados ou em revisão, em revistas internacionais com arbitragem científica, incluídas no Science Citation Index. Estes cinco capítulos são precedidos de um capítulo de introdução geral e seguidos de um capítulo de discussão geral e considerações finais.
Na introdução geral, Capítulo 1 (Parte 1) é feito um enquadramento teórico sobre os vários temas desenvolvidos, dando especial enfase às razões que tornaram urgentes as medidas legislativas de gestão e conservação dos sistemas estuarinos. É ainda realçado o desafio que representa a gestão e a manutenção dos ecossistemas estuarinos, apontando as características inerentes as estes sistemas que tornam complexa a avaliação da sua integridade ecológica. Neste contexto, as particularidades dos pequenos sistemas estuarinos são também referidas. O âmbito do presente trabalho e os principais objectivos são também delineados neste primeiro capítulo.
Os aspectos referentes às características das comunidades de peixes e de macroinvertebrados bentónicos são tratados na Parte 2. A função destes sistemas para as comunidades de peixes costeiras enquanto habitat temporário, abrigo e local de alimentação é descrita no Capítulo 2. Aqui é também apontado o padrão de sasonalidade como um factor importante para a diversidade das comunidades ícticas que utilizam estes ecossistemas. Os factores que influenciam as diferenças entre as comunidades de macroinvertebrados bentónicos entre os diferentes sistemas são desenvolvidos ao longo do Capítulo 3. Para estas comunidades os resultados evidenciaram a complexidade na definição de factores concretos e universais que determinem a distribuição das comunidades. As análises efectuadas realçaram também que, numa escala alargada, i.e. entre estuários, as características do sedimento (e.g. granulometria) são responsáveis por grande parte da variabilidade, em termos de riqueza e diversidade, entre as comunidades dos vários estuários.
Uma vez reconhecidos alguns dos factores que traduzem uma variabilidade natural e que, de certa forma, diferenciam os diferentes sistemas, na Parte 3 da presente tese foram aplicadas diferentes ferramentas, desenvolvidas para dar resposta à actual legislação comunitária, e que se apresentam sob a forma de índices. Estas ferramentas têm como objectivo fazer uma avaliação da qualidade ecológica dos diferentes sistemas, e traduzi-la numa linguagem concreta que permita uma comunicação efectiva entre a comunidade científica e as entidades responsáveis pela gestão ambiental. Assim, e com recurso a uma selecção de índices desenvolvidos para estuários, foi avaliada a qualidade ecológica de cada estuário considerando a comunidade de peixes (Capítulo 4) e a comunidade de macroinvertebrados bentónicos (Capítulo 5). Uma avaliação e quantificação dos níveis de impacto a que cada sistema está sujeito foi feita a priori, por forma a fazer uma correspondência entre o estado ecológico de cada sistema e a magnitude das suas potenciais fontes de impacto (e.g. percentagem de solo utilizado para exploração agrícola, número de estações de aquacultura). Para ambas as comunidades, optou-se pela diferenciação de estados ecológicos fazendo uma abordagem essencialmente comparativa, em vez de estabelecer estados ecológicos concretos correspondentes ao resultado directo da aplicação
de cada índice, dada a elevada dificuldade da definição de comunidades de referência destes sistemas devida à sua elevada variabilidade natural e dinâmicas temporal e espacial. A análise das diferentes métricas dos vários indices mostrou ser muito informativa, particularmente num contexto em que o resultado directo de cada indice dificilmente ditinguiu estados ecológicos. Para ambas as comunidades, a distinção entre a pertubação natural e a pertubação antropogénica mostrou ser o principal problema para a diferenciação e identificação de diferentes estados de qualidade ecológica.
A manutenção da integridade ecológica e a gestão dos ecossistemas, inclui os passos delineados ao longo dos Capítulos 2, 3, 4 e 5. No entanto, a avaliação do estado ecológico, por si só, não identifica as principais pessões a que os sistemas estão sujeitos, nem define prioridades nas medidas mitigadoras a tomar no caso do sistema se afastar do equilíbrio definido como sendo o estabelecido pela variabilidade natural do sistema. Através da avaliação da vulnerabilidade descrita no Capítulo 6 (Parte 4), foi possível determinar e quantificar a vulnerabilidade dos diferentes sistemas e quantificar o risco de alteração de habitat através da quantificação da magnitude das principais fontes de impacto. Sobre os sistemas estudados a informação necessária para uma avaliação precisa de vulnerabilidade é escassa, forçando a análise a uma larga escala de avaliação das forças geradoras de perturbação antropogénica. No entanto, este facto não impossibilitou a sua quantificação, ainda que dados mais localmente concentrados e actualizados fossem preferíveis. Desta forma, medidas concretas e prioridades de acção foram sugeridas para cada sistema, respondendo aos principais objectivos deste capítulo: identificar para cada estuário a origem de vulnerabilidade, quantificar factores concretos de impacto, e sugerir linhas prioritárias para a mitigação do efectivo e potencial risco de perda do valor ecológico e funcional dos pequenos estuários.
Por fim, na Parte 5, Capítulo 7, são descritas as principais conclusões de cada capítulo, sobre as quais incide uma discussão geral, em que se dá relevo à necessidade de se aprofundar o conhecimento sobre a dinâmica das comunidades estuarinas e dos factores ambientais que a determinam. Refere-se ainda a necessidade de testar novas metodologias que permitam de uma forma integradora, que inclua aspectos relacionados com a morfologia e da diversidade de habitat, na avaliação da qualidade ambiental do sistemas. Factores esses absolutamente fundamentais à estrutura e diversidade específica das comunidades biológicas e que são determinantes para uma efectiva interpretação da qualidade ambiental feita a partir da componente biológica dos ecossistemas.
L
IST OF PAPERSThis thesis comprises the papers listed below, each corresponding to a Chapter, from 2 to 5. The author of this thesis is the first author in all papers and was responsible for the conception and design of the work, field surveys, sample collection and processing, laboratory analytical procedures, data analyses and manuscript writing of all the papers. Remaining authors collaborated in some or several of these procedures. All papers published or in press were included with the publishers’ agreement.
CHAPTER 2: Fish assemblages of small estuaries of the Portuguese coast: a functional approach.
Inês Cardoso, Susana França, Miguel P. Pais, Sofia Henriques, Luís Cancela da Fonseca, Henrique N. Cabral.
Published in Estuarine, Coastal and Shelf Science (2011) 93, 40-46.
CHAPTER 3: Distribution patterns of benthic macroinvertebrate assemblages in small estuaries
of the Portuguese coast.
Inês Cardoso, Luís Cancela da Fonseca, Henrique N. Cabral. In review in Estuarine Costal and Shelf Science.
CHAPTER 4: Ecological quality assessment of small estuaries from the Portuguese coast based
on fish assemblages indices.
Inês Cardoso, Miguel P. Pais, Sofia Henriques, Luís Cancela da Fonseca, Henrique N. Cabral. Published in Marine Pollution Bulletin (2011) 62: 992-1001.
CHAPTER 5:Ecological quality assessment of small estuaries from the Portuguese coast based on benthic macroinvertebrate assemblages indices.
Inês Cardoso, Luís Cancela da Fonseca, Henrique N. Cabral. Accepted in Marine Pollution Bulletin
CHAPTER 6: Vulnerability assessment in small estuaries from the Portuguese coast. Inês Cardoso, Luís Cancela da Fonseca, Henrique N. Cabral.
Submitted to Marine and Fresh Water Research.
Inês Cardoso was funded with a Ph.D. grant by Fundação para a Ciência e Tecnologia (FCT) (PTDC/MAR/64982/2006).
P
ART
1
C
HAPTER
1
General introduction, Aims and importance of the thesis and Thesis
outline
General introduction
Aims and importance of the thesis
Thesis outline
General introduction
Estuarine ecosystems are among the most valuable environments in the world, not only because of their high productivity but also due to their fundamental role concerning ecosystem services for coastal communities (Costanza et al., 1997). Ecosystem services are defined as “the direct or indirect contributions that ecological systems make to the well-being of human populations” (U.S. EPA, 2009). The inclusion of this concept in the value of coastal environments happens as a reflection of the acknowledgment that these are human-ecological coupled systems (Luers et al., 2003). In this context, estuarine systems, as all coastal environments, provide a wide range of services that include: coastal protection, erosion control, nutrient cycling, water purification, carbon sequestration, nursery grounds for commercial species and services that include tourism and recreation (Barbier et al., 2011). The question about the maintenance of these services arises because, historically, they all involve some degree of human input with the consequent impact on the good quality of these services and in the processes and system functions in which they are based on (Barbier et al., 2011). In our days, these ecosystems are facing increasing and significant human-induced impacts, which include physical and chemical transformation, habitat destruction and changes in biodiversity (Halpern et al., 2007).
The ultimate challenge of scientists and policy makers is to manage estuarine systems in order to improve their ecological quality, prevent further deterioration, and ensure the progressive reduction of pollution. These are the main objectives of the Water Framework Directive (WFD), developed for the European Union, which has the final goal of achieving a “good ecological quality status” for all water bodies by 2015 (EC, 2000; Borja et al., 2006). This directive urged the development of consistent tools to assess the ecological status of estuarine systems.
The goal of achieving the good quality status requires a fundamental knowledge of ecological integrity of a given system. The general idea is that, when ecosystems are not suffering from unusual external perturbations, we observe certain well-defined developmental trends (Odum, 1985). Thus, ecological integrity indicates the divergence from natural conditions, which is attributable to human activities (Karr, 1991).
The task of evaluating ecosystems health is far from simple. These systems are extremely complex, as they comprise a number of interacting components which may vary in type, structure and function within the whole system (Costanza and Mageau, 1999). This complexity lead to a biological criterion of ecosystem integrity, where biological indicators are used to increase the probability that an assessment program will detect degradation due to anthropogenic influences (Karr, 1991; Nip and Udo do Haes, 1995; Whitfield and Elliott, 2002).
Following the biological criterion, biological communities are chosen for the application of tools in a form of indices in order to extract information about the actual ecosystem ecological integrity. This criterion assumes that biological communities do respond to human impact and that, ideally, shifts on their expected structures are forced by anthropogenic unbalanced use of natural resources. At this point, it is clear that we have to be able to distinguish deviations induced by human activities from the ones resulting on changes of the ecosystems’ equilibrium state originated by natural processes. This is especially difficult in the case of estuaries, since they are naturally stressed and highly variable ecosystems that are at the same time, exposed to high degrees of anthropogenic stress, a problem recently termed as “Estuarine Quality Paradox” (Dauvin, 2007; Elliott and Quintino, 2007).
Fish and benthic macroinvertebrate communities are key biological elements considered in the evaluation of estuarine ecological status (EC, 2000). The first step must be, therefore, to understand natural populations within these communities, and have some reference of their natural driving forces of distribution. Several environmental factors that contribute to community structure were already identified both for fish and benthic macroinvertebrates communities. For fish communities these factors are: habitat availability, salinity, current velocity, temperature, oxygen concentrations (Thiel et al., 1995; Methven et al., 2001) and also seasonal patterns, strongly influenced by biotic factors such as migrations and recruitment patterns (Maes et al., 2004). For benthic macroinvertebrates communities, the choice of a unique set of environmental
factors that are responsible for benthic distribution has still some degree of controversy (Lindegarth and Hoskin, 2001; Edgar and Barrett, 2002; Thrush et al., 2005). Nevertheless, several variables are of recognised relevance such as sediment grain size (Teske and Wooldridge, 2003; Ysebaert et al., 2003; Anderson et al., 2004; Hirst and Kilpatrick, 2007; Anderson, 2008), organic matter content (Magni et al., 2009), salinity (Attrill, 2002; Teske and Wooldridge, 2003; Giberto et al., 2004) and hydrodynamic variability (Thrush et al., 2005). With this knowledge in mind, tools are being developed and applied on the basis of establishing a reference condition allowing having some measure of community structure deviation due to the impact of human activities.
The final objective of this environmental management is thus to protect the structure and function of communities and ecosystems (Ippolito et al., 2010). This implies a course of action for systems and their communities that have already lost their ecological integrity or, are considered at risk. Here, vulnerability assessment becomes an important component of environmental management (Green and McFadden, 2007). This approach helps not only to define protection targets, but also, it contributes to understanding the ways in which particular threats affect ecosystems, setting priorities to the most important or more manageable threats (De Lange et al., 2010; Halpern et al., 2007).
Management tools recently proposed still need further development and are, at this point, being the focus of an important scientific effort. Still, almost all studies regarding it have focused on large estuarine systems that have, in general, large urban and well-industrialized areas with known anthropogenic pressures. Small estuaries have received little management and scientific attention since they are often excluded from priorities derived from different legal frameworks (in particular the WFD).
Small estuarine systems have particular features such as small mouth openings, sometimes with sand barriers that can seasonally close their connection to the sea, freshwater inflows mainly dependent on the rainfall regime, which can lead to even larger fluctuations in the physical environment when compared to larger systems. Hence these estuarine habitats are often more influenced by physical rather than biological variables (Riddin and Adams, 2008) where a single disturbance event can affect a relatively large proportion of the system, making
the achievement of an equilibrium state unlikely (Strugel, 1991). Such features also increase their vulnerability to relatively small anthropogenic influence.
A direct consequence of the necessary displacement of scientific efforts is the lack of fundamental information on biological communities of small estuarine systems, their actual ecological integrity and the main measures to apply, if necessary, to prevent systems deterioration and allow their environmental management.
Aims and importance of the thesis
The Portuguese southwest coast is recognized as one of the least disturbed coastlines of southern Europe, with a very important role in the life cycle of several species (Magalhães et al., 1987) and comprising several small estuarine systems. Yet, knowledge on these systems is scarce and their relative importance and actual ecological status are still unknown. This work aims to contribute to the actual knowledge of small estuarine systems of the Portuguese south and south-western coasts enhancing their ecological relevance. Fish and benthic macroinvertebrates community structures and patterns of distribution of five small estuaries (Mira, Odeceixe, Aljezur, Bensafrim and Gilão estuaries) are analysed. This allows an important step for management purposes which is the application of current tools of ecological integrity analyses. Thus, following the main goal of environmental management, a contribution is made to the establishment of priority measures in order to maintain the ecological function and ecosystem services of these small estuaries.
The main objectives of the present thesis are therefore:
1- Contribute to the actual knowledge on five small estuarine systems of the Portuguese south and southwest coasts;
2- Establish their functional importance;
3- Assess their ecological quality status through the application of tools developed on the scope of the Water Framework Directive;
4- Assess the actual vulnerability of the subject systems, establishing priority measures to their maintenance.
Thesis outline
This thesis comprises five scientific papers published or in review in peer reviewed international journals and it is organized in five parts. The present part (Part 1, Chapter 1) comprises a general introduction and presents the aims and importance of the study and the structure of the thesis.
Part 2, subdivided in two chapters, gives an ecological characterization of the estuarine studied systems, analysing their ecological role based on fish communities (Chapter 2) and exploring macroinvertebrate communities’ characterisation and patterns of distribution (Chapter 3).
Part 3, also divided in two chapters, presents an approach to the ecological quality assessment of the estuarine systems using the tools developed within the scope of the Water Framework Directive, based on fish and benthic macroinvertebrate communities (Chapters 4 and 5, respectively).
Part 4, with one chapter (Chapter 6) presents a vulnerability assessment of the five studied estuarine systems, exploring the main drivers of Human impact for each system and inferring on mitigating measures for achieving/maintaining the systems functional integrity.
Part 5 comprises a general discussion of the main results and the final considerations obtained in the present thesis.
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Ecological Characterization of Small Estuaries Based on Fish and
Macroinvertebrate Communities: A Functional Approach.
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Fish assemblages of small estuaries of the Portuguese coast: a functional approach Inês Cardosoª, Susana Françaª, Miguel Pessanha Paisª, Sofia Henriquesª, Luis Cancela da Fonsecaª,b,c , Henrique N. Cabralª,d
ªCentro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal.
bFaculdade de Ciências do Mar e Ambiente, Universidade do Algarve, Campus de Gambelas,
8005-139 Faro, Portugal.
cLaboratório Marítimo da Guia / Centro de Oceanografia (FCUL), Av. N. Sra. do Cabo, 939,
2750-374, Portugal.
dCentro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo
Grande, 1749-016 Lisboa, Portugal
Fish assemblages of small estuaries of the Portuguese coast:
A functional approach
Abstract
The importance of estuaries for coastal environments is widely acknowledged. Their role, structure and ecological status have been the focus of recent scientific efforts mainly concerning large estuarine areas. In this work we used fish assemblages to establish, for the first time, the functional and ecological role of five small estuarine systems along the Portuguese south and southwest coasts. Our results showed that, at a functional approach, fish communities did not differ between estuaries, and that all systems presented a seasonal pattern in diversity values, ecological and feeding guilds. These small estuaries contribute to the support of coastal fish populations by providing temporary habitats to the critical life stages of marine species, shelter and feeding grounds, and should be considered in an ecological and conservation perspective.
Key-words: Small estuaries, estuarine use, estuarine fish, Portuguese coast
1. Introduction
The importance of estuarine environments is widely accepted among scientists and decision makers as these systems are among the most productive and valuable ecosystems on Earth, with a vital role for coastal communities (Costanza et al., 1997; European Council Directive, 2000). In the past decade, several tools have been developed and widely used in response to the growing demand for establishing the ecological status of these systems. In the European context, the Water Framework Directive (WFD) represents an international commitment to assess the ecological status of transitional waters, being fish communities a key biological element for monitoring purposes (European Council Directive, 2000). In Portugal, as in other coastal countries, growing efforts to improve our knowledge on these ecosystems, particularly the structure and dynamics of their fish communities, have already underlined their importance to commercially important marine fish species as nursery and feeding grounds (e.g. Cabral et al., 2007; Martinho et al., 2007; Vasconcelos et al., 2010). Simultaneously, the degree of anthropogenic pressure in these estuaries and its possible influence on fish assemblages has also been addressed (Vasconcelos et al., 2010). Nevertheless, most studies have focused on large estuarine systems, which have, in general, large urban and well industrialized areas with known anthropogenic pressures. Small estuaries have received less
management and scientific efforts since they are often excluded from priorities derived from different legal frameworks (in particular the WFD).
Small estuarine systems have particular features such as small mouth openings, sometimes with sand barriers that can seasonally close their connection to the sea, and freshwater inflows mainly dependent on rainfall regime that can lead to large fluctuations in the physical environment. Hence these estuarine habitats are more influenced by physical rather than biological variables (Riddin and Adams, 2008). Such features increase their vulnerability to relatively small anthropogenic influence. In our days, former temporarily open/closed estuaries are almost permanently open systems but still with small river catchments, which make them sensitive to changing inflow conditions caused by anthropogenic activities such as sewage effluent discharges (Lawrie et al., 2010). Although there is no guidance in the WFD with regard to the minimal size of transitional water bodies to be included in monitoring programmes, in Portugal, small estuarine systems have been mostly excluded.
Because species diversity is related to estuarine system size (Harrison and Whitfield, 2006; Selleslagh et al., 2009; Nicolas et al., 2010a,b), inferences can be made concerning the low diversity of small estuarine systems, as their morphological and abiotic features lead to low habitat availability for fish assemblages (Whitfield, 1999; Harrison and Whitfield, 2006). Nevertheless, these estuaries may present rare pristine ecological conditions, since many are located in areas with low anthropogenic pressure (Selleslagh and Amara, 2008).
Several environmental factors, in addition to habitat availability, contribute to fish assemblage structure: salinity, current velocity, temperature and oxygen concentrations in different spatial and temporal scales (Thiel et al., 1995; Methven et al., 2001). Seasonal patterns that characterize species composition are also strongly influenced by biotic factors such as migrations and recruitment patterns (Maes et al., 2004) and it is already known that these assemblages may, to some degree, respond to anthropogenic pressure (e.g. Deegan et al., 1997; Harrison and Whitfield, 2006; Coates et al., 2007).
The Portuguese SW coast is recognized as one of the least disturbed coastlines of southern Europe, with a very important role in the life cycle of several species (Magalhães et al., 1987) and comprising several small estuarine systems. Yet, knowledge on these systems is scarce, their relative importance and actual ecological status are still unknown. The need for some comparison bases between estuarine systems led to the approach based on functional guilds of fish communities
(Elliott and Dewailly, 1995), in which the structure of the estuarine ecosystem is reflected (Franco et al., 2008). In this work, we used this approach on fish assemblages to establish, for the first time, the functional and ecological role of five small estuarine systems on the Portuguese south and southwest coasts, in order to understand if small estuarine systems have similar ecological relevance for fish communities, when compared to large systems.
2. Material and methods 2.1. Study areas
Five small estuarine systems located on the Portuguese coast were sampled: Mira, Odeceixe and Aljezur (on the southwest coast) Gilão and Bensafrim (on the south coast) (Fig. 1).
Figure 1- Map of Portugal showing the location of the five estuarine systems studied: Mira, Odeceixe, Aljezur, Bensafrim and Gilão. Sectors in which sampling took place (A, B and C) are shown for each estuary.
The Mira estuary is located in the protected area of Parque Natural do Sudoeste Alentejano e Costa Vicentina (PNSACV). This system was already considered as the less impacted estuary of the Portuguese coast, when compared to larger ones (Vasconcelos et al., 2007) and it is the largest system in the present work, being 30 km long, with a mouth opening of 100 m. The Odeceixe and the Aljezur estuaries, also included in PNSACV, have extensions of 6 km and 7 km, respectively, and both have mouth openings of 50 m. These two systems are located in areas with small villages with a low number of inhabitants. The Bensafrim and the Gilão estuaries are 4 km and 6 km long and have mouth openings of 65 m and 150 m, respectively. These estuaries are located near cities, in areas in which tourism is the main industry, with high seasonal population fluctuations and with unknown sewage loadings. River flow into all estuaries is mainly torrential, directly dependent on rainfall, influencing the spatial and temporal salinity regime.
2.2. Sampling
In each system, three equivalent sectors were defined in order to include the complete potential tide and salinity range of each system: sector A, near to the estuary mouth; sector B, intermediate, and sector C, in the upper part of the estuary with a lower marine influence. With the exception of the Mira estuary, the upstream limit of sector C was mainly defined by navigability range. Sampling was conducted seasonally (spring, summer, autumn and winter), between April 2009 and February 2010. Fish sampling was performed with a beach seine net (with 40 m length, and 1 cm of mesh size) operated from a small boat. Three replicates were done in each sector of each estuary, per season. All individuals caught were preserved in ice and identified and counted at the laboratory.
2.3. Data analyses
Species richness (S) (total number of species), Pielou’s evenness (J) and Shannon-Wiener’s (H') diversity indices were calculated for each estuary per season and over all seasons.
Cluster analysis, using the Bray-Curtis similarity measure, was used to determine similarity between estuarine assemblages based on species presence/absence data regardless of season, using PRIMER 5 software.
Species were classified by functional groups according to Elliott and Dewailly (1995). Each species was assigned to an ecological and to a feeding guild. The ecological guilds contained truly
estuarine resident species (ER), marine adventitious visitors (MA), diadromous (catadromous/anadromous) migrants (CA), marine seasonal migrants (MS), marine juvenile migrants (MJ) and freshwater adventitious visitors (FW). The feeding guilds considered were strictly planktivorous (PS), strictly invertebrate feeders (IS), strictly picivorous (FS), feeding on invertebrates and fishes (IF), carnivorous other than PS, IS, FS or IF (CS), omnivorous (OV) and other herbivorous/carnivorous (HC). Ecological and feeding guilds were analysed both by number of species and number of individuals within each guild. The percentage contribution of each functional category to the total species richness and species abundance was calculated for each estuary and season, and compared to assess the prevailing function of each system during the time period of the present study. Multiple and pairwise differences were tested by non-parametric statistics (Kruskall-Wallis and Mann Whitney tests) in R software version 2.11.0.
Canonical Correspondence Analysis (CCA) was performed in order to observe fish abundance variations between estuaries and seasons, using tide range, salinity, average depth, mouth opening and river flow as explaining variables, using species abundance data for the four seasons. Only species that occurred in more than three samples were included, values were transformed with the Log (x+1) function. For this analysis R software version 2.11.0 was used (package ca).
3. Results
A total of 4450 fish belonging to 11 families and 22 species were caught in the five studied estuaries (Table 1). Mira and Aljezur estuaries were the most diverse systems with higher species richness (S) (16 and 15 respectively) (Table 1). Mira showed a higher Shannon-Wiener’s index value (H=1.6) and higher equitability (J’=0.6). Bensafrim was the system with the lowest diversity.
Table 1- Mean density of individuals per 1000 m2 in Mira, Odeceixe, Aljezur, Bensafrim and Gilão estuaries. Species were assigned to an ecological guild (EG): estuarine resident species (ER), marine adventitious visitors (MA), diadromous (catadromous/anadromous) migrants (CA), marine seasonal migrants (MS) and marine juvenile’s migrants (MJ) and to a feeding guild (FG): strictly planktivorous (PS), strictly invertebrate feeders (IS), strictly picivorous (FS), feeding on invertebrates and fishes (IF), carnivorous (CS) other than PS, IS, FS or IF. herbivorous/carnivorous (HC) but not omnivorous (OV). Values for total species richness (S), Pielou’s evenness (J) and Shannon-Wiener’s (H') diversity indices are also presented.
Species EG FG Mira Odeceixe Aljezur Bensafrim Gilão
Clupeidae Alosa fallax CA PS 1.74 Anguillidae Anguilla anguilla CA OV 0.22 0.22 0.31 Atherinidae Atherina boyeri ER CS 5.67 3.27 Atherina presbyter MJ IF 8.50 7.85 28.13 11.78 75.88 Mugilidae Chelon labrosus MS CS 1.31 1.31 0.44 0.44 Liza aurata MS OV 3.05 14.39 7.41 13.96 0.44 Liza ramada CA OV 3.71 5.45 5.02 9.59 1.09 Liza spp. 7.63 31.62 Moronidae Dicentrarchus labrax MJ IF 0.22 5.89 6.32 25.73 3.49 Dicentrarchus puntactus MJ IF 0.87 Sparidae Diplodus bellotti MJ HC 0.22 Diplodus sargus MJ HC 10.90 0.22 2.62 34.23 0.44 Diplodus vulgaris MJ HC 3.27 1.09 7.20 Sarpa salpa MA HC 0.44 Sparus aurata MJ IS 0.87 2.40 3.05 1.09 0.65 Diplodus spp. MJ HC 0.22 1.96 Engraulidae Engraulis encrasicolus MS PS 42.96 2.18 Gobiidae Gobius niger ER IF 0.22 Pomatoschistus microps ER IS 56.48 88.97 119.06 290.01 8.07 Pomatoschistus minutos ER IS 1.09 Batrachoididae Halobatrachus didactylus MS IS 0.22 Syngnathidae Singnathus acus ER IF 0.22 0.87 Soleidae Solea senegalensis MJ IS 1.53 1.09 0.22 Solea solea MJ IS 0.22 0.44 0.22 S 16 13 15 12 12 H' 1.6 1.3 1.3 1.0 1.3 J' 0.6 0.5 0.5 0.4 0.5
Cluster analysis using species presence/absence data from all estuaries, showed two clear separate groups, one composed by Gilão and Bensafrim estuaries, from the south coast, and a second one including all the systems from the southwest coast (Mira, Aljezur and Odeceixe). Within the southwest group, Odeceixe and Aljezur were clustered at 80% Bray-Curtis similarity (Fig. 2).
Figure 2- Cluster analysis of species presence/absence data for the five sampled estuaries using Bray-Curtis similarity.
Five ecological guilds were identified in each of the selected systems (Fig. 3a, b). Analysing ecological guilds by number of species within each guild, from the 22 species identified in the present study, five were estuarine resident (ER) (Atherina boyeri, Pomatoschistus microps, Pomatoschistus minutus, Syngnathus acus, and Gobius niger), but only at Aljezur it was possible to capture individuals of four resident species. At Odeceixe three species of ER were caught, at Mira, Bensafrim and Gilão estuaries individuals of two and one ER species were captured respectively (Table 1).
In terms of species contribution for each guild, no differences were found between systems. On average, marine juveniles (MJ) represented up to 38% of the number of species caught, estuarine residents (ER) represented 26%, marine seasonal migrants (MS) represented 18% of overall species, diadromous migrants (CA) represented 13% and marine adventitious visitors were represented by 6% of species. In terms of abundance contribution for each guild, no significant differences were found. Nevertheless, Gilão showed contrasting proportions of CA and MJ individuals and lower proportions of ER individuals when compared with the other estuarine systems (Fig. 3b).
Six feeding guilds were identified in this work (Table 1), but only in Mira and Aljezur all the guilds were represented. Analysing species distribution by feeding guilds, Mira and Aljezur estuaries were the most diverse systems (Fig. 3c), followed by Odeceixe, Bensafrim and Gilão in decreasing order of diversity. Significant differences between estuaries were found for species feeding on invertebrates and fishes (IF) and strictly planktivorous (PS). Significant differences in IF species contributions were between Mira and Odeceixe, Aljezur and Gilão (W=0; p<0.05, W=16; p<0.05, W=16; p<0.05
respectively) and between Bensafrim and Gilão (W=0.5; p<0.05). Mira estuary had the lowest contribution of IF species. Planktivorous fish were only caught in Mira and Aljezur estuaries. For the remaining feeding guilds no significant differences were found, with OV representing 29%, IS representing 24%, HC representing 14% and CS representing 8% of the caught species, on average. When analysing the number of individuals, Gilão stands out from Mira, Odeceixe and Bensafrim estuaries due to the dominance of species feeding on invertebrates and fishes (IF) (W=16, p<0.05; W=16, p<0.05; W=0, p<0.05, respectively), which corresponded to 60% of the individuals caught (Fig. 3d).
Figure 3- Percentage of Ecological and Feeding Guilds for each estuary by species composition: a), c) and % of individuals: b), d) respectively. Ecological Guilds - estuarine resident species (ER), marine adventitious visitors (MA), diadromous (catadromous/anadromous) migrants (CA), marine seasonal migrants (MS) and marine juvenile’s migrants (MJ); Feeding Guilds - strictly planktivorous (PS), strictly invertebrate feeders (IS), strictly piscivorous (FS), feeding on invertebrates and fishes (IF), carnivorous (CS) other than PS, IS, FS or IF.
All systems presented a seasonal pattern in diversity values (Fig. 4), ecological and feeding guilds (Fig. 5). Summer and autumn were the most diverse seasons. Seasonal fluctuations in the contribution of different ecological guilds were found both with the number of species and the number of individuals. For ER species, winter was differentiated from spring, summer and autumn (W=1, p<0.05; W=0, p<0.05 and W=0, p<0.05 respectively). For MJ species, winter differentiated from spring, summer and autumn (W=24, p<0.05; W=25, p<0.05 and W=25, p<0.05 respectively) with less contribution of MJ and higher contribution of ER species (Fig. 5a). Fluctuations concerning individuals’ percentage contribution occurred essentially within CA and MA guilds. CA individuals had
higher contribution during autumn (W=25, p<0.05) and MA during summer and autumn (W=25, p<0.05 and W=22,5 p<0.05 respectively) (Fig. 5b).
Figure 4- Seasonal variation of species richness (S), Pielou’s evenness (J) and Shannon-Wiener’s (H’) diversity indices for each estuary.
Figure 5- Seasonal percentage of Ecological and Feeding Guilds for each estuary by species composition: a), c) and % of individuals: b), d) respectively. Ecological Guilds - estuarine resident species (ER), marine adventitious visitors (MA), diadromous (catadromous/anadromous) migrants (CA), marine seasonal migrants (MS) and marine juvenile’s migrants (MJ); Feeding Guilds - strictly planktivorous (PS), strictly invertebrate feeders (IS), strictly piscivorous (FS), feeding on invertebrates and fishes (IF), carnivorous (CS) other than PS, IS, FS or IF.
The CCA performed to explore variations in fish assemblages among estuaries and seasons using environmental variables, accounted for 54% of total variation on the first two dimensions. Figure 6 shows that fish assemblages presented a clear seasonal variation. Winter assemblages of all estuaries were similar, disposed at one end of the gradient, characterized mainly by higher abundances of resident species (P. microps, S. acus and A. boyeri). Fish assemblages from spring to autumn, positioned at the mid-gradient, are characterised by a higher number of species. The proximity between systems assemblages is explained by the relative abundance of individuals. The only exception is the Gilão fish assemblage, which deviates from this seasonal pattern, mainly because of the constant presence of A. presbyter along the sampling period. Overall, it was observed that seasonal variations overlap environmental features, with Mira estuary reaching the maximum values of all the environmental variables.
% o f sp e ci e s a) b) % o f sp e ci e s c) % o f in d iv id u a ls d)
Figure 6- Ordination diagram of the first two axes of canonical correspondence analysis (CCA) based on fish assemblages of the five studied estuaries considering species abundance per estuary and season and the environmental features river flow (Rflow), tide range (Trange), salinity (Sal) and average depth (Depth). Name of estuaries are abbreviated by their first two letters: Al (Aljezur), Be (Bensafrim), Gi (Gilão), Mi (Mira), Od (Odeceixe). Sampled seasons are abbreviated by their first four letters: Winter (Wint), Spring (Spri), Summer (Summ), Autumn (Autu).
4. Discussion
The main goal of this work was to fill in the knowledge gap concerning fish assemblage structure and ecosystem function of small estuaries from the Portuguese coast. Although the ecosystem function can be a holistic approach, which may include all system functional compartments, the present work focused on fish assemblage structure as an indicator of system ecological relevance. This approach was made in light of previously published works that set fish assemblages as useful ecological indicators (e.g. Lobry et al., 2003; Franco et al., 2008).
The sampling effort and methodology were established to observe species composition along seasons. An attempt was made to cover the whole salinity range of the studied systems with the
objective of including all possible estuarine habitats at the ecosystem scale. The species distribution along the salinity gradient was already established by several authors (e.g. Thiel et al., 1995; Selleslagh and Amara, 2008; Selleslagh et al., 2009). In very small systems, with small mouth openings that can periodically be closed, such as the ones focused by this work, the expected salinity gradient can be interrupted with hypersaline areas, that can lead to a local and punctual gradient inversion (Potter et al., 2010). This was the case during our sampling period and intra-estuary sectors based on salinity range were discharged. Temporal gradient and variations in fish assemblage composition were set as the main subjects in whom patterns were to be found. Maes et al. (2004) already supported that strong seasonal variations in estuarine assemblages occur independently of environmental conditions within the estuary, and those variations will be more dependent on recruitment patterns of marine and estuarine species.
The five estuarine systems studied in this work differ from each other, in terms of coastal disposition, anthropogenic pressure and abiotic conditions. In fact, as stated by Whitfield (1999), no two estuaries are identical but if fishes respond to the environment in a consistent manner, then the communities occupying similar types of estuaries in a particular region would be expected to reflect this similarity (Whitfield, 1999; Harrisson and Whitfield, 2006). In light of this, and regarding the pressure levels, coastal disposition and the adjacent environment conditions, it could be expected that Bensafrim and Gilão would be set apart from Aljezur, Odeceixe and Mira in terms of fish assemblage composition and that the Mira estuary would be set apart from Aljezur and Odeceixe, not only because of system size, but also as a consequence of anthropogenic uses and pressures.
Our results are in agreement with this premise. In terms of diversity and species assemblage composition, Mira, Aljezur and Odeceixe estuaries have higher similarity than Bensafrim and Gilão as illustrated by the results of the cluster analysis. Two main gradients can be responsible for the separation of this group, namely coastal disposition and anthropogenic pressure, since Bensafrim and Gilão are located on the Algarve’s south coast, where tourism is the main industry with still unknown loadings but with high levels of expected anthropogenic pressures. Despite the similarity between the fish assemblage of the Mira estuary and those of Aljezur and Odeceixe, diversity was higher in the first. This concurs with the fact that the Mira estuary is by far the largest system and that system size can directly influence estuarine fish assemblages (e.g. Harrison and Whifield, 2006; Selleslagh and Amara, 2008; Sellesagh et al., 2009; Nicolas et al., 2010a).
Fish assemblages of the studied estuaries were dominated by a small number of species, the majority of which were occasional or rare, which is a common pattern observed in other systems around the world (Cabral et al., 2001; Akin et al., 2005; Maes et al., 2005; Elliott et al., 2007).
In terms of ecological and feeding guilds, our results demonstrate that these five systems have some resemblance with what was considered by Elliott and Dewailly (1995) as the typical European estuarine fish assemblage. Marine juveniles (MJ) and estuarine residents (ER) were within the group that dominated fish communities but marine adventitious (MA) were replaced by marine seasonal migrants (MS). With respect to the feeding guilds, an overall dominance of taxa feeding on both invertebrates and fishes (IF), or only on invertebrates (IS) was observed. Nevertheless, we found different guild proportions in number of species, which can be explained by the short time period of the present work and by the sampling procedure. Most of the available data involving comparison and assemblage characterization are based on large temporal series of collections with beam trawl (Elliott and Dewailly, 1995; Lobry et al., 2003; Thiel et al., 2003). For this reason, some bias has to be assumed, and a continuous sampling effort is probably necessary for a more accurate assemblage characterization in terms of guild proportions for the small estuaries studied in this work. In addition, the low habitat diversity, of small estuaries may lead to a different fish assemblage structure (Mathieson et al., 2000).
Although estuarine resident (ER) species dominated in terms of abundance, they were represented only by five of the 22 identified species caught in the present study. This smaller representativity of the ER species, in contrast with the high number of MJ species (10), can be observed in other European estuarine systems, with contrasting system dimensions such as Tejo (Costa et al., 2007; Neves et al., 2008) and with similar dimensions such as the French estuaries of Canche, Authie and Somme (Selleslagh et al., 2009). This fact can be evidence that, as observed in other estuaries, the five systems studied are mostly used as temporary habitat by fish, as feeding and shelter grounds. Although the number of marine juvenile species was similar when compared the above cited works, we didn’t find peaks of MJ individuals that are consistent with the nursery function of an estuary system (Vasconcelos et al., 2010).
Throughout this study, seasonal variations were found in all of the approaches used to analyse fish assemblages: diversity, species compositions, ecological and feeding guild distribution. Overall, the low diversity found in winter contrasted with the growing diversity from spring until autumn.
Estuarine resident species had higher relative abundances in winter and species that use estuaries as potential nursery and feeding grounds had higher relative abundances in summer and autumn. A similar seasonal pattern was observed in other studies (e.g. Blaber and Blaber, 1980; Gordo and Cabral, 2001; Pombo and Elliott, 2007; França et al., 2008; Selleslagh and Amara, 2008). Nevertheless, in our study, higher diversity values and relative abundance of MJ species were more evident in summer than in spring for all estuaries. In this case some inter-annual stochasticity may be involved, but an extension of the sampling period would be needed to make further inferences. This seasonal pattern allows to assess the use of these small estuaries as contributors to the support of coastal fish populations, by containing temporary habitats that provide shelter and feeding grounds to the critical life stages of marine species.
The overall resemblance among estuaries in the proportion of ecological guilds pointed out that the functional structures are probably more influenced by each systems ecological and abiotic conditions rather than system size. Here we will have to consider that the Mira estuary, with a contrasting large dimension when compared to Aljezur and Odeceixe, can have an undervalued fish assemblage in this study, which can be forcing a fish assemblage structure similarity.
Our results showed that, despite the low diversity found, which can be related to the systems’ dimension (Harrison and Whifield, 2006; Selleslagh and Amara, 2008; Selleslagh et al., 2009; Nicolas et al., 2010a), these are estuaries that have to be considered at an ecological and conservation perspective. This work suggested their importance as shelter, potential nursery and feeding grounds for commercially important species such as Dicentrarchus labrax, Diplodus sargus and D. vulgaris. In addition, the systems harbour species classified as “threatened” or rare such as Anguilla anguilla and Dicentrarchus punctatus, which increases their ecological value (Costello et al., 2002). When compared to other European estuaries, their relative importance regarding the functional approach does not differ, which should reinforce their natural inclusion on monitoring and conservation efforts.
This work highlighted the important role of small estuarine systems for coastal fish assemblages. Their coastal disposition makes them important shelter zones with potential pristine conditions since some of these systems are located in protected areas with low levels of anthropogenic impact. Because of their dimension and morphological characteristics they may not cover all the ecosystem functions, such as the nursery function, that are recognized as fundamental features of large
estuarine systems. Nevertheless, they have a complementary role which can be vital in large costal extensions.
5. Acknowledgements
The authors wish to thank all the volunteers involved in the field work and Rita Vasconcelos for the revision of the manuscript. This study was founded by the “Fundação para a Ciência e Tecnologia” (PTDC/MAR/64982/2006). Inês Cardoso was founded with a PhD grant by FCT (SFRH / BD / 31261 / 2006).
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Cabral, H.N., Vasconcelos, R., Vinagre, C., França, S., Fonseca, V., Maia, A., Reis-Santos, P., Lopes, M., Campos, J., Freitas, V., Santos, P.T., Costa, M.J., 2007. Relative importance of estuarine flatfish nurseries along the Portuguese coast. Journal of Sea Research 57, 209–217.
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