doctoral dissertation in biology (especialidade biologia...

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

À minha Mãe e ao meu Pai.

TABLE OF CONTENTS

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

AGRADECIMENTOS 161

ABSTRACT AND KEY WORDS

9

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

11

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

13

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

RESUMO ALARGADO

14

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

RESUMO ALARGADO

15

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.

LIST OF PAPERS

17

LIST OF PAPERS

This 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).

PART 1

Aims and Scope of the Thesis

CHAPTER 1

General introduction, Aims and importance of the thesis and Thesis

outline

CHAPTER 1

23

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.

PART 1

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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

CHAPTER 1

25

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

PART 1

26

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.

CHAPTER 1

27

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.

PART 1

28

Literature cited

Anderson, M.J., Ford, R.B., Feary, D.A., Hoeywill, C., 2004. Quantitative measures of

sedimentation in an estuarine system and its relationship with intertidal soft-sediment infauna.

Marine Ecology Progress Series 272, 33–48.

Anderson, M., 2008. Animal-sediment relationships re-visited: Characterising species’

distributions along an environmental gradient using canonical analysis and quantile regression

splines. Journal of Experimental Marine Biology and Ecology 366, 16–27.

Attrill, M., 2002. A testable linear model for diversity trends in estuaries. Journal of Animal

Ecology 71, 262–269.

Barbier, E., Hacke, S.D., Kennedy, C., Koch, E.W., Stier, A.C., Sillima, B.R., 2011. The

value of estuarine and coastal ecosystem services. Ecological Monographs 81, 169–193.

Borja, A., Galparsoro, I., Solaun, O., Muxika, I., Tello, E., Uriarte, A., Valência, V., 2006.

The European Water Framework Directive and the DPSIR, a methodological approach to

assess the risk of failing to achieve good ecological status. Estuarine Coastal and Shelf Science

66, 84–96.

Costanza, R., Mageau, M., 1999. What is a healthy ecosystem? Aquatic Ecology 33, 105–

115.

Costanza, R., Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K.,

Naeems, S., O’Neill, R.V., Paruelo, J., Raskin, R.G., Sutton, P. van den Belt, M., 1997. The

value of the world’s ecosystem services and natural capital. Nature 387, 253–260.

Dauvin, J., Ruellet, T., Desroy, N., Janson, A., 2007. The ecological quality status of the

Bay of Seine and the Seine estuary: use of biotic indices. Marine Pollution Bulletin 55, 241–257.

De Lange, H.J., Sala, S., Vighi, M., Faber, J.H., 2010. Ecological vulnerability in risk

assessment - a review and perspectives. Science of the Total Environment 408, 3871–3879.

European Council Directive, 2000. Establishing a framework for community action in the

field of water policy. Directive 200/60/EC of the European Parliament and of the Council. Official

Journal of European Community L 327, 1–72.

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Edgar, G.J., Barrett, N.S., 2002. Benthic macrofauna in Tasmanian estuaries: scales of

distribution and relationships with environmental variables. Journal of Experimental Marine

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PART 2

Ecological Characterization of Small Estuaries Based on Fish and

Macroinvertebrate Communities: A Functional Approach.

CHAPTER 2

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

Estuarine, Coastal and Shelf Science (2011) 93, 40–46.

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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


38

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

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39

(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.


40

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

CHAPTER 2

41

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.


42

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).

CHAPTER 2

43

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


44

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

CHAPTER 2

45

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.


46

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

eci

es

a)

b)

% o

f sp

eci

es

c)

% o

f in

div

idu

als

d)

CHAPTER 2

47

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


48

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).

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49

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.


50

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

CHAPTER 2

51

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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structuring the fish community. Journal of Fish Biology 46, 47–69.

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CHAPTER 3

Distribution patterns of benthic macroinvertebrate assemblages in small estuaries of the

Portuguese coast.

Inês Cardosoª, Luís Cancela da Fonsecab,c

, Henrique N. Cabralª



bCentro de Ciências e Tecnologias da Água, Universidade do Algarve, Campus de Gambelas,


cCentro de Oceanografia, Laboratório Marítimo da Guia, Faculdade de Ciências da

Universidade de Lisboa, Av. Nossa Senhora. do Cabo, 939, 2750-374, Cascais Portugal.

Estuarine, Coastal and Shelf Science. (Submitted)

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59

Distribution patterns of benthic macroinvertebrates assemblages in small

estuaries of the Portuguese coast.

Abstract Benthic macroinvertebrates play a fundamental role in estuarine environments as they are partially responsible for the extremely high productivity of these systems and are frequently used in environmental quality assessment of coastal systems. Understanding the distribution patterns of these communities is of relevant importance for proper differentiation between natural variability and patterns induced by anthropogenic impacts. In this work, we studied benthic communities in five small estuarine systems from the Portuguese South and Southwest coasts in order to establish how sediment composition structures these assemblages between and within systems. We found that at a broader scale of (between systems), sediment components explain the main differences in these communities. Within systems, patterns could not be attributed to sediment heterogeneity. In addition, seasonality, a salinity proxy, didn’t have the same impact in equivalent systems, underlying the complexity of factors that an act at small scales in systems with small dimensions. For monitoring purposes, we conclude that in small systems, community analysis shouldn’t discard species composition as it can provide fundamental information upon system features when available data is scarce. We also conclude, in this context, that sampling procedures must cover as much within system heterogeneity as possible, not only by sampling along estuarine gradients, but also covering the seasonal variation that can be of major importance for some small estuaries.

Keywords: Small estuaries, benthic communities, patterns of distribution, Portuguese coast.

1. Introduction

Benthic macroinvertebrates play a fundamental role in estuarine environments as they are

partially responsible for the extremely high productivity of these systems (Rosenberg, 2001;

Mermillod-Blondin et al., 2003; Doi et al., 2005). Beyond their undisputable ecological

relevance, these communities are frequently used in environmental quality assessment of

coastal systems (Chainho et al., 2008; Pinto et al., 2009; Borja and Tunberg, 2011).

Nevertheless, for the implementation of monitoring plans and the application of ecological

quality assessment tools, the understanding of the distribution patterns of these communities is

of relevant importance for proper differentiation between natural variability and patterns induced

by anthropogenic impacts (Hirst and Kilpatrick, 2007). In fact, benthic communities are highly

variable even at small spatial scales (Morrisey et al., 1992; Edgar and Barrett, 2002; Hirst and

Kilpatrick, 2007).

Distribution patterns of benthic macroinvertebrates assemblages in small estuaries of the Portuguese coast.

60

Besides the patchy distribution of these assemblages (Morrisey et al., 1992), several

environmental forces strongly influence the spatial structuring of estuarine macrobenthic

communities (Anderson et al., 2004). Although 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), 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), average salinity (Attrill, 2002; Teske and

Wooldridge, 2003; Giberto et al., 2004) and hydrodynamic variability (Thrush et al., 2005).

Knowledge of the patterns of distribution within the estuary is a crucial basis for further

comparisons between estuaries (Hirst and Kilpatrick, 2007). These patterns must act as the

community’s response to the environment and, because scales of observation can influence the

description of patterns, several temporal and spatial scales have to be considered in order to

reduce the potential mismatch between observations and natural heterogeneity (Levin, 1992).

In small estuarine systems, with small mouth openings, sometimes with sand barriers that

can seasonally close their connection to the sea, and freshwater inflows mainly dependent on

rainfall regime, large fluctuations in the physical environmental are expected (Riddin and

Adams, 2008). These natural fluctuations and their impact on benthic assemblages can act on

several spatial and temporal scales. In addition, environmental gradients may not be as well

structured as in larger systems (Potter et al., 2010). In small estuaries, punctual events of

torrential flow, sediment deposition or salinity gradient inversions may have an important impact

in the establishment of their benthic communities. Despite the known influence of environmental

features on benthic communities, their relative importance in very small systems is still to be

clarified. Benthic assemblages will probably be structured and distributed as a consequence of

a long term succession of events, some of them easily assuming catastrophic proportions, due

to the small size of these systems.

In this work, we studied benthic communities in five small estuarine systems from the

Portuguese south and southwest coasts in order to establish how the main environmental

features mentioned above structure these assemblages. Given the actual need of proper

monitoring programs, and the underlying choice of reference systems, we based the pertinence

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61

of this study on a main question: Is sediment environment a determinant factor for benthic

communities analyses in small estuarine systems?

The Portuguese southwest coast, comprising several small estuarine systems, has an

important ecological role in the life cycle of several coastal species (Magalhães et al., 1987;

Cardoso et al., 2011). Yet, knowledge on these systems and their benthic communities is

scarce. To achieve the goals of the present study, punctual variability of the environmental

features were discarded. Without consistent previous data to support systems’ differentiation,

we chose a sampling methodology capable of characterizing the systems’ potential salinity

range and sediment composition, for all systems at various temporal and spatial scales.

2. Material and Methods

2.1. Study areas

Five small estuarine systems located in the Portuguese coast were sampled: Mira,

Odeceixe and Aljezur (in the southwest coast), Gilão and Bensafrim (in the south coast) (Fig.

1).

The Mira estuary is located in the protected area of Parque Natural do Sudoeste Alentejano

e Costa Vicentina (PNSACV), and was already considered the least impacted estuary of the

Portuguese coast, when compared to larger ones (Vasconcelos et al., 2007). It is 30 km long

with a 100 m wide mouth opening, the largest system in the present work, and has a river flow

of 2.90 m3s-1. Odeceixe and Aljezur estuaries, also included in PNSACV, are 6 km and 7 km

long, with a river flow of 2.84 m3s-1 and 0.97 m3s-1, respectively and both have 50 m wide mouth

openings. These two systems are located in areas with small villages with a low number of

inhabitants. Bensafrim and Gilão estuaries are 4 km and 6 km long, with 65 m and 150 m wide

mouth openings and a river flow of 0.25 m3s-1 and 1.29 m3s-1 respectively. The two latter

estuaries are located near cities, in areas where tourism is the main economical activity, with

high seasonal population fluctuations and unknown sewage loadings. The terminal part of Gilão

is included in a natural park (Parque Natural da Ria Formosa - PNRF).

River flow is mainly torrential in all estuaries, directly dependent on rainfall, and influences

spatial and temporal variations in salinity.


62


2.2. Sampling and laboratory procedures

Benthic samples were collected during winter (January) and summer (June) of 2010. 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 the estuary mouth; sector B, intermediate,

and sector C, in the upper part of the estuary, with a low marine influence. With the exception of

the Mira estuary, the upstream limit of sector C was mainly defined by navigability range (Fig.

1). At each sector, intertidal benthic infauna was sampled using a van Veen grab (sampling

area: 0.05 m2). Three replicates were collected close to each other to minimise inter-sample

variability due to the patchy distribution of benthic communities. After collection, sediment

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63

samples were sieved on a 0.5 mm mesh size, preserved in alcohol (70%) and stained with

Bengal Rose. All animals were identified to the lowest taxonomic level possible and counted.

Additional samples were collected for granulometric and organic matter characterization of

sediment environment at each sector within each estuary. These samples were collected during

the benthic community sampling periods. Additionally, two more sample events were performed

to this characterisation in order to maximise the number of replicates and overcome potential

variability attributed to punctual events. Sediments were dried at 60ºC until constant weight was

achieved. Organic matter content was determined by loss on ignition (4h at 500ºC). Grain-size

analysis was conducted on a series of sieves of different mesh sizes; sediments were divided

into seven fractions, according to the Wentworth scale: silt and clay (<0.063 mm), very fine

sand (0.063 – 0.125 mm), fine sand (0.125 – 0.250 mm), medium sand (0.250 – 0.500 mm),

coarse sand (0.500 – 1.000 mm), very coarse sand (1.000 – 2.000 mm), and gravel (>2.000

mm). After being dried, each fraction retained in each sieve was weighted and expressed as

percentage of total sediment weight.

2.3. Data analyses

Species richness, Shannon-Weiner, Simpson and Pielou indices of diversity and equitability

were calculated for each system and seasons within systems. Habitat diversity was also

calculated based on Shannon-Wiener index for sediment components.

Differences in assemblage’s spatial distribution within and between estuaries were tested

using a nested Permutational Multivariate Analysis of Variance (PERMANOVA), based on

distance matrices as in McArdle and Anderson (2001), considering ‘estuary’, ‘season’ and

‘estuarine sector’ (within each system) as the grouping variables. Tests were based on Bray-

Curtis dissimilarities, calculated among observations for square root transformed macrofaunal

data. Replicates’ data were used instead of averages of species’ abundance. For this analysis

R software version 2.13.0 was used (adonis function from package vegan).

Correlations between estuarine macroinvertebrate assemblages and sediment

characteristics were examined using canonical correlation of principal coordinates with Bray-

Curtis dissimilarity (CAP analysis: Anderson and Willis, 2003; Anderson et al., 2004). Habitat

and species diversity were also included. For this analysis, abundances were averaged and


64

square root transformed. This analysis was also applied, using abundance replicates, to

illustrate significant differences between benthic communities within each estuary, between

sampling seasons and sectors. For this analysis R software version 2.13.0 was used (capscale

function from package vegan).

3. Results

Mira estuary was characterized by a range of finer sediments and it is the system with the

highest percentage of organic matter. Silt and clay fractions dominated at every sector.

Between sectors, differences were mainly found between sector A and C, with an absence of

gravel in A and fine sand in C (Fig. 2). The Odeceixe estuary was characterised by an important

percentage of medium sand, silt and clay fractions, with differences between sectors being

mainly resulting from the larger contribution of coarse sand and gravel at sector C. In Aljezur

estuary, with similar sediment components, sector C was also differentiated with the larger

contribution of gravel and very coarse sands (Fig. 2). On Bensafrim estuary, characterized by

medium sands, sector C differentiated itself by having a higher percentage of silt and clay

fraction and organic matter content (Fig. 2). Finally, Gilão estuary was characterized by coarse

sands, with the larger contribution of medium and finer sands at sectors A and B being

responsible for the differences between sectors. Sector A was also the most enriched with

organic matter (Fig. 2).

A total of 19000 individuals representing 79 taxa were sampled. At the two sampled

seasons, Gilão estuary was the most diverse with 38 taxa, followed by Mira estuary with 28

taxa. In Aljezur and Bensafrim estuaries 21 taxa were collected and in Odeceixe 27 taxa (Table

1).

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65

Figure 2- Sediment granulometric composition and organic matter content for the five estuaries.


66

Table 1- Mean density of individuals per 1 m2 in Mira, Odeceixe, Aljezur, Bensafrim and Gilão estuaries. Values for total species richness (S), Pielou’s evenness (J) and Shannon-Wiener’s (H') diversity indices and species acronyms (Acr) are also presented .

Mira Odeceixe Aljezur Bensafrim Gilão

Acr winter Summer winter Summer winter Summer winter Summer winter Summer

Cnid Cnidaria 2

Nema Nematoda 2 17

Polyc Polychaeta

Aromi Alkmaria romijni 0 11 56 24 79 2

Ccapi Capitella capitata 15 139 53 29 58 51 195 431

Capi Capitellidae 47 4 37

Hfili Heteromastus filiformis 172 82 4 2

Spio Spionidae n.id. 33

Peleg Pygospio elegans 22 136 20 90 88 9

Sshru Streblospio shrubsolii 36 38 172 56 47 4 2720 342

Poly Polydora sp. 2

Hdive Hediste diversicolor 18 16 45 162 397 89 18 511 157 109

Nhomb Nephtys hombergi 108 193

Neph Nephtyidae 2 3

Gconv Glycera convoluta 7

Galba Glycera alba 3

Meli Melinna sp. 6

Amag Amage sp. 2

Aadsp Amage adspersa 22

Eteo Eteone sp. 1

Epict Eteone cf picta 2

Mpapi Magelona papillicornis 18

Neos Neosabellides sp. 133 193 5

Cirr Cirratulidae 4

Onup Onuphis sp. 1

Ofusi Owenia fusiformis 4

Amph Ampharetidae 8

Fenig Ficopomatus enigmaticus 4

Mpapi Magelona papillicornis 1

Tmari Tharyx marioni 13

Scol Scolelepis sp. 15

Chon Chone sp. 1

Olig Oligochaeta 11 76 53 861 504 39

Sipu Sipuncula 4

Crus Crustacea 3

Corie Corophium orientale 11 308 7 17

Cvolu Corophium volutator 13

Gchev Gammarus chevreuxi 3 20 3

Gamm Gammaridae 9

Gamma

Gammaropsis sp. 25

Lpilo Leptocheirus pilosus 2

Mpalm Melita palmata 582

Melit Melitidae 3 0

Mgryl Microdeutopus gryllotalpa 4

Hoers Heterotanais oerstedii 1 20 13

Ccari Cyathura carinata 58 124 763 873 87 564 75 1349 76 1058

Pform Paragnathia formica 3 7 2

Gnat Gnathiidae 10 2

Lhook Lekanesphaera hookeri 2 46 58 68

Peleg Palaemon elegans 15

Upog Upogebiidae 1

Cmaen Carcinus maenas 4 2 2 3

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67

Table 1 (cont.)

Mira estuary assemblages, with an overall higher equitability, were dominated by the

Polychaeta class, which was represented by 15 species with dominance of the capitelidae

Hetromastus filiformis (Table 1). Odeceixe estuary, with the lowest values of equitability, was

dominated by the Crustacea Cyathura carinata and the Gastropoda Hydrobia ulvae in both

sampling seasons (Table 1). Aljezur estuary assemblages were characterised in the winter by

the dominance of the polychaetes Hediste diversicolor and Neosabelides sp., by the crustacean

Corophium orientale and the gastropod Ventrosia ventrosa. Higher densities of Cyathura

carinata characterized summer samples, with a substantial decrease in species abundances.


Acr winter Summer winter Summer winter Summer winter Summer winter Summer

Cope Copepoda 2 2

Ostr Ostracoda 2 4

Molu Mollusca

Hulva Hydrobia ulvae 342 507 469 3 13 1508 2357 27 218

Vvent Ventrosia ventrosa 2 348 18 11 102

Hacut Hydrobia acuta 11 4

Rtrun Retusa truncatula 16

Tell Tellina sp. 2

Tdona Tellina donacina 1

Vene Veneridae 9

Rdecu Tapes decussatus 1

Pseu Pseudopythina sp. 1

Aabra Abra alba 13

Atorn Acteon tornatilis 7

Cera Cerastoderma sp. 63

Cglau Cerastoderma glaucum 14 67 33

Cedul Cerastoderme edule 3 11 7

Card Cardiidae 7

Seme Semelidae 2

Splan Scrobicularia plana 2 89 14 28 4 39 182 2

Briozoa

Mmemb Membranipora membranacea 2

Phor Phoronida 28 4

Neme Nemertinae 2

Inse Insecta 53 1 13 13 78

Quir Quironomidae 2

S 20 15 14 21 15 14 13 15 32 19

H' 2.35 2.07 1.43 1.76 1.99 1.48 1.22 1.62 2.41 1.85

Simpson (1-lambda) 0.87 0.83 0.68 0.73 0.83 0.60 0.59 0.75 0.86 0.79

J' 0.79 0.76 0.54 0.58 0.73 0.56 0.48 0.60 0.69 0.63


68

Bensafrim assemblages were characterised by the dominance of Streblopio shrusbsolii and

Cyathura carinata during the summer, and high densities of Hydrobia ulvae at both sampling

periods (Table 1). Gilão estuary was characterised by Capitela capitata at both sampling

seasons and by high densities of Melita palmata and Cyathura carinata during the summer.

PERMANOVA results allowed to distinguish communities between systems (F=6.49,

p<0.001). And the CAP analysis was able to explain these differences based on the sediment

and diversity parameters considered, with 50% of total variance explained by the first two

components (Fig. 3). In the Mira estuary, characterised by a range of finer sediments and high

content of organic matter, assemblages showed a higher diversity of small polychaetes (Fig. 3).

Odeceixe and Aljezur estuaries, characterised by the presence of all sediment fractions, but

with a strong contribution of silt and clay and medium sand had a larger diversity and

abundance of small crustaceans. In Bensafrim, characterised almost exclusively by medium

sands, assemblages were differentiated from the others mainly due to the dominance of the

spionidea Streblospio shrubsolii and the small gastropod Hydrobia ulvae. Habitat diversity in

terms of sediment components was not related with species diversity at the studied systems

(Fig. 3).

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Figure 3- CAP analysis for the correlation between estuarine macroinvertebrate assemblages and sediment characteristics. Species acronyms are shown in Table 1. Names 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 letter: Winter (W), Summer (S). Shannon-Wiener diversity (H) and habitat diversity are also included in this analysis.

The nested PERMANOVA enabled to distinguish macroinvertebrate assemblages within

systems, between seasons and sectors (F=7.42 and F=2.63 respectively, p<0.001). The CAP

analysis allowed to observe that these two factors have different relative importance in all

systems, with the exception of Bensafrim, where sectors and seasons were not significantly

different (Fig. 4d). We can therefore observe that: in Mira estuary, sectors were better

distinguished during summer, in respect to their macroinvertebrate assemblages (Fig. 4a); in

Odeceixe differentiation between sectors prevails upon seasonality (Fig. 4b); and in Aljezur and

Gilão differentiation between sectors was more pronounced during winter (Figs. 4c, e).


70

Figure 4 - CAP analysis for macroinvertebrate assemblages distributions within estuaries, sectors and sampling season: a) Mira, b) Odeceixe, c) Aljezur, d) Bensafrim, e) Gilão. Species acronyms are shown in Table 1. Names of estuaries are abbreviated by their first letter: M (Mira), O (Odeceixe), A (Aljezur), B (Bensafrim), G (Gilão). Sectors are represented by A, B and C. Sampled seasons are abbreviated by the first letter: Winter (W), Summer (S).

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4. Discussion

In this study we made an attempt to cover the most important features that influence the

distribution patterns of macroinvertebrate assemblages. We characterised sediment with

granulometric and organic matter content; salinity was an underling factor from the two

sampling seasons, winter with high fresh water inflows and summer with higher influence of

tidal currents. Distribution gradients within estuaries were also taken into account, with the

establishment of three sectors along the longitudinal salinity gradient. The five estuarine

systems have shown different benthic assemblage composition, with the dominance of different

species between estuaries. In agreement with previous studies these differences between

systems were well explained by sediment composition and organic matter content (e.g. Meire et

al., 1991; Ysebaert et al., 2003; Anderson et al., 2004; Dethier and Schoco, 2005; Hirst and

Kilpatrick, 2007; Anderson, 2008; Magni et al. 2009).

Although the studied estuaries have necessarily different freshwater inflows, a reflection of

the different watersheds that support them, the amount of variance explained by sediment

components and organic matter content have shown that salinity is probably not the major

factor responsible for the different assemblages found between systems. This is in agreement

with Hirst and Kilpatrick (2007) suggestion that macroinvertebrate assemblage structure is

primarily responding to changes in sediment characteristics, rather than salinity per se.

Nevertheless, communities cannot be considered self-contained entities. Understanding

and being able to distinguish patterns at this level of organisation is not independent from a

close look at the individual species that compose them (Levin, 1992). In fact, when these

patterns exist, they reflect the response of each individual species to the environment and not

simply a generalised community response (Levin, 1992). Hence, we found in the Mira estuary

assemblages that are typical for muddy sediments enriched by organic matter, characterised by

small polychaetes such as Heteromastus filiformis (Warwick and Clarke, 1994; Ysebaert and

Herman, 2002). In Odeceixe and Aljezur we found similar assemblages with not only small

polychaetes such as Capitela capitata, Pygospio elegans and Streblospio shrusbsolii, but also a

clear dominance and diversity of small crustaceans. Although sediment composition

differentiates these two systems from the others, between Odeceixe and Aljezur, differences

may also be due to salinity range. An evidence of this, besides their different river flow, is the


72

presence of two gastropods, Hydrobia ulvae in Odeceixe and Ventrosia ventrosa in Aljezur, that

seem to have different salinity requirements at their larval settlement phase (Grudemo and

André, 2001; Ysearbert and Herman, 2002). Previous work by Magalhães et al. (1987) also

found similar sediment composition between these two systems.

In Bensafrim estuary, characterised mainly by fine grain sand, communities are mainly

dominated by the small opportunistic polychaetes S. shrubsolii, oligochaetes and the gastropod

H. ulvae. The obvious dominance of these taxa is probably not only related with sediment type,

but also with human induced levels of pollution (Sardá and Martin, 1993) that were not reflected

in the organic matter content. In fact, Bensafrim has been reported as the most impacted

system considered in the present study (Cardoso et al., 2011).

In the Gilão estuary, characterised by coarse sediment, the high diversity is probably not

related to granulometry, but can be due to the proximity of the Ria Formosa, a lagunar system

with a previously reported high diversity in macrobenthic communities (Gamito, 2008). This is in

agreement with Dithier and Schoco (2005) who suggested that species diversity is not

independent from adjacent systems and that connectedness can occur via pelagic larval and

current dispersal processes.

In resume, at a broader scale of benthic assemblage comparison (between systems),

sediment components seem to explain the main differences in these communities. At this scale,

seasonal variation and the underling salinity range are not fundamental factors, which is in

agreement with the statement by Johnson et al. (2008) that system differences are greater than

seasonal differences. Nevertheless, we found that even with substantially different sediment

composition, other processes may be responsible for communities’ differences, which are more

directed with species relative dominance than by overall species composition. This is

particularly relevant when there is a clear dominance of indicator species such as S. shrubsolii

for pollution, and H. filiformis for organically enriched environments.

Within estuaries different patterns were found, being weakly explained by sediment

heterogeneity within systems. In opposition to other studies where seasonal variance was much

lower than spatial variance (Edgar and Barrett, 2002), this was not the case for all the estuaries

considered in the present study. Exceptions were Bensafrim, in which communities did not differ

between sectors or sampling seasons, and Odeceixe, where the spatial pattern of distribution

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prevailed upon seasonal variation. In the Mira, Aljezur and Gilão estuaries, seasonal

differentiation seem to be important for the definition of spatial heterogeneity in assemblage

distribution. Furthermore, we found that this spatial heterogeneity in assemblages’ distributions

did not take place on the same season. We acknowledge that sampling procedure can produce

false patterns if replicates are not enough to overcome the patchy distribution of these

assemblages. Nevertheless, this factor per se can not explain the consistent seasonal

heterogeneity of these communities.

For the Mira estuary, spatial heterogeneity was more obvious during summer, which may

be related with the better stratified longitudinal salinity gradient, promoted by low fresh water

inflow and high tidal influence. For Aljezur and Gilão, this heterogeneity between sectors

occurred in winter. In the case of Aljezur the torrential flow of fresh water that occurs during

winter may promote a more permanent and wider connection to the sea and, consequently, a

more effective water renewal and a shorter residence time. In summer, a drastic decrease in

species abundances is probably affecting the capacity to distinguish spatial patterns. This can

be related to an eutrofication process caused by poor water renewal, combined with high levels

of human pressure during this season. Here, the narrow mouth opening and sand barriers can

alter the influence of tidal currents on this estuary with an already reported decrease in

productivity (Costa et al., 1988). At the Gilão estuary we observed the opposite - an increase in

species densities during summer and lower equitability values, probably inducing spatial

heterogeneity. For Odeceixe, results suggest a smaller impact for seasonal heterogeneity in

assemblage distribution, probably because of its higher river flow compared with Aljezur.

With this work we addressed three main scales of distribution: inter and intra-estuarine

patterns, and seasonal heterogeneity. Our results support that at the inter-estuarine scale

sediment composition is a major factor for benthic communities and, in fact, it explained a great

percentage of total variance, which is in agreement with previous studies (e.g. Teske and

Wooldridge, 2003; Gladstone et al., 2006). However, when indicators taxa are present in the

assemblages, one must take into account the importance of other potential driving forces such

as pollution and salinity ranges.

We also conclude that at a smaller scale, sediment composition between sectors of each

estuary is not a major factor driving the distribution of assemblages. Furthermore, the factors


74

that rule benthic distribution are probably not the same in the different systems. In agreement

with the findings of Hewitt and Thrush (2009), our results showed that, within estuarine scales

of distribution, there must be a complex relationship between spatial variability and mean

abundances for species at a variety of spatial and temporal scales that do not represent a

simple power law operating at broader scales.

Both the environmental heterogeneity that occurs within an estuary and factors that vary

between estuaries do affect species-environment relationships (Thrush et al., 2005). As a

consequence, different species may respond to different features in different ways through time

(Levin, 1992; Gladstone et al., 2006). This adds several degrees of complexity to systems’

ecological characterisation. For monitoring purposes, or comparison between the system’s

benthic communities, sampling procedures must cover as much within system heterogeneity as

possible. In the case of the present systems or equivalent ones, this would be achieved not only

by sampling along estuarine gradients, but also covering the seasonal variation that can be of

major importance for some small estuaries.

5. Acknowledgements

The authors wish to thank all the volunteers involved in the field work and Miguel Pessanha

Pais 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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PART 3

Ecological Quality Assessment on Small Estuaries of the Portuguese

South and Southwest Coasts based on Fish and Macroinverterate

Communities.

CHAPTER 4

Ecological quality assessment of small estuaries from the Portuguese coast based on

fish assemblages indices.

Inês Cardosoª, Miguel Pessanha Paisª, Sofia Henriquesª, Luís Cancela da Fonsecab,c

,

Henrique N. Cabralª



bFaculdade de Ciências do Mar e Ambiente, Universidade do Algarve, Campus de Gambelas,


cLaboratório Marítimo da Guia / Centro de Oceanografia (FCUL), Av. N. Sra. do Cabo, 939,

2750-374 Cascais, Portugal.

dCentro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo

Grande, 1749-016 Lisboa, Portugal

Marine Pollution Bulletin (2011) 62, 992 –1001.

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Ecological quality assessment of small estuaries from the Portuguese

coast based on fish assemblages indices.

Abstract The importance of establishing the ecological quality of estuarine systems has been widely acknowledged and led to the development of several fish community-based multimetric indices. Nevertheless, a question rose about the accuracy of these tools when natural disturbance is acting upon the organization the of systems’ communities. Four multimetric indices were used to examine their ability to differentiate the ecological status of five small estuarine systems (southern Portugal), and also to test if they reflected the level of anthropogenic pressures. Fish assemblages from Mira, Odeceixe and Aljezur (in the southwest coast), Gilão and Bensafrim (in the south coast) estuaries were sampled seasonally for one year, and anthropogenic sources of pressure were identified and quantified. We found that although the applied indices provided information on ecological condition differentiation among systems, they are unable to explain different classes of ecological status in systems with equivalent pressure levels.

Key-words: Fish assemblages, small estuaries, ecological integrity, fish based multimetric

indices, Portuguese coast.

1. Introduction

Estuarine ecosystems are among the most valuable in the world because of their high

productivity and their fundamental role concerning ecosystem services (Costanza et al., 1997).

Nevertheless, this widely accepted statement is actually coupled with the knowledge that 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, developed for the European context, which has the final goal of achieving a “good

ecological quality status” for all water bodies by 2015 (European Council Directive, 2000; Borja

et al., 2006). This directive urged the development of consistent tools to assess the ecological

status of estuarine systems.

Ecological quality assessment of small estuaries from the Portuguese coast based on fish assemblages indices.

84

The task of evaluating ecosystems health is far from simple mainly because of the

complexity of the systems, and the consequent articulation of a number of interacting

components. In general, these components 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). 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).

Along with other biological components of aquatic systems, fish-based indicators have been

considered a good way of evaluating the environmental status of the ecosystem (e.g.

Brind’Amour and Lobry, 2010). In this regard, several multimetric indices have been developed

(e.g. Karr, 1991; Deegan et al., 1997; Harrison and Whitfield, 2004, 2006; Breine et al., 2007;

Coats et al., 2007; Breine et al., 2010; Delpech et al., 2010), all attempting to meet the

assumptions that the ideal index would be sensitive to all human-generated stresses exerted on

biological systems, while also having limited sensitivity to natural variation in physical and

biological environments.

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). The difficulty level increases exponentially wherever individual

disturbances are so large that a single disturbance event can affect a relatively large proportion

of the system, making the achievement of an equilibrium state unlikely (Strugel, 1991).

Small estuaries, with low river flow and narrow mouth openings that can periodically be

closed to the sea, are, with this regard, examples of estuarine systems where the achievement

of an ecological equilibrium is probably driven by distinct processes when compared to larger

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85

systems. This sustains that there must be a range of ecosystems that can legitimately be

considered “natural” (Strugel, 1991).

The aim of the present work is to provide information on the ecological integrity of five

scarcely known small estuarine systems of the Portuguese coast. We used the available data

concerning the main driving forces of anthropogenic impacts and also applied a selection of

fish-based multimetric indices to fish community data. We attempted to answer two main

questions: Are the selected estuarine systems at an equivalent ecological integrity status? And

if they differ, are the fish-based multimetric indices reflecting natural or anthropogenic driving

forces?

2. Material and Methods

2.1. Study areas

Five small estuarine systems located in the Portuguese coast were sampled: Mira,

Odeceixe and Aljezur (in the southwest coast), Gilão and Bensafrim (in the south coast) (Fig. 1).

The Mira estuary is located in the protected area of Parque Natural do Sudoeste Alentejano

e Costa Vicentina (PNSACV). This system was already considered the least impacted estuary

of the Portuguese coast, when compared to larger ones (Vasconcelos et al., 2007) and, being

30 km long with a 100 m wide mouth opening, it is the largest system in the present work.

Odeceixe and Aljezur estuaries, also included in PNSACV, are 6 km and 7 km long respectively,

and both have 50 m wide mouth openings. These two systems are located in areas with small

villages with a low number of inhabitants. Bensafrim and Gilão estuaries are 4 km and 6 km

long and have 65 m and 150 m wide mouth openings, respectively. The two latter estuaries are

located near cities, in areas where tourism is the main economical activity, with high seasonal

population fluctuations and unknown sewage loadings. The terminal part of Gilão is included in

a natural park (Parque Natural da Ria Formosa - PNRF).

River flow is mainly torrential in all estuaries, directly dependent on rainfall, and influences

spatial and temporal variations in salinity.


86


2.2. Fish community sampling

In each system, three equivalent sectors were defined in order to cover the entire potential

tide and salinity range of each system: sector A, near 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 between April 2009 and February 2010 (spring, summer,

autumn and winter). Fish sampling was performed with a beach seine net (40 m long, with 1 cm

mesh size) operated from a boat. Three replicates were done per sector, in each estuary and

season. All individuals caught were preserved in ice and identified and counted at the

laboratory.

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2.3. Anthropogenic pressure quantification

In order to quantify the anthropogenic pressures acting on the five systems, we used a

method based on the Environmental Integrative Indicators (EII) approach suggested by Aubry

and Elliott (2006). Although they proposed three groups of potential indicators of disturbance

(Coastline morphologic change, Resources use change and Environmental quality and its

perception), because of the lack of consistent monitoring and institutional data upon the

different systems, we based our analysis on a set of indicators concerning only Resource use

change. The following indicators were quantified: anthropogenically affected coastline,

construction licences (number), % of urban land, % of industrial land, % of land for agricultural

use, population density, water treatment discharges, livestock, aquaculture, intensity of marina

developments capacity, intensity of port developments (number of registered vessels) and

tourism and recreation (% of affected coastline). Data for the time period of this study was

obtained from governmental and public sources (INE), and refer to the surrounding counties.

Expert judgment was applied whenever required, namely for the following indicators:

anthropogenically affected coastline and tourism and recreation. Indicator results were

standardized according to a scoring system ranging from 0 (no resources use) to 9 (very high)

(Table 1). The final score of EII was determined as the arithmetic mean of all indicators scores.

The EII’s classification scheme comprises five classes according to the final score: no

disturbance (0); very low (0<EII<2); low (2!EII<4); medium (4!EII<6); high (6!EII<8) and very

high disturbance (8!EII!9).

2.4. Fish community-based multimetric indices

Four fish community-based multimetric indices were applied to fish community data of the

five estuaries: Estuarine Biotic Index (EBI) (Deegan et al., 1997); Estuarine Fish Community

Index (EFCI) (Harrison and Whitfield, 2004); Transitional Fish Classification Index (TFCI)

(Coates et al., 2007) and AZTI’s Fish Index (AFI) (Uriarte and Borja, 2009). For all indices, and

to allow for the comparison of results among indices, final index results were standardized, i.e.

Relative Ecological Quality values (EQR) were calculated as follows: EQR = sample score /

maximum score possible. Some adaptations to the formulation of the original indices were made

and will be detailed in the following sections.

Table 1- Environmental Integrative Indicators (EII): Resource Use Change after Aubry and Elliott (2006).

No resources use (0) Very low (1) Low (3) Medium (5) High (7) Very High (9)

Antropogenically affected coastline (%) no development <5 !5 and <30 !30 and <60 !60 and <90 !90 Construction licences (number) 0 licenses <60 !60 and <90 !90 and <120 !120 and <150 !150 Water treatment discharges (number) 0 discharge <6 !6 and <9 !9 and <12 !12 and <15 !15 % Urban land no development <1 !1 and <2 !2 and <3 !3 and <4 !4 % Industrial land not applicable <0.1 ! 0.1 and <0.15 ! 0.15 and <0.2 !0.2 and <0.25 !0.25 Population density not applicable <54 !54 and <81 !81 and <108 !108 and <135 !135 % Land for agricultural use not applicable <18 !18 and <27 !27 and <36 !36 and <45 !45

Livestock/ha not applicable <0.1 ! 0.1 and <0.15 !0.15 and <0.2 !0.2 and <0.25 !0.25 Aquaculture no aquaculture <1 ! 1 and <2 !2 and <3 !3 and <4 !4 Intensity of marina developments capacity no marina <180 !180 and <270 !270 and <360 !360 and <450 !450 Intensity of port developments no harbour <30 !30 and <45 !45 and <60 !60 and <75 !75 Tourism and recreation (% of affected coastline) not applicable <10 !10 and <30 !30 and <60 !60 and <90 !90

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2.4.1. Reference Condition

To establish the reference community without comparable data from systems known as not

degraded or least affected, we used the best values obtained for each metric during the period

of the present study in any of the sampled systems (Harrison and Whitfield, 2004, 2006).

Once a reference condition was established, each metric was assessed according to the

extent of its deviation from the reference condition. Whenever the indices’ original thresholds

where not in agreement with our reference community, new thresholds were calculated

following the proposed methodologies for each index and equivalent alterations were made for

every index, in order to permit the comparison of results.

2.4.2. Estuarine Biotic Integrity Index (EBI) (Deegan et al., 1997)

The EBI was developed using data from Warquoi Bay and validated using data from

Buttermilk Bay both in southern Massachusetts (USA), and originally comprised eigth metrics.

All metrics were used in the present study (Table 2), with the exception of that concerning the

proportion of abnormal individuals. Maximum score of the adapted index is 35.

Table 2- Estuarine Biotic Integrity Index (EBI) (Deegan et al., 1997) (N- number; %-percentage).

Metric Scores

0 5

Species Richness (N) <6 !6 Dominance (N) <3 !3 Fish abundance (N) <3.8 !3.8 Nursery species (N) <3 !3

Estuarine spawners (N) <3 !3 Resident species (N) <4 !4 Proportion benthic fishes (%) 0.70 !0.70

2.4.3. Estuarine Fish Community Index (EFCI) (Harrison and Whitfield, 2004)

The EFCI was developed for South African estuaries and accounts for biogeography and

estuary typology, in view of the diversity of system types in South Africa. Different types of

estuaries were considered (small closed estuaries, moderate to large closed estuaries and

predominantly open estuaries) and for each type different thresholds were established for cool-

temperate, warm temperate and subtropical regions. In the present work we used the scoring


90

system for cool-temperate small closed estuaries as a starting point. Metric thresholds were

recalculated based on the present reference condition (Table 3).

Table 3- Estuarine Fish Community Index (EFCI) (Harrison and Whitfield, 2004) (N- Number; %- percentage).

Metrics Scores 5 3 1

Species richness (N) !12 !3 and <7 "7

Rare or threatened species presence absence

Exotic or introduced species absence presence

Species composition (% similarity) !80 >50 and <80 "50

Species abundance (% similarity) !60 >40 and <60 "40

Species that make up 90% of abundance (N) !6 >4 and <6 "4

Estuarine residente species (N) !3 >2 and <3 "2

Estuarine-dependent marine species (N) !7 >4 and <7 "4

Abundance of estuarine 25- 75 !10 and <25 or <10 or >90 resident species (%) >75 and "90

Abundance of estuarine-dependent 25-75 !10 and <25 or <10 or >90 marine species (%) >75 and "90

Benthic invertebrate feeding species (N) !4 >2 and <4 "2

Piscivorous* species (N) !3 >2 and <3 "2

Abundance of benthic invertebrate feeding species (%) !50 >30 and <50 "30

Abundance of piscivorous species*(%) !7 >4 and <7 "4

*species that feed on other fish but not exclusively.

2.4.4. Transitional Fish Classification Index (TFCI) (Coates et al., 2007)

The TFCI was developed for the Thames estuary (UK), and compared to a reference

estuarine fish community derived from data for several estuaries of the same typology as the

Thames. New thresholds were calculated based on the present reference condition, with the

methodology proposed by Coates et al. (2007). Because of the low species diversity in the

presently analysed systems, and to allow for a more accurate differentiation, the metric

“sensitive species” was replaced with “endangered species” (Table 4).

2.4.5. AZTI’s Fish Index (AFI) (Uriarte and Borja, 2009)

This index was proposed for small estuaries in the Basque Country (northern Spain). This

index originally comprises 9 metrics, and in the present analysis the metric concerning fish

health was excluded (Table 5). The maximum score was recalculated to 40. For this index we

used only fish community data.

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Table 4- Transitional Fish Classification Index (TFCI) (Coates et al., 2007) (N- number; %- percentage).

Metrics Scores ________

1 2 3 4 5

Species composition (% similarity) <19.9 20-39.9 40-59.9 60-79.9 80-100 Presence of endangered species absence presence

Species relative abundance (% similarity) <19.9 20-39.9 40-59.9 60-.79.9 80-100 Taxa that make up 90% of the abundance (N) <1.19 1.2-2.39 2.4-3.59 3.6-4.79 !4.8 Estuarine resident species (N) 1 1-1.99 2-2.99 3-3.99 !5

Estuarine-dependent marine species (N) <2.59 2.60-5.19 5.20-7.79 7.80- 10.39 >10.40 Functional guild composition (N) 1 2 3 4 5 Benthic invertebrate feeding species (N) <0.79 0.8-1.59 1.60-2.39 2.40-3.19 >3.20

Piscivorous species (N)* 0.39 0.40-0.79 0.80-1.19 1.20-1.59 >1.60 Feeding guild composition 0 1 2 3 4

*species that feed on other fish but not exclusively.

Table 5- AZTI’s Fish Index (AFI) (Uriarte and Borja, 2009) (N- number; %- percentage).

Metric Scores

1 3 5

Species richness (N) <3 4-9 >9

Pollution indicator species (%) >80 30-80 <30 Introduced species (%) >80 30-80 <30 Flatfish presence (%) <5 5-10 or >60 10-60

Trophic composition (% omnivorous) <1 or >80 1-2.5 or 20-80 2.5-20 Trophic composition (% piscivorous) <5 or >80 5-10 or 50-80 10-50 Estuarine resident (N) <2 2-5 >5

Resident species (%) <5 or >50 5-10 or 40-50 10-40

2.5. Data analyses

Differences in species spatial distribution within and between estuaries were tested using

Permutational Multivariate Analysis of Variance (PERMANOVA) using distance matrices, as in

McArdle and Anderson (2001). The grouping variables were: estuary, season and estuarine

sector (within each system). For this analysis R software version 2.11.0 was used (adonis

function from package vegan).

Concordance between indices along seasonal variation was established based on Kendall’s

coefficient of correlation (#). This correlation coefficient varies between -1 (total disagreement)

and 1 (total agreement), and if the correlation equals zero, the rankings are completely

independent. This analysis was performed in Statistica 9.0.

In order to differentiate ecological ratios within our samples, we performed a k-means

clustering analysis. After data normalization, and based on metrics’ mean values, the analysis of

the mean value of each metric, per cluster was performed. For this analysis, we selected TFCI

and EFCI, for their similarity in included metrics and for their strong dependency on the

reference condition. Estuary and season combinations were considered as samples in the


92

analysis. The appropriate number of clusters was determined by the number of ecological

quality levels obtained with each index and by plotting the variation of the within groups sum of

squares with increasing number of clusters. Results of this non-hierarchical cluster analysis

were projected on cluster plots. This analysis was performed using R software version 2.11.

3. Results

3.1. Anthropogenic pressure quantification

3.1.1. Ecological Integrative Indicators (EII)

The five analysed estuaries ranged from very low to medium pressure levels according to

the final scores of the EII (Table 6). Mira and Gilão estuaries were assigned low pressure

values. Main pressure sources in the Mira estuary were related to animal production (livestock),

agriculture, aquaculture and intensity of port developments; in the Gilão estuary the main

sources were anthropogenically affected coastline, construction licenses, livestock, intensity of

port developments and tourism and recreation. Odeceixe and Aljezur estuaries were assigned

very low-pressure levels according to the EII, and identified sources were related to agriculture

and animal production. Bensafrim estuary had the highest final EII score (medium), and main

sources were construction licenses, urban and industrial land area, population density, intensity

of marina development capacity and tourism and recreation.

Table 6- Systems values for the considered Environmental Integrative Indicators (EII).

Indicador Mira Odeceixe Aljezur Bensafrim Gilão

Anthropogenically affected coastline 1 1 1 5 5 Construction licences 3 1 1 7 9 Water treatment discharges 1 1 1 1 1 % Urban land 1 1 1 9 3 % Industrial land 1 1 1 7 1 Population density 1 1 1 7 1 % Land for agricultural use 9 7 7 3 3

Livestock/ha 7 5 5 5 7 Aquaculture 9 0 3 0 0 Intensity of marina developments 0 0 0 9 0 Intensity of port developments 9 0 0 3 7 Tourism and recreation 1 1 1 7 7

EII 3.58 1.58 1.83 5.25 3.67

Class (pressure) low very low very low medium low

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3.2. Estuarine Ecological Quality based on fish multimetric indices

PERMANOVA results identified estuary and season as significant grouping variables (F=4.26,

p<0.01, and F=3.69 p<0.01, respectively). Following these results, all samples for an estuary were

considered as replicates, and sectors within estuaries were disregarded. The species list is presented

in Table 7.

The four multimetric indices applied to estuarine fish communities of all estuaries and

seasons had a high correspondence: Kendall’s correlations for all combinations were positive

and significant at p<0.05. The strongest correspondence was found between TFCI and AFI

(#=0.65; p<0.001). The weakest correspondence was between EBI and AFI (#=0.38; p=0.018).

These correlations were reflected in the seasonal variation of the EQR’s (Fig. 2). The

general tendency was for lower EQR in winter and higher EQR in spring and summer. The

exceptions were in Odeceixe estuary, where overall seasonal variation of EQR values was not

that evident, and also in Bensafrim estuary where AFI showed no seasonal variation. Mira and

Aljezur presented more pronounced seasonal variations when compared to the other systems.

Highest TFCI and EFCI values were reached in Mira estuary (spring and summer respectively),

followed by Aljezur (summer). For EBI the maximum value occurred in Bensafrim (summer),

and for AFI in Gilão (autumn).


94

Table 7- List of the species caught at the five estuarine systems. Ecological guilds were assigned following Elliott et al. (2007) classification. Estuarine use functional groups (EUFG) - catadromous species (CA), estuarine species (ES), marine migrants (MM), marine stragglers (MS) - and Feeding mode functional group (FMFG) - piscovore (PV), omnivore (OV), zooplanktivore (ZP), zoobenthivore (ZB) – are presented.

Species EUFG FMFG Mira Odeceixe Aljezur Bensafrim Gilão

Clupeidae Alosa fallax CA PV x Anguillidae Anguilla anguilla* CA OV x x x Atherinidae Atherina boyeri ES ZP x x Atherina presbyter MM ZB x x x x x

Mugilidae Chelon labrosus MS OV x x x x Liza aurata MS OV x x x x x Liza ramada CA OV x x x x x Liza spp. x x Moronidae Dicentrarchus labrax MM PV,ZB x x x x x Dicentrarchus puntactus MM PV,ZB x

Sparidae Diplodus bellotti MM ZB x Diplodus sargus MM ZB x x x x x Diplodus vulgaris MM ZB x x x Sarpa salpa MS ZB x Sparus aurata MM ZB x x x x x Diplodus spp. MM ZB x x

Engraulidae Engraulis encrasicolus MS ZP x x Gobiidae Gobius niger ES ZB x Pomatoschistus microps ES ZB x x x x x Pomatoschistus minutos ES ZB x Batrachoididae Halobatrachus didactylus MS ZB x

Syngnathidae Singnathus acus ES ZB x x Soleidae Solea senegalensis MM ZB x x x Solea solea MM ZB x x x

*critically endangered species

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Figure 2- Fish based multimetric indices seasonal variation.

The k-means analysis performed on EFCI and TFCI data highlighted three different clusters

(considering each estuary-season combination as a sample) (Figs. 3 and 4). For both indices,

cluster composition was similar. The analysis highlighted one cluster mainly comprising Mira

estuary samples and a sample from Aljezur (summer) (Figs. 3a and 4a). This cluster is

characterized by high values of the overall metrics for both indices (Figs. 3b and 4b). A second

cluster was essentially composed of Gilão and Bensafrim samples (regardless of season) and a

third cluster mainly comprised winter samples of all estuaries. Odeceixe estuary samples were,

for both indices, distributed between the second and third clusters (Figs. 3a and 4a). These

clusters were characterized by generally low values of index metrics (Figs. 3b and 4b).

By plotting results of the Estuarine Integrative Indicators (EII) according to the clusters (of

estuaries and seasons) obtained in k-means analysis (Figs. 3b and 4b), some tendencies were

observed. The cluster with higher EFCI and TFCI (fish community-based multimetric indices)


96

metric means also presented lower EII (anthropogenic pressure-based multimetric index) mean

values. On the other hand, for both indices, the cluster composed manly by winter samples

corresponded to the highest mean values of EII.

Figure 3- EFCI k-means clustering analysis and metrics normalized means for each identified cluster (1-3): a) cluster plot with the first two components explaining 69.53% of point variability; b) metrics normalized mean at the first axis and EII values at the second axis represented by a solid line. Names of estuaries are abbreviated by their first letter: A (Aljezur), B (Bensafrim), G (Gilão), M (Mira), O (Odeceixe). Sampled seasons are abbreviated by their first four letters: winter (wint), spring (spri), summer (summ), autumn (autu).

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Figure 4- TFCI k-means clustering analysis and metrics normalized means for each identified cluster (1-3): a) cluster plot with the first two components explaining 63.45% of point variability; b) metrics normalized mean at the first axis and EII values at the second axis represented by a solid line. Names of estuaries are abbreviated by their first letter: A (Aljezur), B (Bensafrim), G (Gilão), M (Mira), O (Odeceixe). Sampled seasons are abbreviated by their first four letters: winter (wint), spring (spri), summer (summ), autumn (autu).


98

4. Discussion

The accuracy of establishing the ecological integrity of estuarine systems is largely

dependent on two main data sources. One concerns the driving forces of impacts, and another

the actual level of impacts to which systems are subjected to (Aubry and Elliott, 2006).

Knowledge on the level of impacts requires previous and consistent monitoring of the systems’

environmental conditions, such as contamination levels and eutrophication indicators. The

estuarine systems subject of this work have not been included in a monitoring programme or a

comprehensive set of studies. Because of this, the necessary degree of inter-system

comparison with respect to the level of impacts was not achieved. Therefore, available data on

driving forces of pressure were used to evaluate the ecological integrity of these systems.

Although some accuracy can be lost by inferring ecological integrity based only on driving

forces, three classes of pressure levels among the five analysed estuaries could be

distinguished: Odeceixe and Aljezur estuaries, located in low urbanized areas and included in a

natural park with limitations on urban development, had very low pressure of the studied driving

forces; to Bensafrim estuary, located in a highly urbanized area, with important touristic

infrastructures, was attributed a medium pressure level class; Mira and Gilão estuaries (also

adjacent to and at least partially included in natural parks), in spite of having two different

nearby landscapes, were both classified with low pressure. Nevertheless, the main driving

forces acting in the two systems differed: in Mira estuary, agricultural exploitation, aquaculture

production and intensity of port developments are the main sources of impact, while in Gilão

estuary considerably high levels of urban development represents the main source. In view of

these results, Odeceixe and Aljezur estuaries probably have a lower impact level from the

analysed anthropogenic activities, whereas Mira and Gilão present a medium level of impact

and Bensafrim likely suffers the highest anthropogenic impacts.

Most fish-based multimetric indices developed to assess the ecological quality status of

estuarine systems are highly dependent on important methodological factors such as the

reference condition and sampling methodologies (e.g. Harrison and Whitfield, 2006; Coates et

al., 2007). Direct applications of fish multimetric indices to different environments are still scarce

(e.g. Harrison and Whitfield, 2006; Martinho et al., 2008; Henriques et al., 2008), apart from the

original study, and the intercalibration process for their application is still in development. For

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this reason, the current approach was based on multiple indices and aimed at a comparative

assessment between estuaries (and, within systems, between sampling seasons). In view of

this comparative rationale, instead of classifying the ecological status of these systems in a

categorical manner, we compared EQR values among estuaries and along sampling seasons.

The analysed estuarine systems revealed different ecological status, as indicated by the

applied fish community-based multimetric indices. According to these indices, and despite some

degree of response to fish community seasonality, Mira and Aljezur estuaries showed higher

ecological status on the terms in which the applied indices were developed. A lower ecological

status was indicated for Gilão, Bensafrim and Odeceixe estuaries. Even though Odeceixe and

Aljezur estuaries are similar in morphology and in overall levels of pressure (EII), they showed

differences regarding their ecological status as measured with fish community-based indices.

The degree to which these results reflect only anthropogenic induced degradations and are not

influenced by natural perturbation inherent to the system is unclear. Taking into account that

seasonality was the natural source of variation considered in our sampling procedure, and to

overcome the lack of consistent knowledge about these systems’ function, observations had to

be made based on the empirical fact that the used indicators may respond to various types of

pressure, natural or anthropogenic (Nip and Udo de Haes, 1995). We may emphasise that

Odeceixe was the less buffered regarding salinity variations due to rainfall, which is a season

dependent variable (Magalhães et al., 1987).

Following the suggestion by Jordan and Vaas (2000) that higher sensitivity to ecosystems’

integrity can be achieved using the information of the actual metric values than with the final

values of multimetric indices, we performed the cluster analysis to TFCI and EFCI results to all

estuaries and seasons followed by the analysis of metric mean values for each cluster. For both

indices, samples were grouped by season (almost all winter samples were clustered) and also

by ecological status regardless of season (Mira and Aljezur samples separated from Gilão and

Bensafrim). Only samples from Odeceixe were evidently distributed between two different

clusters. In addition, a gradient was found when analysing mean metric’s values for each of the

three clusters: from Mira and Aljezur at one end, with highest metric values; through mainly

Bensafrim and Gilão at an intermediate position and, finally, the winter cluster, with most

systems represented at the other end with lowest mean values for almost all metrics. The main


100

achievement of this analytic approach was the ability to separate, among the estuarine samples

with low EQR values, two groups which differ in mean metric values suggesting that these

groups reflect different sources of disturbance. Taking into account that one of these sources

was the natural seasonal fluctuation, which is overlapping EII mean values on the obtained

clusters, the other should be the anthropogenic level of pressure.

Nevertheless, doubts remain in regard to the Odeceixe estuary, which as stated before, has

the same level of pressure of Aljezur, induced by the accounted anthropogenic driving forces.

This suggests the existence of some factors that overcome seasonal fluctuations, which are

being responsible for defining the fish community structure, which were translated by the

applied multimetric indices as low EQR values for Odeceixe estuary. In fact, several

environmental factors contribute to estuarine fish assemblage structure: habitat availability,

salinity, current velocity, temperature and oxygen concentrations in different spatial and

temporal scales (Thiel et al., 1995; Methven et al., 2001). Particular features of small estuarine

systems, such as small mouth openings, barriers that can periodically close their connection to

the sea, freshwater inflow mainly dependent on rainfall regime that can lead to large fluctuations

in the physical environment, make these estuarine environments largely influenced by physical

variables (Riddin and Adams, 2008). Natural perturbations, such as the ones described, play an

important role in maintaining spatial-temporal heterogeneity in ecosystems, introducing local

and rapid fluctuations, which may prevent the systems from reaching a steady state (Scheffer et

al., 2003). These factors, and their interaction, may have had in Odeceixe estuary a higher

impact than in Aljezur during the time period covered by the present work, as it was noticed 25

years ago (Magalhães et al., 1987). This underlines the fact that the used biological indicators

are unable to differentiate between human sources of stress and natural sources of variability

and fluctuation (Quintino and Elliott, 2006; de Jonge, 2007; Zonta et al., 2007). This difficulty

arises in part from the fact that the commonly applied biological indicators explore the structure

of a given assemblage but do not integrate structure and function. Consequently, they do not

cover the environmental, geomorphologic and biological heterogeneity of these transitional

waters (de Jonge, 2007). These types of indicators seem to fall in the common misconception

that abiotic conditions are “external”, neglecting that an ecosystem is an interactive biotic-abiotic

entity (Scheffer and Carpenter, 2003). This is particularly worrying for estuarine management,

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where communities well adapted to natural stress can, with the referred indicators, be

misclassified, which is the underlining concept of the “Estuarine Quality Paradox” (Quintino and

Elliott, 2006).

Two main questions were to be answered with the present work: one was if the small

estuarine systems had different ecological status and a second concerned the underlying

causes of their ecological status, whether they were due to natural or anthropogenic driving

forces. With the applied fish community multimetric indices, we were able to distinguish different

ecological conditions among the five estuarine systems, and we found some degree of

correspondence between the indices’ results and the anthropogenic driving forces of pressure.

Nevertheless, doubts remain when systems with the same level of pressure have significant

different index responses.

Just like any other ecosystem, estuarine systems are complex and dynamic in terms of their

species structure and functioning (Zonta, 2007), and measuring all components relevant from

the normative viewpoint is not a feasible task. Therefore, the use of ecological indicators as

quality variables is currently growing (Nip and Udo de Haes, 2000). Nevertheless, the available

tools based on fish communities, seem to overvalue an empirical equilibrium in the structure of

these communities. Although some effort is being done to consider different typologies, based

mainly on salinity range (Breine et al., 2010), currently established methodologies disregard

morphological and physical characteristics of a system which can highly influence the potential

optimum fish community that a system can shelter. Models including this ability have been

developed for other ecosystems that seem to undergo the necessity of establishing different

tools for different morphological types of systems and integrating different types of indicators

with fuzzy logic (Ocampo-Duque et al., 2007). Costanza and Mageau (1999) already advised

that network analysis is a potential approach that can allow incorporating exchange pathways

connecting systems components. We believe that enriching currently available tools with this

approach would probably contribute to the development of tools aiming at a broader application,

by taking into account not only the fish community structure but also the main factors that

influence the potential optimum for this community.


102

5. Acknowledgements

We thank all people involved in field work. We also thank 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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Ecological quality assessment of small estuaries from the Portuguese coast based on

benthic macroinvertebrate assemblages indices.

Inês Cardosoª, Luís Cancela da Fonsecab




bCentro de Oceanografia, Laboratório Marítimo da Guia, Faculdade de Ciências da

Universidade de Lisboa Av. N. Sra. do Cabo, 939, 2750-374, Cascais, Portugal.

Marine Pollution Bulletin (Accepted)

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Ecological quality assessment of small estuaries from the Portuguese

coast based on benthic macroinvertebrate assemblages indices.

Abstract Benthic macroinvertebrates communities are the most consistently emphasized biotic component of aquatic ecosystems and are one of the biological indicators required for assessment by the European Water Framework Directive. In this context, several indices based on these communities have been developed in order to assess ecological quality of estuarine systems. In the present paper we used AMBI, M-AMBI, BENTIX and BAT to distinguish the ecological status of five small estuarine systems of the Portuguese south and southwest coasts. Although indices outputs did not differ between systems and sampling seasons, results indicated that the metrics in which these indices are based could differentiate community structures as a result of two main gradients that force these communities: the natural variability, and the anthropogenic impact.

Key-words: benthic macroinvertebrate communities, small estuaries, ecological integrity,

benthic macroinvertebrate based indices, Portuguese coast.

1. Introduction

The Water Framework Directive (WFD) has established the goal of achieving a “good

ecological quality status” for all European water bodies by 2015 (European Council Directive,

2000; Borja et al., 2006) in which estuaries are included. The baseline underlined in this goal is

that scientists should provide recommendations which guide policy makers to manage estuarine

systems in order to improve their quality, prevent deterioration, and ensure the progressive

reduction of pollution. To achieve this, an imperative ability of evaluating the ecosystems health

has urged the development of consistent tools to assess the ecological status of estuarine

systems.

The task of evaluating ecosystems health is far from simple mainly because of the

complexity of these systems and the consequent articulation of a number of interacting

components. In general, these components 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

Ecological quality assessment of small estuaries from the Portuguese coast based on benthic macroinvertebrate

assemblages indices.

110

and Udo do Haes, 1995; Whitfield and Elliott, 2002). 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).

Ecological indicators are commonly used to supply information about the state of

ecosystems (Salas et al., 2006). These indicators are quantitative representations of the forces

that drive a system (Salas et al., 2006), and allow the assessment and evaluation of a system

status (Pinto et al., 2009). Within this approach, ecological indices are used as quantitative tools

to simplify, through discrete and rigorous methodologies, the attributes and weights of multiple

indicators (Hyatt, 2001), and are often used to evaluate and assess ecological integrity as it

relates to a specific qualitative or quantitative feature of the system (Pinto et al., 2009). In this

context, the first aim of indicators is to distinguish between a healthy and degraded water

system with sufficient precision to identify the critical border between the need for “action” and

“no action” to improve the ecological condition. Hence, they must be able to detect

anthropogenic impacts and, ideally, be insensitive to natural variability (Van Hoey et al., 2010).

Benthic macroinvertebrates communities are the most consistently emphasized biotic

component of aquatic ecosystems (Borja and Dauer, 2008), as well as the most controversial

biological indicators required for assessment by the WFD (Puente and Diaz, 2008). Several

characteristics make macrobenthic organisms useful and suitable indicators: they live in bottom

sediments, where exposure to contaminants and oxygen stress is most frequent (Dauvin et al.,

2007); most species are relatively sedentary and reflect the quality of their immediate

environment (Dauer, 1993); many species have relatively long life spans ant their responses

integrate water and sediment quality changes over time (Dauer, 1993, Reiss and Kronck, 2005;

Dauvin et al., 2007); they include diverse species with a variety of life features and tolerances to

stress, which allow their inclusion into different functional responses groups (Person and

Rosenberg, 1978); some are prey of commercially important species (Reiss and Kroncke,

2005); and play a vital role in cycling nutrients and materials between the underling sediment

and the overlying water column (Dauvin et al., 2007).

In recent years, numerous benthic indices have been developed or adopted to fulfil the

WFD requirements following the criteria of disturbance sensitive taxa (e.g. Simboura and

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Zenetos, 2002; Borja et al., 2004; Rosenberg et al., 2004; De Paz et al., 2008; Dauvin and

Roullett, 2009), which have been applied and tested (e.g. Teixeira et al., 2007; Chainho et al.,

2008) still with no widely agreement concerning the best approach.

For a better assessment of ecological status several ecosystem compartments have to be

addressed and some degree of concordance among tools’ results or trends for ecological

integrity are to be expected. As such, this work observes the behaviour of four benthic

community based indices in five small estuaries of the Portuguese coast presenting low river

flow and narrow mouth openings, that can periodically be closed to the sea, and for which fish

assemblage-based indices have been applied (Cardoso et al., 2011). The main goal is to

distinguish ecological conditions among estuaries with different degrees of anthropogenic

impacts and high levels of natural variability.

2. Methods

2.1. Study areas

Five small estuarine systems located on the Portuguese coast were sampled: Mira,

Odeceixe and Aljezur (in the southwest coast), Gilão and Bensafrim (on the south coast) (Fig.

1).

Mira estuary is located in the protected area of Parque Natural do Sudoeste Alentejano e

Costa Vicentina (PNSACV), and was already considered the least impacted estuary of the

Portuguese coast, when compared to larger ones (Vasconcelos et al., 2007). Its 30 km

extension and 100 m wide mouth opening make it the largest system considered in the present

work, with a river flow of 2.9 m3s

-1. Odeceixe and Aljezur estuaries, also included in PNSACV,

are 6 km and 7 km long, with a river flow of 2.84 m3s

-1 and 0.97 m

3s

-1 respectively, and both

have 50 m wide mouth openings. These two systems are located in areas around small villages

with a low number of inhabitants. Bensafrim and Gilão estuaries are 4 km and 6 km long, with

65 m and 150 m wide mouth openings and a river flow of 0.25 m3s

-1 and 1.29 m

3s

-1 respectively.

These estuaries are located near cities, in areas where tourism is the main economical activity,

with high seasonal population fluctuations and unknown sewage loadings. The terminal part of

Gilão is included in a natural park (Parque Natural da Ria Formosa). River flow is mainly



112

torrential in all estuaries, directly dependent on rainfall, and influences spatial and temporal

variations in salinity.


2.2. Sampling and laboratory procedure

Benthic samples were collected during winter (January) and summer (June) of 2010.

In each system, three equivalent sectors were defined in order to include the wide salinity

range in each system: sector A, near the estuary mouth; sector B, intermediate; and sector C, in

the upper part of the estuary, with a low marine influence. With the exception of the Mira

estuary, the upstream limit of sector C was mainly defined by navigability range (Fig. 1). At each

sector, benthic macroninvertebrates were sampled using a van Veen grab (sampling area=0.05

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m2). Three replicates were collected in each sector and sampling period. Immediately after

collection, sediment samples were sieved (0.5 mm mesh size), fixed and stained with Bengal

Rose. All animals were identified to the lowest taxonomic level possible and counted.

2.3. Data analyses

Species richness, Shannon-Weiner, Simpson and Pielou’s indices of diversity and

equitability were calculated for each system and season within systems.

Among the indices available, we chose the following four: AMBI (Borja et al., 2000), M-

AMBI (Muxika et al., 2007), BENTIX (Simboura and Zenetos, 2002) and BAT (Teixeira et al.,

2009). AMBI, M-AMBI and BENTIX are indices based on ecological groups, which are ranked

according to their sensitivity to an increasing stress gradient. For AMBI and M-AMBI groups are

classified according to the as per the updated list published by the AZTI Laboratory

(www.azti.es): Group I (species very sensitive to organic enrichment); Group II (species

indifferent to enrichment); Group III (species tolerant to excessive organic enrichment); Group

IV (second-order opportunistic species); and Group V (first-order opportunistic species); In

BENTIX, there are only two groups -. The number or groups considered varies with the index:

five for AZTI methodologies (AMBI and M-AMBI) and two for BENTIX sensitive and

opportunistic. Indices are calculated according to the following formulations:

AMBI=[(0x%GI)+(1.5x%GII)+(3x%GIII)+(4.5x%GIV)+(6x%GV)]/100

and

BENTIX = (6 x %GS + 2 x %GT)/100,

where, for AZTI methodologies, %GI is the relative abundance of species sensitive to

disturbance (Group I), %GII the relative abundance of disturbance-indifferent species (Group II),

%GIII, the relative abundance of disturbance-tolerant species (Group III), %GIV, the relative

abundance of second order opportunistic species (Group IV), and %GV, the relative abundance

of first order opportunistic species (Group V); for BENTIX, %GS is the relative abundance of

sensitive species, corresponding to %GI+%GII, and %GT is the relative abundance of tolerant

species, corresponding to %GIII+%GIV+%GV. For comparisons proposes 1/BENTIX was used

instead of the absolute values.



114

The M-AMBI is a multivariate factorial analysis combining AMBI with the Shannon-Weiner

diversity and species richness indices (Borja et al., 2004, 2007; Muxika et al., 2007). The BAT

index is a multimetric methodology that combines Margalef, Shannon-Weiner and AMBI indices.

This index was calculated according to Teixeira et al. (2009).

Without any previous data that could support a proper reference condition, indices were

used for comparison purposes between indices behaviour and not to assess the actual

ecological status of each system. Hence, for M-AMBI and BAT oligohaline/mesohaline

reference conditions were used for all systems. For BENTIX and BAT scores, thresholds were

defined according to grain size classes, as proposed by the authors. AMBI and M-AMBI were

calculated using AMBI© software.

Kruskal-Wallis analysis was used to evaluate differences between systems considering all

seasons and also between sampling seasons within each system. Principal components

analysis, applied to indices’ metrics, was used to observe the influence of these metrics on

samples differentiation.

The relation between indices’ results and the Environmental Integrative Indicators (EII)

previously published for the same systems by Cardoso et al. (2011) was examined through

Spearman’s correlations. For the EII the following indicators were quantified: anthropogenically

affected coastline, construction licences (number), % of urban land, % of industrial land, % of

land for agricultural use, population density, water treatment discharges, livestock, aquaculture,

intensity of marina developments capacity, intensity of port developments (number of registered

vessels) and tourism and recreation (% of affected coastline). The EII’s classification scheme

comprises five classes according to its final score: no disturbance (0); very low (0<EII<2); low

(2!EII<4); medium (4!EII<6); high (6!EII<8) and very high disturbance (8!EII!9). Systems final

scores are presented in Table 1 (Cardoso et al., 2011).

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Table 1- Systems values for the considered Environmental Integrative Indicators (EII) (Cardoso et al., 2011).

Indicador Mira Odeceixe Aljezur Bensafrim Gilão

Anthropogenically affected coastline 1 1 1 5 5 Construction licences 3 1 1 7 9 Water treatment discharges 1 1 1 1 1 % Urban land 1 1 1 9 3 % Industrial land 1 1 1 7 1

Population density 1 1 1 7 1 % Land for agricultural use 9 7 7 3 3 Livestock/ha 7 5 5 5 7 Aquaculture 9 0 3 0 0 Intensity of marina developments 0 0 0 9 0 Intensity of port developments 9 0 0 3 7 Tourism and recreation 1 1 1 7 7

EII 3.58 1.58 1.83 5.25 3.67

Class (pressure) low very low very low medium low

3. Results

Mira and Gilão communities were considerably more diverse, followed by Odeceixe estuary

and by Aljezur and Bensafrim, which presented the lowest diversities (Table 2). At all systems

some variation in diversity and species richness values occurred between seasons with no

common pattern between systems. Equitability seasonal variations were considerably small with

the exceptions of Aljezur estuary, which had a reduction during summer sampling season. Mira

estuary showed the highest values.

Table 2 -Seasonal diversity values for the five studied systems. Species richness (S), Shannon-Wiener diversity (H’) and Pielou’s equitabilty (J’).

Benthic communities from all estuaries were clearly dominated by species that are included

on Group III (tolerant species) (Fig. 2). In Aljezur, Odeceixe and Bensafrim this dominance

resulted in values above 90% of species abundances; in Mira and Gilão estuaries this group

had a weaker expression but still reached values above 70%. First order opportunistic species

(Group V) were the second most represented ecological group in terms of species abundances.

This group was strongly represented during winter in Bensafrim and Gilão estuaries reaching


winter summer winter summer winter summer winter summer winter summer

S 20 15 14 21 15 14 13 15 32 19

H' 2.35 2.07 1.43 1.76 1.99 1.48 1.22 1.62 2.41 1.85

J' 0.79 0.76 0.54 0.58 0.73 0.56 0.48 0.60 0.69 0.63



116

values above 50%. The relative abundance of sensitive species (Group I) was low in all

estuaries with the exception of Gilão where they represented more than 20% of the abundance

of individuals. Ecological groups II and IV (species indifferent to organic enrichment and

second-order opportunistic species, respectively) were only present at Mira estuary, reaching

values above 20%, and in Gilão estuary during winter with a value lower than 10% (Fig. 2).

Figure 2- Relative percentage of the five ecological groups (I, II, III, IV, V) found in the studied

systems.

Benthic community-based indices’ outputs were not considered significantly different

between estuarine systems (AMBI: H=1.85, p>0.05; M-AMBI: H=6.33, p>0.05; BENTIX: H=7.42,

p>0.05; BAT: H=6.65) or between seasons (AMBI: H=0.88, p>0.05; M-AMBI: H=0.09, p>0.05;

BENTIX: H=0.27, p>0.05; BAT: H=0.53, p>0.05). Within estuaries no significant differences

were found. Nevertheless, AMBI and M-AMBI followed the same tendency along seasons with

the exception of Aljezur summer sample. Indices highest scores did not occur in coincident

seasons for all the systems studied (Fig. 3).

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Figure 3- Indices values obtained for each system. For comparison proposes 1/BENTIX was used instead of BENTIX. The axes refer to AMBI values on the right and M-AMBI, 1/BENTIX and BAT on the left.

The highest values for 1/BENTIX were reached in Odeceixe, Aljezur and Bensafrim. For

BAT the highest values were obtained in Gilão and Mira estuaries during summer. For AMBI the

highest value was found for Bensafrim estuary during winter, followed by summer in Aljezur and

winter in Gilão; the lowest values were obtained in Gilão and Mira estuaries during summer. For

M-AMBI index, the highest score was found in Gilão estuary followed by Mira, both during

winter; the lowest scores were obtained in Bensafrim estuary during summer and in Aljezur

during winter (Fig. 3).

PCA analysis, with 90% of variance explained by the first two axes, showed that ecological

groups II, IV and V considered in the several indices were the ones that better distinguished

estuarine samples. The presence of these groups separated samples by seasons in three

systems: winter in Mira, Gilão and Bensafrim estuaries (with the highest relative importance of

groups IV and V). The high dominance of Group III clustered Aljezur and Odeceixe estuaries

with summer samples of Mira and Bensafrim (Fig. 4). There was no correlation between indices’

scores and the considered EII (Fig. 5).



118

Figure 4- Principal components analysis plot. Name of estuaries are abbreviated by: Alj (Aljezur), Ben (Bensafrim), Gil (Gilão), Mir (Mira), Ode (Odeceixe). Sampled seasons are abbreviated by: Wint (winter), Sum (summer). Ecological groups are represented by I (species very sensitive to organic enrichment), II (species indifferent to enrichment), III (species tolerant of excessive organic enrichment), IV (second-order opportunistic species) and V (first-order opportunistic species). H and S refer to species richness and Shannon-Weiner diversity indices, respectively.

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Figure 5- Relation between indices results and the Environmental Integrative Indicators (EII).

4. Discussion

Based on a selection of ecological indices using macrobenthic communities and with some

previous knowledge on the anthropogenic levels of impacts that systems are facing, we made

an attempt to distinguish the outputs of the selected indices in five small estuaries. The goal

was not to classify the ecological status of the systems but to compare indices results. In order

to overcome the lack of previous data for these poorly studied estuaries, which could support

the settlement of proper reference conditions, the approach followed here did not focused on

the final score of each index, instead emphasizing indices relative values and the ecological

status distinctiveness of each estuary. A similar approach was followed in Cardoso et al. (2011)

using fish community-based indices, concluding that based on the analysis of two indices and



120

relating them to the level of impact of the same systems, that ecological status distinctiveness

was achieved.

Nevertheless, macrobenthic based community indices did not reveal a consistent pattern,

and presented small variations in systems scores. Thus it was not possible to infer on systems’

ecological integrity differentiation. Several authors have already mentioned the cautions that

have to be taken when applying such tools to naturally disturbed systems (e.g. Diaz et al., 2004;

Chainho et al., 2007; Dauvin et al., 2007; de Jonge, 2007; Elliott and Quintino 2007; Zonta et

al., 2007; Blanchet et al., 2008; Borja et al., 2008; Chainho et al., 2008; De Paz et al., 2008;

Dauvin and Ruellet, 2009; Pinto et al., 2009). This question is now very present in literature and

is the object of the actual debate upon scientific efforts to respond to European legislation.

Recently, Green and Chapan (2011) have pointed out and resumed the problems involved

in the development of indices and their utility, arguing that the currently available methodologies

are not working and do not give any measure of certainty for the decisions to make. In addition

they do not give a measure of probability to the accurate score of a given index. This is also the

case with the present study. We acknowledge the fundamental weakness of this applicability:

the settlement of a proper reference condition. Nevertheless, in systems with high natural

variability at all temporal scales, such as the ones studied here, this is probably very difficult to

overcome. First, there is an absence of historical data, previous to impact, that could support

this potential community. Second, if it existed, probably could not be considered as a reference

since coastal systems are dynamic and small estuaries can be on one extreme of this coastal

dynamic. Even their morphological characteristics can change with low level of predictability. In

small-scaled ecosystems, coastal lagoons can evolve to equivalent but not identical systems by,

for example, the consistent opening of their connection to the sea. Events like this have

structural impact in several features such as salinity and grain size in which the present indices’

methodologies base their reference values.

Other question that arises with our attempt to use the actual tools is the community

structure. In establishing a reference condition, there is an actual need to settle a potential

community corresponding to a low level of anthropogenic impact. However, in systems with low

levels of impact but very poorly diverse communities, the poor ecological state that is commonly

the output of the applied tools must be rejected. The concept of potential community can not be

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of a different nature from the natural community - it has to be dynamic, respecting and following

the natural oscillations of species assemblages to the natural fluctuation of their environment

(Strugel, 1991; Teixeira et al., 2008).

Our results agree with the ones by Puente and Diaz (2008), which also could not

differentiate ecological integrity of a set of systems. Results in the present study however

indicate that the metrics in which these indices are based can, to some degree, differentiate

community structures that can be interpreted as a result of two main gradients that force these

communities: the natural variability, and the anthropogenic impact, resumed to organic

enrichment by the applied methodologies (e.g. Simboura and Zenetos, 2002; Borja et al., 2004;

Rosenberg et al., 2004; Dauvin and Roullett, 2007). Our samples could be grouped by the

weight of tolerant species (Group III), and by the presence of the groups II, IV, and V. In this

way, through the analysis of metrics, it was possible to detect anthropogenic impact in

Bensafrim and Gilão, which is agreement with the previous study’s reported levels of impact

(Cardoso et al., 2011). In addition, the Mira estuary, one of the most diverse considered here,

presented species that may correspond to a healthy community but with the presence of

species from group IV indicating a possible diagnostic of an important impact from organic

inputs. Nevertheless, most samples were clustered by influence of ecological group III, which

dominated most estuaries in terms of abundance of individuals. This is probably a consequence

of the high natural variability inherent to all systems. In this context metrics seem to be more

informative than the indices based on them, as suggested by Jordan and Vaas (2000) and

Cardoso et al. (2011).

Apart from the anthropogenic impacts and biological factors that act on the structure of

macrobenthic communities, environmental features are known to be determinant. For these

communities several environmental factors have been considered: sediment grain size (Teske

and Wooldridge, 2003; Ysebaert et al., 2003; Anderson, 2004; Hirst and Kilpatrick, 2007;

Anderson, 2008) and organic matter content (Magni et al., 2009), average salinity (Attrill, 2002;

Teske and Wooldridge, 2003; Giberto et al., 2004) and hydrodynamic variability (Thrush et al.,

2005). Nevertheless, reference conditions are based on one or two from the list above, i.e.

salinity and grain size, even though their role is still not well established (Lindegarth and Hoskin,

2001), and with no regard to the interaction between their individual effects.



122

It is of common sense that the ability to extract information from complex ecosystems is

limited. But it is becoming clear that taking small ecosystem compartments and interpreting

them without any reference to their interaction is probably not the best approach for all systems

(e.g. Diaz, 2004). Small estuaries, which are more likely to demonstrate a response to a given

disturbance (organic input or other) than large estuaries are a good example (Meeuwing, 1999).

A large percentage of tolerant species in estuaries as that found in the present study was

also observed in the estuaries studied by Chainho et al. (2008) and Puente and Diaz (2008).

This fact only, is independent of the reference condition chosen to the interpretation of results.

This is, in fact, one of the main characteristics of the communities within these systems, and it is

probably reason enough to discard the applied tools as they are presented in their absolute

outputs. In such cases, it is extremely difficult to differentiate anthropogenic impacts from

natural perturbations and this is why, even with a definition of a proper reference community,

the interpretation of indices does not necessarily accurately reflect ecological states derived

from anthropogenic impacts.

In view of the difficulties and limitations of these methodologies, testing other developed

ones becomes of increased importance, as suggested by Green and Chapman (2011). Studies

such as that from Reynoldson et al. (1997) present other methodologies that should be kept in

mind to the settlement of reference conditions; approaches like that used by Ocampo-Duque et

al. (2007) are worth trying and do respond to Costanza and Mageau (1999) suggestion of using

network analysis in this context.

In conclusion, the applied tools take into consideration very important features of

communities’ response to organic enrichment. The metrics on which they are based are highly

informative within this gradient. Nevertheless, they simplify the anthropogenic perturbations to

only one aspect of their impact. In addition, factors such as system dimensions, mouth

openings, or plant cover within systems, all extremely important for community structure and

overall diversity which clearly depends on environment stability (Dye and Barros, 2005), have

been discarded from the settlement of reference conditions. The common biological indicators

are measuring the degree of structure of a given assemblage, but do not integrate its structure

and functions (de Jonge, 2007). Without detracting the used methodologies, in our opinion their

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application could be enriched through the inclusion of other features of ecosystems in a more

integrative tool, as already suggested by Borja et al. (2008).

5. Acknowledgements

We thank IMAR-CMA for the help and application of BAT. We also want thank all involved

in 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 and PEst-

OE/MAR/UI0199/2011). Inês Cardoso was founded with a PhD grant by FCT (SFRH / BD /

31261 / 2006).

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PART 4

Vulnerability Assessment.

CHAPTER 6

Vulnerability assessment in small estuaries from the Portuguese coast

Inês Cardosoª, Luis Cancela da Fonsecab,c




bCentro de Oceanografia, Laboratório Marítimo da Guia, Faculdade de Ciências da

Universidade de Lisboa Av. N. Sra. do Cabo, 939, 2750-374, Portugal.

cCentro de Ciências e Tecnologias da Água, Universidade do Algarve Campus de Gambelas,

8005-139, Portugal.

Marine and Freshwater research (submitted)

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Abstract Estuaries are worldwide examples of human-ecological coupled systems and are subject to many pressures derived from human activities. The rapid population growth and uncontrolled development in many coastal regions caused a wide array of human impacts that can compromise their ecological integrity and lead to an intuitive statement that these systems are vulnerable. The vulnerability of five small estuaries from the Portuguese coast (Mira, Odeceixe, Aljezur, Bensafrim and Gilão) was assessed. The applied methodology identified: (1) the number of driving forces acting in each system and their magnitude; (2) system vulnerability in two components, i.e. susceptibility and sensibility of exposure; and (3) ecosystem’s potential of alteration. The studied systems presented different magnitudes for the driving forces considered (population density, percentage of industrial and agricultural land, livestock and hydromorphological features). Results revealed Mira and Gilão estuaries were at smaller risk of alteration. On the other hand, Bensafrim estuary had the highest risk of alteration due to high magnitudes of the main driving forces that contribute to this system’s vulnerability. The results allowed setting guidelines and recommendations for management and preservation of each system. Key-words: Vulnerability; anthropogenic impact; human-ecological coupled systems; small

estuaries.

1. Introduction

The ecological, functional and economical value of estuaries is largely accepted in

nowadays (Constanza, 1997; Kennish, 2002). These naturally stressed ecosystems (Elliott

and Quintino, 2007) are worldwide examples of human-ecological coupled systems, reason

why these systems are subject to many pressures from human activities (Leurs et al.,

2003), originated within the estuary, in adjacent areas, or even in distant areas from the

estuarine system (Zacharias and Gregr, 2004). Because of rapid population growth and

uncontrolled development in many coastal regions, estuaries exhibit a wide array of human

impacts that can compromise their ecological integrity (Kennish, 2002), leading to an

intuitive statement that these systems are vulnerable. Estuarine systems are subject to

impacts of various sources such as chemical spills, swage/outflow, sediment mobilization,

species introduction, agricultural runoff, urban runoff, land-cover alteration, dredging and

infilling, change in freshwater input, dams construction, all having direct and indirect


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consequences to communities’ composition, habitat diversity and ecosystem function

(Zacharias and Gregr, 2004).

Although there is no widely accepted consensus on the definition of vulnerability, it is

generally considered a measure of exposure to a stressor effect (also termed sensitivity or

potential impact) (Turner et al., 2003; Wilson et al., 2005) and of recovery potential (also

termed resilience or adaptive capacity) (Turner et al., 2003; Adger, 2006; Gallopín, 2006;

De Lange et al., 2010). It is widely noted that vulnerability to environmental change does not

exist in isolation from the wider political economy of resources use. Vulnerability is driven by

inadvertent or deliberate human action that reinforces self-interest and the distribution of

power in addition to interacting with physical and ecological systems (Adger, 2006). We

assume ecosystem stability, resilience, adaptability, and resistance when we extract

resources, depend on it to purify wastes, or impose recreational impacts. However, these

assumptions are no longer valid when the stresses imposed are outside the range the

system has adapted to. Thus, the vulnerability of an ecological system increases as the

number, intensity, and frequency of stressors increases (Bradley and Smith, 2004).

The increasing perception that human impacts are affecting our coastlines has, in this

way, promoted the concept of vulnerability (Woodroffe et al., 2007). Ecological vulnerability

is a general term which can be used as several hierarchical levels (organism, ecosystem,

and landscape) (De Lange et al., 2010) and several approaches and attempts have been

made to quantify vulnerability. In a review of studies which focus on ecological vulnerability,

De Lange et al. (2010) showed that almost all published works were on landscape analysis,

and the algorithms developed until now focus on very large areas when quantifying

vulnerability, whilst few studies focus vulnerability at the ecosystem level (e.g. Halpern et

al., 2007, Ippolito et al., 2010).

At the political level, an increase of concern with environmental conservation led to the

implementation of several legislative documents, namely the Water Framework Directive

(WFD) which seeks to ensure the highest possible ecological status for all water bodies,

including transitional waters, within European Union (EU) borders (European Council

Directive, 2000) and demands for efforts towards improving local habitat conditions and the

chemical status of water bodies. The WFD stipulates that water status should be monitored

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by Member States on a systematic and comparable basis throughout the EU, using

standardized methods of monitoring, sampling and data analyses (Zonta et al., 2007).

Hence, hydrological basins have been established and the main systems within these

basins were included in national monitoring programs. The final objective of this

environmental management strategy is to protect the structure and function of communities

and ecosystems (Ippolito et al., 2010). In this context, vulnerability assessment clarifies a

course of action (Green and McFadden, 2007), and provides support to risk management

by better defining the target of protection and by developing scenarios of potential impact on

a number of ecological traits (De Lange et al., 2010). Understanding the ways in which

particular threats affect ecosystems can aid in prioritizing the most important or more

manageable threats (Halpern et al., 2007).

In the context of the Portuguese coast, the WFD monitoring program includes mostly

large estuarine systems, usually with high levels of anthropogenic disturbance. This

nevertheless excludes small estuarine systems, which may be important but are

simultaneously poorly known and studied. In this way, biotic diversity and natural resources

may continuously be reduced, and there is no time to wait for sufficient knowledge (which

we usually never obtain) before action (Nilsson and Grelsson, 1995). It is possible that small

estuarine systems, with high ecological value can functionally disappear, with unknown

consequences to coastal communities. In the present study, we aimed establishing the

current ecological vulnerability of five small estuaries from the Portuguese south and

southwest coasts. Although the ecological status of these systems is still unclear due to the

difficulties in the application of currently available tools (see Cardoso et al., 2011a), their

functional importance has already been enhanced (Cardoso et al., 2011b). The main goals

of this work are, therefore to identify the main drivers of anthropogenic impact in these

systems and to quantify systems vulnerability, which are the necessary steps to effective

pressure mitigation (Mcfadden et al., 2007).


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2. Methods

2.1. Study areas

Five small estuarine systems located in the Portuguese coast were considered: Mira,

Odeceixe and Aljezur (in the southwest coast), Bensafrim and Gilão (in the south coast)

(Fig. 1).

Figure 1- Location of the the five small estuarine systems considered in this study: Mira, Odeceixe and Aljezur estuaries, located in the Southwest coast, and Bensafrim and Gilão estuaries in the Portuguese South coast.

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The Mira estuary is located in the protected area of Parque Natural do Sudoeste

Alentejano e Costa Vicentina (PNSACV), and was considered the least impacted estuary of

the Portuguese coast, when compared to larger ones (Vasconcelos et al., 2007). It is the

largest system included in the present work, with 30 km long and a 100 m wide mouth

opening. Odeceixe and Aljezur estuaries, also included in PNSACV, are 6 km and 7 km

long, respectively, and both have 50 m wide mouth openings. These two systems are

located in areas nearby small villages with a low number of inhabitants. Bensafrim and

Gilão estuaries are 4 km and 6 km long, and have 65 m and 150 m wide mouth openings,

respectively. The two latter estuaries are located near cities, in areas where tourism is the

main economical activity, with high seasonal population fluctuations and unknown sewage

loadings. The terminal part of Gilão is included in a natural park (Parque Natural da Ria

Formosa - PNRF). River flow is mainly torrential in all estuaries, directly dependent on

rainfall, and influences spatial and temporal variations in salinity.

2.2. Vulnerability assessment

We adapted the methodology proposed by Ippolito et al. (2010) to the current state of

knowledge on the analysed systems. Four main steps were considered within this

methodology: (1) identification of the main driving forces of stress and quantification of their

magnitude; (2) expert judgment on vulnerability components of communities and habitats;

(3) evaluation of systems vulnerability to each driving force; and (4) estimation of systems’

potential of alteration by each driving force. The four components are explained hereafter.

2.2.1. Identification and quantification of the magnitude of the main driving forces

Data on these systems are scarce and local monitoring efforts are low. Even though

this is not impeditive to the identification of driving forces, it adds some constraints on the

considered scale of stressors characterization. Five main driving forces of pressure were

identified and their magnitude quantified: urban (characterized by population density);

industrial (measured with percentage of land used for industrial purposes); agricultural

(measured with percentage of land used for agriculture); livestock (measured with density of

raised animals - number of animals per ha); and hydromorphological. This latter driving


138

force has three important components: factors with positive influence on river flow (number

of urban sewage inputs); factors with negative influence on river flow (dams and flow

barriers), and system length. The hydromorphological driving force is expressed as (1):

(1) Hydromorphological=(Barriers+Input Sources)/System length

Driving forces’ magnitudes were standardized according to a scoring system ranging

from 0 (null magnitude) to 5 (high magnitude). Data for this evaluation was obtained from

governmental and public sources - National Statistics Institute (Instituto Nacional de

Estatística, INE), National Water Institute (Instituto Nacional da Água, INAG) - and refer to

the surrounding municipalities (Table 1).

Table 1- Driving forces scoring system. Population density (number of individuals per km2), % of industrial land of total county area (Km), % of agriculture land of total county area, livestock (number of animals per ha), hydromorphological ((Barriers+Input Sources)/System length). 0 1 2 3 4 5

Population density 0-27 28-54 55-81 82-108 109-135 >135 Industrial Land (%) 0-0.03 0.031-0.06 0.061-0.09 0.091-0.12 0.0121-0.15 >0.151 Agricultural Land (%) 0-10 10.1-20 20.1-30 30.1-40 40.1-50 >50.1 Livestock (animals/ha) 0-0.04 0.41-0.08 0.081-0.12 0.121-0.16 0.161-0.20 >0.20 Hydromorphological 0-0.4 0.41-0.8 0.81-1.2 1.21-1.60 1.61-2 >2.01

3. Results

The analysed systems presented different magnitudes for the considered driving forces

(Table 2). Mira estuary was affected by the lowest number of driving forces of impact. Still,

and together with Gilão estuary, it had the highest levels of livestock source of impact.

Odeceixe, Aljezur and Bensafrim estuaries had the highest level of hydromorphological

sources of perturbation. Bensafrim estuary was affected by all the considered driving forces

of impact with the highest magnitude for population density.

The assessment of system vulnerability (Vx) to each driving source via expert

judgement allowed identifying the main sources of vulnerability for each system (Fig. 2). In

Mira estuary the most important source of vulnerability was agricultural exploitation,

followed by urban and livestock, both with intermediate values below 8. In Odeceixe and

Aljezur estuaries the main sources of vulnerability were hydromorphological driving forces

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139

and agricultural exploitation, both with intermediate to high levels of system vulnerability,

with values between 6 and 8 of the applied index. For Bensafrim estuary, the importance of

urban and hidromorphological sources was clear, reaching the value 8 in the system

vulnerability assessment. In Gilão estuary the expert judgment rendered similar system

vulnerabilities, between 4 and 6, for all considered driving forces, with vulnerability to urban

sources reaching an intermediate level (6). The maximum score for the applied index (12)

was not reached in any system.

Table 2- Driving forces’ magnitude at the studied systems. Mira Odeceixe Aljezur Bensafrim Gilão

Population density 0 0 0 4 1 Industrial Land 0 2 2 5 0 Agricultural Land 4 3 3 3 5 Livestock 5 4 4 4 5 Hydromorphological 3 5 5 5 3

The evaluation of potential of alteration of each system based on the vulnerability

scores and magnitude of driving forces enabled a risk assessment for these systems (Fig.

3). Bensafrim estuary, with three driving forces clearly acting (urban, industrial and

hydromorphological) and with the highest value of potential of alteration (114) had the

highest levels of risk of community and habitat degradation. For Odeceixe and Aljezur

estuaries, with a potential of alteration of 77 and 73, respectively, hydromorphological

factors were the main sources of pressure acting upon this systems. In Mira estuary, with a

value of potential of alteration of 67, agricultural and livestock exploitations were the main

sources of pressure. Gilão estuary presented the lowest value of risk of alteration (54) and

the main acting pressure was livestock exploitation.

4. Discussion

The applied approach allowed for an assessment of vulnerability for five small estuaries

from the Portuguese coast with different levels of pressure, three of them located within a

protected area. The fundamental objectives of this study were to present a measure of

vulnerability for these small estuaries, and to identify critical factors that should be

considered in management.


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The selection of driving forces and the assessment of their impacts are, such as the

establishment of the ecological quality state of estuarine systems, within the scope of the

European Water Framework Directive (European Council Directive, 2000; Borja, 2006).

These two components concern the main objective of achieving good ecological quality

state and management of coastal systems. Although the establishment of the ecological

state is critical, it gives per se little information about necessary measures to be taken if

good quality state is not presently achieved. In addition, it does not give information about

system vulnerability to driving forces currently acting and the consequences to expect if

their magnitudes change.

The present ecological state of an estuary can be considered as the system’s response

to past and current impacts, and thus the concept of vulnerability here applied represents a

conceptual link between changes in the external environment and the responses of the

affected system. The nature of vulnerability only matters to the extent to which it produces

insights that will help us to adapt to, or mitigate, external changes (Green and McFadden,

2007; Halpern et al., 2007).

Because the estuarine systems considered in this study are not included in any

consistent monitoring effort, and information about their sources of impact is scarcely

quantified, expert judgement plays an important role in inferring on the impact of current and

potential driving forces on the communities. The quantification of the driving forces was

based on official data concerning the respective watersheds, and represents a broad scale

analysis of impact sources. Even though this can give some indication of potential risk, a

more small-scale analysis at the ecosystem level would probably give more accurate

information.

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Figure 2 - Vulnerability in each system according to driving sources.


142

Figure 3- Potential of alteration in each system according to driving sources.

Despite the scarce data and scientific knowledge on the considered systems, it was

possible to achieve a vulnerability assessment using the applied methodology. We adopted

Ippolito et al. (2010) index of vulnerability with some necessary modifications that follow the

level of knowledge on the studied estuaries. Although the original formulation of the applied

index has a reference to the recovery capability of communities in the system, we opted to

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exclude this component for two main reasons. Firstly, since recovery capability is a

propriety inherent to the community, then it would be necessary to identify a particular

community to infer about its resilience since response times differ between biological

communities (Ippolito et al., 2010) and between habitats (McFaden et al., 2007). The

second reason was the risk of obtaining highly subjective answers by the consulted experts,

due to the broad-scale within each driving force. In this way, without sufficient scientific

knowledge on one particular community, we excluded the component that was more

obviously dependent on a community characterization. We acknowledge that these are

limitations for the vulnerability assessment although the lack of consistent information

cannot be impeditive in setting directions for management and sustainable uses of natural

resources. This is particularly true considering that natural systems are disappearing and in

some cases there is probably little time to act (Nilsson and Grelsson, 1995). And, in the

context of the watersheds in which these five small estuaries are included, this can happen

in a rather discrete manner.

The applied methodology allowed establishing the number of driving forces acting in

each system, their magnitude, system vulnerability (in two components: susceptibility and

sensibility of exposure) and ecosystems’ potential of alteration. In this way, Mira estuary,

with three of the five considered driving forces acting as pressure sources, is probably in the

highest risk of ecosystem alteration due to the potential impact of agricultural and livestock

exploitation. This concurs with Vasconcelos et al. (2007), which identified anthropogenic

pressure descriptors for eight Portuguese estuaries and highlighted agriculture as the most

important in this estuary, even though livestock was not considered. Given that the highest

driving force on system vulnerability is also the source of higher risk for potential of

alteration, advise for monitoring effort and management of this factor should be taken into

account, enouncing the need for a consistent quantification and assessment of agricultural

and livestock runoffs.

For Odeceixe and Aljezur estuaries, although agricultural exploitation is the main driving

force for vulnerability, the sources of potential alteration are factors related with their

hydromorphlogy. This illustrates the high magnitude of this driving force in these systems,


144

and emphasizes importance of reducing barriers to water flow, or at least, of local measures

to avoid an increase of water captions.

Finally, Bensafrim and Gilão estuaries have a generally similar distribution of system

vulnerability to driving forces although the former presented higher vulnerability to urban

and hydromorphological driving forces. Despite this similarity, the systems differ notably in

terms of potential of alteration: Bensafrim estuary had the highest potential of alteration, due

to hydromorpological and urban driving forces, whilst Gilão estuary had the lowest potential

of alteration among all systems. Bensafrim estuary is located in an important tourism region,

with high seasonal fluctuation of population density and growing urban development.

Cardoso et al. (2011) highlighted the probable poor ecological quality state of this system

comparatively to the other four systems, which is in agreement with the results in the

present vulnerability assessment. The ecological quality status and the high potential of

alteration in Bensafrim estuary advises for measures that mitigate the impact of urban and

hydromorphological pressures, and the urgency of a monitoring effort directed at urban

sewage, to evaluate if this particular organic input is within the system’s coping capability. In

contrast, the low potential of alteration in Gilão estuary likely reflects the proximity to Ria

Formosa, the adjacent lagunar system, that slows the urban development at the

surrounding areas reducing, by consequence, the magnitude of each driving force.

Nevertheless, livestock exploitation more upstream and their consequent organic input to

the estuary should be taken into account. Although this work emphasised drivers of

pressure that can not be compared with other works (e.g. livestock and hidromorphological),

the main drivers considered here (population density, agricultural) are common sources of

impact already considered by Borja et al. (2006) for small estuaries within the Basque

country.

In coastal environments, three systems collide: the socio-economic system, the

geomorphologic system and the ecosystem (McFadden and Green, 2007). As a result, all

five studied systems have some degree of anthropogenic pressure, as measured in the

magnitudes of the observed driving forces, and cannot be considered in a pristine condition

even though some systems (Mira, Odeceixe and Aljezur) are inserted in a protected area. A

sustainable management of sources of pressure is therefore imperative in order to maintain

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the functional proprieties of these systems, not only concerning biological communities

(Cardoso et al., 2011) but also human populations that inhabit and use these watersheds.

For small Portuguese estuaries, such as the ones considered in this study, with the

exception of Mira estuary, this has not been a priority until now, probably due to their

discrete coastal disposition and distance from important centres of administrative and

scientific resources. Nevertheless, since an estuary’s response to land and resource use is

a function of both the magnitude of the disturbance and of the estuary’s sensitivity to the

disturbance, small estuaries are more likely to demonstrate a response to a given

disturbance than large estuaries, assuming other factors are constant, since sensitivity is

determined by the morphometry of the estuary (Meeuwing, 1999).

The three challenges noted by Adger (2006), i.e. measuring vulnerability, treating

perceptions of risk, and addressing governance, have to be set as priorities similarly to the

way that the assessment of estuaries ecological quality is considered in monitoring and

scientific efforts. This approach contributes to ecosystem protection and is a means to attain

the sustainable use of natural resources. The current scarce knowledge on small estuaries

should not be seen as a limitation to their management, instead it should be viewed as a

warning signal of their potential degradation and risk of disappearance (functionally, even if

not structurally). If systems vulnerability is underestimated, areas that are threatened can be

overlooked and their conservation values are at risk of being reduced or eliminated (Wilson

et al., 2005).

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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McFadden, L., Penning-Rowsell, E., Nicholls, R.J. (eds.), Managing Coastal Vulnerability,

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Zacharias, M.A., Gregr, E.J., 2004. Sensitivity and vulnerability in marine environments:

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Zonta, R., Guerzoni, S., Pérez-Ruzafa, A., de Jonge, V.N., 2007. Measuring and

managing changes in estuaries and lagoons: morphological and eco-toxicological aspects.


PART 5

General discussion and final remarks

CHAPTER 7


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In this work we have focused on some relevant aspects of estuarine ecology having the

small estuarine systems of the Portuguese coast as case study. The broad scale of the

analyses performed here challenged the necessary detail of knowledge contribution.

Nevertheless, with the limited published studies based in almost all the systems object of this

work, and the urgent need of information that could contribute to their functional maintenance

and support their environmental management, we believe that the main goals of this study were

achieved.

The first step for environmental management is to understand the ecological function of

such systems and to have some degree of knowledge on their biological communities. Ideally,

this would be a holistic approach, which is very difficult, if not impossible, to achieve in a broad

ecological scale of analyses. For these reasons we choose fish and macroinvertebrates

communities within the estuarine ecological compartments as fundamental indicators of

systems function, role and integrity.

Fish communities have been considered as useful ecological indicators (e.g. Lobry et al.,

2003; Franco et al., 2008) and were analyzed here to establish the ecological role of the five

small estuaries for adjacent coastal environment and their contribution for coastal fish

communities. Within the studied estuaries, these communities were dominated by a small

number of species, the majority 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). The analyses based on ecological guilds showed these systems are mostly used

as temporary habitats by fish, as their feeding and shelter grounds, presenting guilds’

composition similar to those of estuaries with contrasting dimensions, such as Tejo (Costa et

al., 2007; Neves et al., 2008) and similar dimensions, such as the French estuaries of Canche,

Authie and Somme (Selleslagh et al., 2009).

Once established estuaries’ ecological role, the analyses of the main environmental factors

that are responsible for fish communities’ structuring becomes a fundamental step to recognize

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the main natural drivers responsible for that structuring. Within the studied systems, as in other

estuaries (e.g. Blaber and Blaber, 1980; Gordo and Cabral, 2001; Pombo et al., 2007; França et

al., 2008; Selleslagh and Amara, 2008), seasonal variations were found to be the main drivers

for community structure, independently of the approach used to analyse fish assemblages:

diversity, species’ composition, and ecological and feeding guild distribution.

For benthic macroinvertebrates’ communities, we addressed three main scales of

distribution - inter and intra-estuarine patterns, and seasonal heterogeneity. Our results are in

agreement with previous studies (e.g. Teske and Wooldridge, 2003; Gladstone et al., 2006)

supporting that, at the inter-estuarine scale, sediment composition is a major factor for benthic

communities. Nevertheless, when indicator taxa are present in the assemblages, one must take

into account the importance of other potential driving forces such as pollution and salinity

ranges. At a smaller scale, sediment composition between sectors of each estuary was not a

major factor driving the distribution of assemblages. Furthermore, the factors that rule benthic

distribution are probably not the same in the different systems. In agreement with the findings of

Hewitt and Thrush (2009), our results showed that, within estuarine scales of distribution, there

must be complex relationships between spatial variability and abundances of species operating

at a variety of spatial and temporal scales, that do not represent a simple power law of those

operating at broader scales. Further detailed studies, within a wider temporal scale would be

necessary to accurately assess the main drivers that contribute to macroinvertebrates

communities’ structure within each system.

Based on these results it was possible to choose, for each community, the applicable tools

for the assessment of the ecological quality of each system. Seasonality and sediment features

are, in this way, factors that have to be considered for the application of the available indices

(based on fish and macroinvertebrates communities) and for the settlement of the systems’

reference conditions. Nevertheless, with no sufficient knowledge on fish and macrobenthic

potential communities previous to anthropogenic pressures acting in the subject systems, we

based our ecological quality assessment on systems distinctness using indices outputs only for

comparative purposes, analysing in greater detail the behaviour of their individual metrics. For

this assessment we previously established the level of pressure through the quantification of the

magnitudes of a selection of driving forces of impact.

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Three classes of pressure levels among the five analysed estuaries could be distinguished:

very low pressure, identified in Odeceixe and Aljezur estuaries; low pressure, within Mira and

Gilão estuaries; and medium pressure in Bensafrim estuary. Despite presenting similar levels of

pressure, the main driving forces acting among systems differed: in Mira estuary, agricultural

exploitation, aquaculture production and intensity of port developments are the main sources of

impact while in Gilão estuary considerably high levels of urban development represents the

main source. In view of these results, Odeceixe and Aljezur estuaries probably have a lower

impact level from the analysed anthropogenic activities, whereas Mira and Gilão present a

medium level of impact and Bensafrim likely suffers the highest anthropogenic impacts.

With some limitations detailed along chapter 3, it was possible, to some degree, to infer

about the systems’ ecological conditions. Our results showed that metrics seem to be more

informative than the indices based on them, similarly to that observed by Jordan and Vaas

(2000). Based on indices’ analyses, for both fish and macroinvertebrate communities, it was

possible to acknowledge that Mira and Aljezur estuaries showed a higher ecological integrity

than Odeceixe, Bensafrim and Gilão estuaries. Nevertheless, for systems with similar

morphologies and overall levels of impact, such as Aljezur and Odeceixe, the differences in

their ecological integrity found in the analyses are probably a consequence of the high natural

variability inherent to these systems. This fact highlights the issue raised by Elliott and Quintino

(2007) with the concept of the “Estuarine Quality Paradox”.

The development of indices such as those applied in chapter 3 is of an high importance, not

only for the ecological quality assessment but also for the amount of valuable information that

they were able to reveal. It is undeniable that the actual approaches have raised important

questions about scientific knowledge on estuaries and their ecological communities.

Nevertheless, and recognizing that taking small ecosystem compartments and interpreting them

without any reference to their interaction is probably not the best approach for all systems (e.g.

Diaz et al., 2004), new methodologies should now be tested. A more integrative tool should be

developed to include factors that have been discarded from currently used methodologies, such

as systems dimensions, mouth openings and plant cover within systems, all extremely

important for community structure and overall diversity which clearly depends on environment

stability (Dye and Barros, 2005). Thus, the common biological indicators are measuring the

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degree of structure of a given assemblage, but do not integrate their structure and functions (de

Jonge, 2007).

Finally, the ultimate goal of environmental management is to prevent further deterioration of

natural systems by the settlement of priorities of actions in order to mitigate, reduce and prevent

unbalanced uses of natural resources (e.g. Adger, 2006). This setting of priorities is achieved by

the vulnerability analysis, which not only identifies the most vulnerable communities, habitats

and ecosystems but is also able to clarify the most important factors contributing to their

vulnerability (e.g. Halpern et al., 2007; Ippolito et al., 2010; De Lange et al., 2010). Given the

results of the assessment made in the present study, Bensafrim estuary was considered as the

one at greatest risk of alteration, and several priorities were established for each system: for

Mira estuary, monitoring effort and management of the agricultural sources of pressure are

advised; for Odeceixe and Aljezur estuaries, it would be important to reduce barriers to water

flow, or at least, to implement local measures to avoid an increase of water harvesting; for

Bensafrim estuary, the high potential of alteration should be translated into measures that

mitigate the impact of urban and hydromorphological pressures, prioritizing a monitoring

scheme that would enable understanding if urban sewage has the optimal treatment system,

and if this particular organic input is within the system’s coping capability; for Gilão estuary, with

actual low levels of risk of alteration, a close observation of the livestock exploitation should be

taken into account since these farms act as pressure sources upstream, with a consequent

organic input at the estuary.

This work reflected the actual need of further scientific knowledge on estuarine ecology.

The urgency for the development of tools for quality assessment and environmental

management surpassed to some degree our capability to understand estuarine systems and

their biological communities. Small estuarine systems have been excluded from monitoring

efforts on the scope of Water Framework Directive but this does not mean that their importance

is negligible. By the contrary, these systems have undeniable ecological importance in the

Portuguese coast and can be valuable sources of information on fish and macroinverterates

communities. Their small dimensions and high levels of natural variability on a wide range of

sources provide the rare opportunity for community research in environments were several

gradients interact in a short spatial scale. Further research on communities’ structure is

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necessary not only to understand their main driving forces, but to identify these driving forces

given an estuarine system in which knowledge is still to obtain. This should be a necessary

ground for ecological research with the updated need to outline scenarios by environmental

change due to increasing anthropogenic impact. The need for further research on ecological

quality assessment was also highlighted. More integrative tools should be developed, not

necessarily meaning the development of new indices with different combinations of similar

metrics. Tools that allow the inclusion of the information required by the actual indices,

combining them with other important ecosystem features should be tested.

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Akin, S., Buhan, E., Winemiller, K.O., Yilmaz, H., 2005. Fish assemblage structure of

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Blaber, S.J.M., Blaber, T.G., 1980. Factors affecting the distribution of juvenile estuarine

and inshore fish. Journal of Fish Biology 17, 143–162.

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de Jonge, V.N., 2007. Towards the application of ecological concepts in EU coastal water



assessmnent- a review and perpectives. Science of the Total Environment 408, 3871–3879.

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with stress?. The Open Ecology Journal 2, 37–46.

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basin study. Science of the total Environment 408, 3880–3890.

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Jordan, S.J., Vaas, P.A., 2000. An index of ecosystem integrity for northern Chesapeake

Bay. Environmental Science and Policy 3, 59–88.

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161

Agradecimentos

A todas as pessoas que contribuíram para este trabalho, expresso o meu profundo

agradecimento, especialmente:

Ao Professor Henrique Cabral, pela orientação plena em todas as fases dos últimos anos, pela

motivação objectiva, amizade e confiança que transformaram ideias e ideiais em metas

possíveis e alcançáveis.

Ao Professor Luís Cancela da Fonseca, pela orientação franca, presente e fundamental desde

o início da minha incursão na ciência, e que, pelas inúmeras e longas tertúlias orientadoras

transformou esta oportunidade de investigação numa experiência de vida.

Tive o privilégio de ter uma orientação completa e complementar à vida fundamental para um

crescimento contínuo com pontos de partida renovados a cada etapa ultrapassada. Este foi um

projecto que teve o seu início numa conversa, que passou a ideia, que se transformou em

perguntas sucessivas que levantaram outras, sempre de uma forma orientada por dois

Professores na efectiva essência do que entendo por Professor. Para além de um termo ou

título é sobretudo um conceito e uma forma de ser.

À Professora Maria José Costa pela oportunidade de integrar a equipa de zoologia marinha do

Centro de Oceangrafia, FCUL.

Aos co-autores Drª. Sofia Henriques e Dr. Miguel Pessanha Pais, que abraçaram este projecto

com uma energia incrível, boa disposição e objectividade científica. Vestiram a camisola pela

causa dos pequenos estuários e ajudaram-me a ver obstáculos como desafios. Não houve

açude que limitasse a navegação, não houve cansaço que limitasse a boa disposição, não

houve eco em vale nenhum que impedisse a força de expressão.

À co-autora Doutora Susana França que me apoiou em partes fundamentais na minha primeira

incursão pelas associações de peixes. A sua boa disposição, calma e a forma como fez com

que houvesse solução para cada desafio foram, para mim, também uma aprendizagem.

A todos os colegas de grupo e laboratório, que partilharam comigo horas e horas, com muita

paciência, amizade e entre-ajuda fundamentais, especialmente à Doutora Célia Teixeira, Dr.

Joana Oliveira e Dr. Maria Paula Serafim.

162

Aos colegas Doutora Rita Vasconcelos, Doutora Vanessa Fonseca, Doutora Joana Marques,

Doutora Susana França, Drª. Susanne Tuner, Drª Marisa Batista, Drª Sofia Henriques, Dr.

Miguel Pessanha Pais, Dr. Patrick Reis-Santos, pelo apoio em todas as fases da vida ao longo

destes anos, pela amizade, pelo trabalho verdadeiramente de equipa, pela discussão contínua

e troca de ideias, pela revisão de manuscritos, pela crítica sempre objectiva e construtiva que

fazem de cada trabalho individual uma verdadeira causa de grupo.

A todos os amigos, sempre presentes das mais variadas formas, pelo apoio, multiplicação de

ombros, mãos e braços, pelas simples palavras mas também pelos silêncios e partilhas, que

tornam a vida mais real quando é vivida, especialmente à Joana, Teresa, Sofia, Susana,

Miguel, Pedro e Catarina.

A toda a minha família, por embarcarem comigo em todas as aventuras e por me lançarem

noutras, pelo apoio incondicional, pela cumplicidade, pela estrutura fundamental que me dá

confiança a cada dia que passa. Ao João e à Guidinha por falarem a minha língua esquisita

que aprendo e aprendi com eles.

Aos meus avós, por me fazerem brilhar aos seus olhos e me darem a confiança de que

continuar é possível e acreditar que todo o esforço vale a pena. E sobretudo, por me fazerem

reconhecer em mim que a prioridade são os afectos, demostrando-me vezes sem conta que a

vida é muito maior que os dias que passam. Crescer com eles é querer ser mais e melhor, sem

nunca perder o sentido de humor a cada recuo.

Ao meu irmão, meu melhor amigo. Não há palavras suficientes para expressar o que é tê-lo

comigo, e o que foi partilhar com ele os últimos anos. Deu-me, em conjunto com a Xana, a

alegria maior e soberana, o Pedrinho.

Aos meus pais, pelos quais e com os quais expresso o meu profundo amor. Dão a duas

pessoas a alegria de serem irmãs uma da outra, e a mim, a vantagem de ser a irmã mais nova.

Dão-me a confiança, o exemplo de afecto, humanidade, respeito incondicional, observam-me

com paciência nos devaneios e depois amparam o caminho seja ele qual for. Dão-me tudo.

Acreditam em mim, e eu acredito neles. Partilhamos a cumplicidade centífica, e isso ensina-me

sempre que a humildade é a porta que se abre para aprender e descobrir o que se vai

conhecendo. Não há distância, no tempo e no espaço que me faça sentir a sua ausência

mesmo quando a saudade se apodera de mim.

doctoral dissertation in biology (especialidade biologia...

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